The Subcommissural Organ: Key Words

MICROSCOPY RESEARCH AND TECHNIQUE 41:98123 (1998)
The Subcommissural Organ

ESTEBAN M. RODRIGUEZ,* SARA RODRIGUEZ, AND SILVIA HEIN
Instituto de Histologa y Patologa, Facultad de Medicina, Universidad Austral de Chile, Valdivia, Chile
KEY WORDS subcommissural organ; glycoproteins; Reissners fiber; cerebrospinal fluid

ABSTRACT The subcommissural organ (SCO) is a phylogenetically ancient and conserved
structure. During ontogeny, it is one of the first brain structures to differentiate. In many species,
including the human, it reaches its full development during embryonic life. The SCO is a glandular
structure formed by ependymal and hypendymal cells highly specialized in the secretion of proteins.
It is located at the entrance of the aqueduct of Sylvius. The ependymal cells secrete into the ventricle
core-glycosylated proteins of high molecular mass. The bulk of this secretion is formed by
glycoproteins that would derive from two different precursors of 540 and 320 kDa and that, upon
release into the ventricle aggregate, form a threadlike structure known as Reissners fiber (RF). By
addition of newly released glycoproteins to its proximal end, RF grows caudally and extends along
the aqueduct, fourth ventricle, and the whole length of the central canal of the spinal cord. RF
material continuously arrives at the dilated caudal end of the central canal, known as the terminal
ventricle or ampulla. When reaching the ampulla, the RF material undergoes chemical modifica-
tions, disaggregates, and then escapes through openings in the dorsal wall of the ampulla to finally
reach local blood vessels. The SCO also appears to secrete a cerebrospinal fluid (CSF)-soluble
material that is different from the RF material that circulates in the ventricular and subarachnoidal
CSF. Cell processes of the ependymal and hypendymal cells, containing a secretory material,
terminate at the subarachnoidal space and on the very special blood capillaries supplying the SCO.
The SCO is sequestered within a double-barrier system, a bloodbrain barrier, and a CSF-SCO
barrier. The function of the SCO is unknown. Some evidence suggests that the SCO may participate
in different processes such as the clearance of certain compounds from the CSF, the circulation of
CSF, and morphogenetic mechanisms. Microsc. Res. Tech. 41:98123, 1998. r 1998 Wiley-Liss, Inc.
INTRODUCTION (Oksche, 1969; Olsson 1958a,b). These glycoproteins

The subcommissural organ (SCO) is a small gland escape through the dorsal wall of the terminal ventricle
located in the dorsocaudal region of the third ventricle, to reach local blood vessels (Peruzzo et al., 1987).
at the entrance of the Sylvian aqueduct (Fig. 4). It is a The SCO is an ancient and conserved structure of the
highly differentiated ependyma that covers the ventral vertebrate brain (Oksche, 1961). It is well developed in
aspect of the posterior commissure. Its topographical monkeys and young anthropoid apes. In the human, the
position and its location at the interface between the SCO reaches its full development during fetal life and
cerebrospinal fluid (CSF) and a special and circum- undergoes regression after birth (Oksche, 1969). The
scribed vascular plexus led Hofer (1959) to consider the SCO develops very early in ontogeny, representing one
SCO as one of the circumventricular organs. The SCO of the first brain secretory structure to differentiate
cells are arranged into two layers, ependyma and (Schoebitz et al., 1986).
hypendyma. The ependymal cells release their secre- In 1860, Reissner, anatomist at the University of
tion into the ventricular CSF; the hypendymal cells Dorpat, published a monograph on the microscopic
project processes to the local blood vessels and to the structure of the spinal cord of Petromyzon fluviatilis.
subarachnoidal space (see Leonhardt, 1980; Rodrguez He described a string of 1.5 m in diameter character-
et al., 1992). ized by its high refringence, its extremely regular
The SCO secretes glycoproteins of high molecular shape, and its lying free within the central canal (Figs.
mass (Nualart et al., 1991); the bulk of these glycopro- 2, 3). In 1866, Kutschin confirmed Reissners observa-
teins is released into the ventricle where they condense tions and named the fibrous structure Reissners fiber.
to form a threadlike structure, the Reissners fiber (RF) The first description of what later became known as
(Sterba, 1969). By addition of newly released glycopro- the subcommissural organ was given by Edinger in
teins to its cephalic end, RF grows caudally and extends 1892. Studnicka (1900) called attention to uncommonly
along the aqueduct, fourth ventricle, and the whole tall ependymal cells covering the posterior commissure
length of the central canal of the spinal cord (Leon-
hardt, 1980; Reissner, 1860; Sargent, 1900). At its Contract grant sponsor: National Research Council of Chile; Contract grant
caudalmost end, the central canal becomes dilated, sponsor: Volkswagenwerk-Stiftung Federal Republic of Germany; Contract grant
forming a terminal ventricle, also known as ampulla sponsor: Universidad Austral de Chile.
caudalis (Olsson, 1958b). When reaching the terminal *Correspondence to: Esteban M. Rodrguez, M.D., Ph.D., Instituto de Histo-
loga y Patologa, Facultad de Medicina, Universidad Austral de Chile, Valdivia,
ventricle, RF glycoproteins undergo some chemical Chile.
changes and form a gel mass, known as massa caudalis Received 7 October, 1996; Accepted 1 December 1996
r 1998 WILEY-LISS, INC.

THE SUBCOMMISSURAL ORGAN 99
species, most of these processes originate from the
secretory ependymal cells; in mammals they originate
from both ependymal and hypendymal cells.
The rich vascularization of the SCO was first re-
ported by Pesonen (1940), which was confirmed by
several investigators (see Rodrguez et al., 1992). How-
ever, the only investigation designed to analyze the
vascularization of the SCO was performed by Duvernoy
and Koritke in 1964; this study was confined to domes-
tic mammals.
LINEAGE OF THE SCO CELLS
The glandular structure of the SCO is remarkably
stable throughout the vertebrate phylum. There are,
however, important species variations concerning cer-
tain structural features, such as the neural input and
the expression of molecular markers. Interestingly,
these two features appear to be interrelated.
The use of antibodies against glial and neuronal
markers indicate that the cells of the SCO are glial in
nature. However, many of the results obtained using
these probes are confusing and difficult to interpret.
Thus, whereas the SCO cells of the rat and cat do not
display two typical glial markers, namely, glial fibril-
lary acidic protein (GFAP) and S-100 protein (S-100)
(Chouaf et al., 1989; Didier et al., 1986; Rodrguez et al.,
Fig. 1. First line drawing depicting the subcommissural organ 1989), the SCO of other rodents express GFAP or S-100
(Studnicka, 1900). a: Ammocoetes. b: Petromyzon fluviatilis. (Redecker, 1989). The rat SCO lacks, -enolase, a specific
Fig. 2. First line drawing depicting Reissners fiber (b) in the
neuron enolase; however, when transplanted under-
lumen of the central canal (a) of Petromyzon fluviatilis (Reissner, neath the kydney capsule, the rat SCO does express the
1860). neuronal enolase (Rodrguez et al., 1989). Whereas the
Fig. 3. Reissners fiber (RF) in the central canal (cc) of the spinal
SCO of the rat and cat accumulates gamma-aminobu-
cord of the lamprey Geotria australis. Aldehyde-fuchsin staining. tyric acid by specific uptake mechanisms, the mouse
3900. (From S. Rodrguez et al., 1987). and rabbit SCO does not (Chouaf et al., 1989; Gamrani
et al., 1981). Ontogenetic, transplantation, and denerva-
tion studies have indicated that the expression by the
of Petromyzon fluviatilis and provided the first line SCO cells of one or other cell marker may depend on the
drawing of this structure (Fig. 1). Sargent (1900) was presence or absence of a neural input and on the nature
the first to associate RF with the region of the SCO. His of the transmitter involved (Didier-Bazes et al., 1993).
publication, which includes an amazingly accurate
schematic representation of the SCO-RF complex, rep- Ultrastructure
resents the first leap in the knowledge of the SCO and Ependymal Cells
RF. In 1910, Dendy and Nicholls introduced the term The ependymal layer of the SCO is formed by very
subcommissural organ. high cylindrical cells (Figs. 6, 10, 11). They display an
infolded nucleus with abundant euchromatin and are
GENERAL STRUCTURE located in the basal cell region (Herrlinger, 1970;
The secretory cells of the SCO are arranged into two Stanka et al., 1964). The cell body presents a clear
different layers, the ependyma and the hypendyma. zonation; the following cytoplasmic regions may be
The term hypendyma was introduced by Krabbe (1933) recognized: perinuclear, intermediate, subapical, and
to identify a tissue layer located under the ependyma of apical. The basal process represents another distinct
the SCO, which is characterized by numerous blood area. This zonation is specially marked in certain
capillaries and glial cells with special characteristics. species, such as in the rat, which will be used for the
Ultrastructural and immunocytochemical studies have following description (Fig. 11).
shown that the ependymal and the hypendymal cells Perinuclear Region. The most distinct ultrastruc-
share the same secretory properties. The ependyma of tural feature of the SCO of virtually all species is the
the SCO does not undergo major evolutionary changes; presence of large and dilated cisternae of the rough
the degree of development of the hypendyma may vary endoplasmic reticulum (RER), which may reach a diam-
from a few cells lying under the ependyma in lower eter of 7 m (Herrlinger, 1970; Stanka et al., 1964).
vertebrates to a distinct subependymal layer in some Only about 25% of the surface area of these cisternae
mammals. In many species, hypendymal cells are also is studded with ribosomes, indicating that in each
located within the posterior commissure and in the cisternum the rate of synthesis is low. The big lumen of
vicinity of subarachnoidal space (Figs. 510). the RER is filled with a filamentous material (Fig. 13)
Processes of the secretory cells of the SCO project that is strongly immunoreactive with antibodies against
dorsally to end on local blood vessels or at the external the glycoproteins secreted by the SCO (Fig. 14) (Rod-
limiting membrane of the brain. In nonmammalian rguez et al, 1986). This is in agreement with the
Fig. 4. Scanning electron microscopy of the bovine subcommis- Fig. 6. Scanning electron microscopy of the bovine SCO (upside
sural organ (SCO). SA, aqueduct of Sylvius. 315. down). E, ependymal layer; arrows, ventricular protrusions of ependy-
mal cells. 3350.
Fig. 5. Sagittal section through the bovine SCO immunostained
with an anti-RF serum. E, ependyma; Hy, hypendyma; pc, posterior
commissure traversed by immunoreactive cells. 318.
Fig. 7. Sagittal section of the rat brain immunostained with an Fig. 9. Frontal section of the rat diencephalon immunostained
anti-RF serum. The subcommissural organ (SCO) is selectively stained. with an anti-RF serum. SCO, subcommissural organ. 317.
cc, cerebral cortex; c, cerebellum; p, pineal. Two long arrows indicate
plane of section of the brain shown in Figure 9. 311. Fig. 10. Detailed magnification of the SCO shown in Figure 9. E,
ependyma; Hy, hypendyma; p, immunoreactive basal process. 3150.
Fig. 8. Higher magnification of the epithalamus shown in Figure 7. (From Rodrguez t al., 1984a).
Thick arrow, subcommissural organ; thin arrow, immunoreactive ependy-
mal cell reaching the subarachnoid space; H, habenula; III V, third
ventricle; SA, Sylvian aqueduct. 338. (From Rodrguez et al., 1984a).
exceptional property of these cells to store most of its high. The basal two-thirds of this column correspond to
secretion within the RER rather than in secretory the intermediate region. RER and the Golgi apparatus
granules (Rodrguez et al., 1992). are the main organelles of this region. The RER cister-
Intermediate Region. The cytoplasmic column ex- nae are dilated but smaller that those of the peri-
tending from the nucleus to the ventricle is about 70 m nuclear region (Fig. 11). They are located in the periph-
102 E.M. RODRIGUEZ ET AL.
Fig. 11. Schematic representation of a secretory ependymal cell of material that remains soluble in the cerebrospinal fluid. BP, basal
the rat SCO. The secretory glycoproteins are shown as core- process ending on an expanded area of the perivascular space (PVS)
glycosylated precursor forms stored in RER (1), as complex-type partially filled with long-spacing collagen (LSC). Double arrow, exten-
precursor forms stored in immature secretory granules (2), as pro- sions of the perivascular basal lamina; C, capillary; yellow structures,
cessed N-linked glycoproteins in mature secretory granules, (3) and nerve endings contacting the secretory cell. (From Rodrguez et al.,
after their release in the ventricle where they appear partially packed 1993).
forming pre-RF (4) and densely packed forming RF (5). 6, Secretory
eral cytoplasm surrounding a centrally located Golgi formed by two to three flattened cisternae. Typical
apparatus. The Golgi apparatus is well developed and secretory granules are missing in the vicinity of the
formed by several arrays of elongated cisternae. The Golgi apparatus. The involvement of the Golgi appara-
cis-Golgi is formed by dilated and fenestrated cisternae tus in the secretory process of the SCO has been and
overlooking the RER cisternae. The trans-Golgi is still is a matter of controversy. Many investigators have
presented ultrastructural evidence suggesting that se- In the rat, these terminals contain a mixed population
cretory vesicles derived from the RER would bypass the of round and elongated granules of low electron density
Golgi apparatus and release its secretory content into and that largely differ from the secretory granules
the ventricle; this mechanism would coexist with the present in the ventricular cell pole. The granules in the
classical secretory pathway including the Golgi chan- terminal are not reactive with the antisera against RF
nels (Chen et al., 1973; Murakami and Tanizaki, 1963; glycoproteins, indicating they may contain a material
Oksche, 1969; Papacharalampous et al., 1968; Rod- different from that released into the ventricle. The dog
rguez, 1970a; Stanka et al., 1964). Recent ultrastruc- SCO displays the typical structure of an endocrine
tural immunocytochemistry and lectin histochemistry gland, i.e., a solid mass of secretory cells penetrated by
have not clarified this aspect. numerous blood capillaries (Fig. 12) (Oksche, 1969;
Subapical Region. This is a short region mainly Rodrguez et al., 1984a, 1986). Many of the cells do not
occupied by bundles of microtubules, mitochondria, and reach the ventricle but are in close contact with the
smooth endoplasmic reticulum. A few small RER cister- capillaries; at their vascular pole, these cells present
nae and secretory granules are present (Fig. 11). numerous small granules of high electron density and
Apical Region. Transmission and scanning elec- that are not reactive with anti-RF sera (Rodrguez et
tron microscopy show that each ependymal cell projects al., 1987b). A completely different situation is found in
a large protrusion into the ventricle (Herrlinger, 1970; the bovine SCO. The ependymal cells project short
Krstic, 1975; Stanka et al., 1964; Weindl and Schinko, processes to the numerous intraependymal capillaries;
1975). The cells display a few cilia and numerous these ependymal endings are packed with mitochon-
mitochondria (Leonhardt, 1980). The protrusions are dria and contain very few secretory granules (Isomaki
occupied by microtubules, mitochondria, secretory gran- et al., 1965), which do react with anti-RF sera (Perez et
ules, and spherical RER cisternae. The content of the al., 1995).
granules and the RER is immunoreactive with antibod- The leptomeningeal endings contain, in addition to
ies specific for the SCO secretion (Figs. 15, 16) (Rod- secretory granules and mitochondria, whorllike struc-
rguez et al., 1986, 1987a,b). There are conspicuous tures formed by concentrically arranged RER cisternae
species variations in the number, size, shape, and inner (Fernandez-Llebrez et al., 1987; Oksche, 1969; Rod-
structure of the secretory granules located in the ven- rguez, 1970b). This peculiar arrangement of RER is
tricular cell pole (for references, see Rodrguez et al, found in the perinuclear region of the ependymal cells
1992). of several species. In the bovine SCO, the thin lumen of
The distinct zonation of the SCO ependymal cells, these RER cisternae contain a material immunoreac-
which is also distinguishable at the light microscopic tive with polyclonal and monoclonal antibodies against
level, has facilitated the investigation of the secretory RF glycoproteins (Perez et al., 1995).
process because different phases of this process occur in
discrete but separate areas of the cell, namely, synthe- Hypendymal Cells
sis in the perinuclear and intermediate regions, storage
of precursor forms in the big RER cisternae, processing The hypendymal cells, like the ependymal cells, are
and packaging in the intermediate region, transport in polarized elements. In several species, the apical pole
the subapical region, storage of processed forms, and of a group of these cells is packed by junctional com-
release in the apical region. Furthermore, the SCO plexes, forming rosettelike structures. In the rat, the
offers a unique feature: the secretory material on lumen of these rosettes is only visible under the elec-
release condenses first as a film on the surface of the tron microscope (Rodrguez et al., 1992). In the bovine
organ and then after further packaging into RF (Figs. SCO, the rosettes display a rather large cavity (Isomaki
11, 16). The released material can be visualized in et al., 1965; Olsson, 1958a). The essential ultrastruc-
tissue sections. tural characteristics of the nucleus and cytoplasm of
Basal Processes of the Ependymal Cells. In non- the hypendymal cells is similar to those described for
mammalian species, in which hypendymal cells are the ependymal cells, although the zonation of the
rare, the ependymal cells project long processes that cytoplasm is less evident. The dilated RER cisternae
end on local blood capillaries or, after traversing the are located in the vicinity of the nucleus, and numerous
posterior commissure, end on the dorsal brain surface secretory granules accumulate at the pole lining the
(Figs. 11, 19, 21). These processes contain numerous rosette cavity (Rodrguez et al., 1992). These granules
secretory granules and microtubules (Fig. 22) (Fernan- and the content of the rosette cavity immunoreact with
dez-Llebrez et al., 1987; Rodrguez, 1970b). polyclonal and monoclonal antibodies against RF glyco-
There are large species variations with respect to the proteins (Perez et al., 1995). There is no information on
content of the terminals of the ependymal processes. In the fate of the material secreted into these cavities.
those nonmammalian species investigated, the vascu- The other cell pole of the hypendymal cells is repre-
lar and leptomeningeal endings contained secretory sented by one or two processes ending on local blood
granules and RER cisternae (Fig. 23). Many of the vessels or on the external limiting membrane of the
granules are immunoreactive with antisera against RF brain and is immunoreactive with anti-RF sera (Figs.
glycoproteins; there are secretory granules, especially 10, 12, 21) (Rodrguez et al. 1984a,b). The ultrastruc-
in those ending contacting the leptomeninges, which ture of these processes and their endings is similar to
are not reactive with these antisera (Peruzzo et al., that described for the processes of the ependymal cells.
1990). In mammals, there are large species variations There is a large series of monoclonal and polyclonal
with respect to the content of the ependymal endings. antibodies raised against the secretory proteins ob-
Fig. 12. Sagittal 1-m-thick section of the dog SCO immuno- reaching the subarachnoid space; white rectangle frames an area
stained with an anti-RF serum. c, capillaries in the SCO; P, pineal; III similar to that shown in Figures 13 and 14; black square frames a
V, third ventricle; SA, aqueduct of Sylvius; long arrows, columns of region shown in Figures 15 and 16. 355.
immunoreactive cells traversing the posterior commissure (PC) and
tained from the SCO proper or from RF. All these ing of this space is not known. It has been suggested
antibodies stain in the same way, both the ependymal that its presence is indicative of a leacky bloodbrain
and the hypendymal cells, indicating that at least some barrier (Brightman et al., 1970). In all circumventricu-
of the material secreted by both cell types is similar or lar organs but the SCO, the presence of a perivascular
identical in nature. The relevant difference of these space coexists with a fenestrated endothelium and the
immunoreactive materials is their fate; thus, whereas absence of a bloodbrain barrier. In the SCO, the
that of the ependymal cells is released into the ventricu- endothelium is not fenestrated and has a tight endothe-
lar CSF, that of the hypendymal cells would possibly lium to tracer injected intravascularly (Broadwell and
reach the subarachnoidal CSF. Brightman, 1976; von Bomhard et al., 1974; Weindl and
Joynt, 1973). Thus, despite possessing capillaries with
BLOOD VESSELS AND BARRIERS a perivascular space, the SCO appears to have an
The blood capillaries supplying the SCO have charac- efficient bloodbrain barrier (Bouchaud, 1975; Poirier
teristics that make them unique in the central nervous et al., 1983). This probability does not rule out that
system. A feature characterizing the capillaries of all substances released from the terminals of the SCO
circumventricular organs, including the SCO, is the secretory cells may reach the blood stream. Conven-
presence of a perivascular space. The functional mean- tional transmission electron microscopic (Hofer, 1986)
Fig. 13. Transmission electron micrograph of the dog SCO. For orientation, see rectangle in Figure 12.
G, Golgi apparatus; asterisks, dilated cisternae of the rough endoplasmic reticulum; arrows, secretory
granules. 36,000.
and recent ultrastructural immunocytochemical (Pe- 1963; Stanka et al., 1964; Schwink and Wetzstein,
ruzzo, 1995) studies support this possibility. 1966). To our knowledge, there is no other region in the
Another exceptional characteristic of the SCO capil- central nervous system endowed with long spacing
laries is the presence in the perivascular space of long collagen. The capillaries of the human ciliary body do
spacing collagen (Naumann, 1963; Wetzstein et al., display long spacing collagen. The presence of long
Fig. 14. Dog SCO. Area similar to that shown in Figure 13. Protein apical secretory granules; arrows, released material not yet aggre-
A-gold immunostaining using an anti-RF serum. The content of the gated. 310,000.
dilated cisternae of the rough endoplasmic reticulum (asterisks)
appears labeled. m, mitochondria. 36,000.
Fig. 16. Ventricular cell pole of the dog SCO cells. The apical
Fig. 15. Ventricular cell pole of the dog SCO cells (for orientation, secretory granules (sg) and the pre-RF material (pre-RF) are selec-
see square in Fig. 12). Immunostaining using an anti-RF serum. sg, tively immunostained. c, cilia. 310,000.
spacing collagen could result from the release into the having a poorly developed junction (Gotow and Hashi-
perivascular space of the secretory glycoproteins of the moto, 1982a; Madsen and Mllgard, 1979). The exis-
SCO. Indeed, in vitro formation of long spacing collagen tence of gap junctions is also a matter of discrepancy
may be induced adding glycoproteins to collagen solu- (see Madsen and Mllgard, 1979).
tions (Randall et al., 1953). Furthermore, when the rat The tightness of the SCO-CSF barrier to tracers
SCO was transplated under the kidney capsule, the administered into the ventricle vary with the species.
newly formed blood capillaries that revascularized the Although the existence of a SCO-CSF barrier needs to
grafted tissue became endowed after 1 week with long be investigated further, there is evidence supporting
spacing collagen (Figs. 17, 18) (Rodrguez et al., 1989). the presence of a barrier to large lipid-insoluble mol-
This clearly indicates that the presence of long spacing ecules (see Rodrguez et al., 1992). All the other circum-
collagen in these capillaries was triggered by factors ventricular organs lack a bloodbrain barrier but do
provided by the grafted SCO secretory cells. The clarifi- possess a barrier with the CSF; thus, in these organs
cation of the nature of these factors may help us to the bloodbrain barrier has shifted to the ventricular
understand the function of the SCO. border (Leonhardt, 1980; Rodrguez et al., 1992). How-
The ependymal cells are linked together by tight ever, all brain areas protected by the bloodbrain
junctions and zonulae adherens, which have been iden- barrier are in open communication with the ventricular
tified by conventional and freeze-fracture electron mi- CSF (Leonhardt, 1980). All these considerations lead to
croscopy (Gotow and Hashimoto, 1982a,b; Kimble et al., a surprising conclusion: the SCO is a unique brain
1973; Rodrguez, 1970a). The number of strands at the structure, with its cells being sequestered within a
tight junction varies with the species, with the gerbil double-barrier system whose functional significance is
SCO displaying the tightest junction and the rat SCO absolutely enigmatic.
Fig. 17. Rat SCO grafted under the kidney capsule for 1 month. Fig. 18. Rat SCO 1 week after transplantation under the kidney
Immunostaining with an anti-RF serum. The ependymal (E) and capsule showing the contact between the basal processes of the SCO
hypendymal (H) cells are strongly immunoreactive. Secretory mate- cells (stars) and the perivascular basal lamima (arrows) of a newly
rial is also present in basal processes of the ependymal cells (small formed capillary revascularizing the graft. Long spacing collagen
arrows) and as a loosely aggregated layer on the free surface (large (asterisks) is seen in expansions of the perivascular basal lamina.
arrow). K, kidney. 3230. (From Rodrguez et al., 1989). 316,000. Inset: Detailed magnification of long spacing collagen
(arrows). 320,000. (From Rodrguez et al., 1989).
NATURE OF THE SECRETORY PRODUCTS also used for the demonstration of neurosecretion. This
Histochemistry observation in the frog was soon confirmed and ex-
The first report on the existence in the SCO of a tended to several species (for references, see Rodrguez
secretory stainable material was published by Stutin- et al., 1992). The secretory material of the SCO is also
sky in 1950 by applying the Gomori method that was stainable with the periodic acid-Schiff method (for
references, see Ziegels, 1976). Several histochemical and with RF (Figs. 710). They immunostained the
test led to the conclusion that the secretion of the SCO SCO of all vertebrate classes, from cyclostome to mon-
is a glycoprotein or a mucopolysaccharide-protein com- keys (Rodrguez et al., 1984a; S. Rodrguez et al., 1987;
plex (Diederen, 1970; Naumann, 1968; Oksche, 1962). Sterba et al., 1982). The SCO of anthropoid apes and
Olsson (1958a) indicated that the secretion of the human fetuses were completely negative with these
bovine SCO must be rich in sialic acid, perhaps in the antisera (Rodrguez et al., 1984a). Antisera raised
form of a syalilated protein. Autoradiographic investiga- against bovine RF glycoproteins after an irreversible
tions after the administration of radioactive cisteine cleavage of the disulfide bonds by alkylation or after
and cystine have shown that the SCO and the RF alkylation and deglycosylation are strongly reactive
become strongly labeled (Diederen et al., 1987; Er- with the bovine SCO-RF complex, but do not react with
misch, 1973; Leatherland and Dodd, 1968; Rodrguez et the SCO of other species, indicating that the conserved
al., 1992; Sterba et al., 1967b). In brief, all the histo- epitope is conformational in nature (Nualart and Rod-
chemical studies have indicated that the secretory rguez, 1996). Polyclonal antibodies have also been
material of the SCO is a carbohydrateprotein complex raised against extracts of the SCO proper (Grondona et
(or a complex of glycoproteins) with a high content of al., 1994a; Karoumi et al., 1990; S. Rodrguez et al.,
cysteine and sialic acid. 1985) or against specific glycoproteins collected from
preparative gels of SCO extracts (Lopez-Avalos et al.,
1995; Nualart et al., 1991). These anti-SCO sera
Lectin Histochemistry stained the SCO and the RF. Monoclonal antibodies
Meiniel and Meiniel (1985) were the first to report on have been obtained by using immunogen on the bovine
the lectin binding properties of the SCO. They con- SCO (R. Meiniel et al., 1988) and the bovine RF (Perez
cluded that the secretion of the SCO is rich in mannosyl et al., 1995). Ultrastructural immunocytochemistry
residues. The combined use of immunocytochemistry using polyclonal and monoclonal antibodies has demon-
(anti-RF serum), lectins, and specific glycosidades ap- strated strong labeling of the secretory material located
plied in sequence to the same sections led to the in the dilated RER cisternae (Figs. 15, 16) and the
following conclusions: (1) the secretory products within secretory granules located at the apical cell pole (Gron-
the RER are N-linked, high-mannose-type glycopro- dona et al., 1994b; Losecke et al., 1984; Perez et al.,
teins; (2) the products within the apical secretory 1995; Peruzzo et al., 1990; Rodrguez et al., 1986,
granules are N-linked, complex-type glycoproteins, with 1987a,b) and in the vascular and leptomeningeal epen-
the sequence in the terminal chain of -GlcNac-Gal- dymal endings (Peruzzo et al., 1990; Rodrguez et al.,
sialic acid; and (3) the apical secretory granules and the 1987b). There are monoclonal antibodies that react
pre-RF material share the same immunocytochemical with the secretory granules but not with the RER
and lectin binding properties (Fernandez-Llebrez et al., content (Perez et al., 1995).
1987; Grondona et al., 1994b; Herrera and Rodrguez,
1990; Nualart et al., 1991; A. Meiniel et al., 1988; R. Biochemistry of Reissners Fiber Glycoproteins
Meiniel et al., 1990; Rodrguez et al., 1986, 1987b, 1990; Studies with the bovine RF using electrophoretic
S. Rodrguez et al., 1987). Ultrastructural lectin histo- analysis under nondenaturating conditions led Wolf
chemistry has confirmed these observations (Grondona and Sterba (1972) to conclude that the bovine RF is
et al., 1994b; A. Meiniel et al., 1988; Peruzzo et al., made up of a fibrous glycoprotein of high molecular
1990; Rodrguez et al., 1986). Core glycosylation of the weight and a second one of low molecular weight
SCO glycoproteins was confirmed by the disappearance associated to the first one by nonconvalent links. Immu-
of the Con-A binding sites after the in vivo administra- noblotting employing polyclonal antibodies raised
tion of tunicamycin (Herrera and Rodrguez, 1990). against secretory products of the bovine SCO has been
Partial sequencing of a RF glycoprotein has shown used to identify the secretory compounds present in the
several cryptic sequencies for N-glycosylation (Nualart bovine SCO and RF (Hein, 1988; Nualart et al., 1991;
et al., 1995). Deglycosylation of the RF glycoproteins by Rodrguez et al., 1987b, 1990). Four secretory glycopro-
endoglycosidase F leads to a decrease in their molecular teins were consistently found in the SCO with molecu-
mass of 1525% (Nualart and Rodrguez, 1995). This lar weight of 540, 450, 320, and 190 kDa. Another
result agrees with the first chemical estimates made by polypeptide, of 50 kDa, was detected only in some
Hadge and Sterba (1973) that the RF consists of 80% extracts. Immunoreactive bands of 450, 300, 230, 190,
proteins and 16% carbohydrates. 145, and 89 kDa were identified in RF extracts (Nualart
et al., 1991). R. Meiniel et al. (1991) used a monoclonal
Immunocytochemistry antibody to purify by affinity chromatography the secre-
tory products of the bovine SCO and then identified
The RF may be regarded as a pure secretory product these products by lecting binding on Western blots.
of the SCO. Thus, by isolating RF, a pure SCO secretion They recognized three glycopeptides of 84, 54, and 34
may be obtained. RF is readily obtained by perfusing kDa. These results are not in agreement with those
the central canal of the bovine spinal cord. After the reported by Nualart et al. (1991).
isolation of RF, the solubilization of the RF glycopro- Secretory glycoproteins of high molecular mass (in
teins has been obtained by using various extraction the range of 400600 kDa) have been detected by
procedures. Sterba et al. (1982) and Rodrguez et al. immunoblotting in the SCO of the dogfish (Grondona et
(1984a) raised polyclonal antibodies (anti-RF sera) and al., 1994b; Lopez-Avalos et al., 1995) and the SCO of
used them for immunocytochemical studies of the chick embryos (Didier et al., 1995).
SCO-RF complex of several species. These antisera Studies of the SCO secretions using molecular biol-
react specifically with the secretory material of the SCO ogy tools have recently been started. Meiniel et al.
(1995) obtained a cDNA insert of 0.4 kb from a clon probability, precursor forms because they bind Con A
identified with anti-RF serum and used it as a probe for but not LFA and they are present in the SCO and
an in situ hybridization study. Nualart et al. (1998) missing in RF. The anti-540-kDa serum reacts in the
cloned and sequenced a bovine SCO cDNA of 2.5 kb; by dog SCO with the RER content but not with the
performing a Northern blot analysis, these researchers secretory granules. (2) The 450- and the 190-kDa
identified a large size mRNA (.9.5 kg) encoding for a compounds display all properties of processed forms,
RF glycoprotein. This result supports those immuno- namely, they bind Con A and LFA, and they are present
blot findings indicating that the SCO does produce high in the SCO and RF. Furthermore, the anti-320-kDa
molecular mass glycoproteins. protein serum reacts with the 190-kDa polypeptide but
CSF-Soluble Secretory Material not with the 450-kDa polypeptide, suggesting that both
processed forms originate from different precursors.
The bulk of the secretion released by the SCO into the This possibility is supported by comparative immunocy-
ventricle becomes packed to form RF (see Leonhardt, tochemical findings: the anti-540-kDa protein and anti-
1980; Rodrguez et al., 1992). There is evidence that 450-kDa protein sera strongly react with the bovine
part of the SCO secretion released into the CSF re- and dog SCO but not with the rat SCO; the anti-320-
mains soluble. Under certain physiological conditions, kDa protein serum reacts with the SCO of bovine, dog,
such as the embryonic period (chicken, rat, and human) and rat.
and under specific experimental conditions, such as The existence of high-molecular-weight precursor
hydrocephalus, the SCO would secrete CSF-soluble and processed forms has been described in two other
compounds that do not form an RF, although they react species. The lectin binding properties of the secretory
with anti-RF sera (Irigoin et al., 1990; Rodrguez et al., compounds of the dogfish SCO, reported by Lopez-
1993; Schoebitz et al., 1993). Avalos et al. (1995), point to a 600-kDa compound as a
In the ventricular and subarachnoidal CSF of adult precursor form and to 475-, 400-, and 145-kDa polypep-
rabbits, soluble compounds immunoreactive with tides as processed forms. Similarly, a 390-kDa immuno-
anti-RF sera were detected by ELISA and immunoblot- reactive compound, identified by Didier et al. (1995) in
ting (Jara, 1995; Rodrguez et al., 1993). The SCO of the
the chick embryo, exhibited affinity for Con A and
adult rabbit would secrete both CSF-insoluble (RF-
wheat germ agglutinin (affinity 5 glucosamine and si-
material) and CSF-soluble compounds. Lehmann and
alic acid).
Sterba (1993), using ELISA, detected RF-immunoreac-
tive compounds in the culture medium of bovine SCO The carbohydrate moeity of the SCO secretory glyco-
explants. proteins also undergoes processing. These glycopro-
Furthermore, there is evidence that the SCO may teins are N-linked, high-mannose type while stored in
secrete CSF-soluble compounds different from RF glyco- the RER and become processed to complex-type glyco-
proteins. Antibodies raised against CSF-specific glycoproteins when they are packed into secretory granules
proteins (glycoproteins present in the CSF but missing (Diederen et al., 1987; Herrera and Rodrguez, 1990).
from the plasma) obtained from the CSF of hydroce- In most species, the relatively small pool of secretory
phalic children react with the human and rat SCO granules concentrates in the ventricular cell pole, just
(Montecinos, 1995; Rodrguez et al., 1993). distal to the subapical region, containing a large num-
The detection of CSF-soluble secretory material in ber of microtubules (Rodrguez et al., 1992). No apical
the CSF of the lateral ventricle and cisterna magna secretory granules occur in the SCO of rats after
(Rodrguez et al., 1993) indicates that such a material colchicine has been injected into the CSF (Rodrguez et
circulates in the ventricular and subarachnoidal CSF. al., unpublished observations). Processing and trans-
Because both CSF compartments are in open communi- port of granules to the ventricular cell pole appear to be
cation with the brain tissue, the SCO-soluble secretion interrelated phenomena.
could reach any region of the central nervous system, Synthesis, processing, transport to the ventricular
with the exception of the other circumventricular or- cell pole, and release of the secretion occur in approxi-
gans. mately 1 hour (Herrera, 1988; Rodrguez et al., 1990,
1992). In contrast, 4 days after injection of 35S-cysteine
BIOSYNTHESIS OF THE REISSNERS into the ventricular CSF of the rat, the label is still
FIBER GLYCOPROTEINS found in the RER and the most proximal part of RF.
Blots of bovine SCO and RF have been processed for This result and results obtained with intraventricu-
immunostaining with anti-RF sera and for binding of larly injected tunicamycin (Herrera and Rodrguez,
Con A (affinity 5 mannose and glucose) and Limax 1990) indicate that a pool of the secretion is stored
flavus agglutinin (LFA; affinity 5 sialic acid). Con A within the RER for several days after its synthesis.
identifies N-linked glycoproteins; LFA identifies glyco- This deposit would be slowly and continuously trans-
proteins that have not passed (negative binding) or that ported and released into the ventricle. This property
have passed (positive binding) through the Golgi appa- and the fact that, in the SCO, the RER is the main
ratus. This type of analysis and the raising of antibod- storage site of the secretion characterize the SCO as a
ies against each of the three major compounds of the rather unique type of gland. Grondona et al. (1994b)
bovine SCO (540, 450, and 320 kDa) and the use of described, in the dogfish S. canicula, typical apical
these antibodies in a comparative immunocytochemical secretory granules and lysosomelike granules located
study have allowed us to draw some important conclu- in the supranuclear region that react with an anti-RF
sions (Hein, 1988; Hein et al., 1993; Nualart et al., serum. They suggested that some of the glycoproteins
1991; Rodrguez et al., 1987a, 1992). (1) The 540- and synthetized by the SCO (incorrect folding?, incorrect
the 320-kDa immunoreactive glycoproteins are, in all glycosylation?) would be transported to lysosomes.
Fig. 19. Schematic representation of the anuran SCO. I, Ventricu- Fig. 20. The SCO-RF complex of anurans. 1, Subcommissural
lar cell pole of the ependymal cells displaying numerous secretory organ; 2, Reissners fiber; 3, massa caudalis; 4, ampulla caudalis; 5, RF
granules (AG); pre-RF material and Reissners fiber (RF); II, central material escaping through the dorsal wall of the ampulla; 6, vascular
portion of ependymal cells; III, basal pole of ependymal cells projecting projections of secretory cells; 7, leptomeningeal projections of secre-
basal processes ending on the external basal lamina of the brain (BL) tory cells; 8, meningeal capillary. (From Oksche, 1969).
and on blood vessels (6). Basal processes show (1) accumulation of
secretion, (2) local swellings, (3) saclike accumulations of granules, (4)
varicosities, and (5) vacuoles. 8, Extraependymal bipolar secretory
cell; PT, pineal tract; k, capillary. (From Oksche, 1961).
SITES OF RELEASE Subarachnoidal (Leptomeningeal)

OF THE SECRETORY PRODUCTS Cerebrospinal Fluid
Ventricular Cerebrospinal Fluid The ependymal cells in nonmammalian species and
The ependymal cells of the SCO release the major the hypendymal cells in mammals project basal pro-
part or the whole bulk of their secretory material to the cesses terminating on the dorsal brain surface (Fernan-
ventricular CSF. Some of the released material con- dez-Llebrez et al., 1987; Hofer, 1958; Murakami and
denses to form RF (Figs. 11, 19, 20, 24) (Sterba, 1969). Tanizaki, 1963; Oksche 1954, 1956, 1961, 1962, 1969;
In this respect, the most convincing evidence has been Rodrguez, 1970a; Rodrguez et al., 1984a,b). In the
obtained from immunocytochemical investigations. In- terminals of these processes, there are secretory gran-
deed, antibodies raised against RF glycoproteins react ules with immunocytochemical and lectin binding prop-
specifically with the secretory material of the SCO erties similar to those of the secretory granules located
(Perez et al., 1995; Rodrguez et al., 1984a; Sterba et al., at the ventricular cell pole (Peruzzo et al., 1990). After
1981, 1982). In contrast, antibodies against secretory lesion of the leptomeningeal processes, Oksche (1962)
products extracted from the SCO immunostain the RF found an accumulation of secretory material in the
(Grondona et al., 1994a; Karoumi et al., 1990; R. proximal stump of the transected process. Biosynthetic
Meiniel et al., 1988; S. Rodrguez et al., 1985). labeling has shown that labeled secretion may be found
Furthermore, some of the secretion released into the at the ependymal ending 2 hours after the administra-
ventricle would remain CSF soluble (Rodrguez et al., tion of the radioactive precursor (Herrera and Rod-
1993; see CSF-Soluble Secretory Material). rguez, unpublished observation). Transport of secre-
Fig. 21. Section of the SCO of the toad Bufo arenarum H. basal processes (arrow). N, cell nucleus; PT, pineal tract. 310,000.
immnostained with an anti-RF serum. Rectangle frames area similar (From Rodrguez 1970b).
to that shown in Figure 22; square indicates area shown in Figure 23.
Arrows, pre-RF material. 3110. (From Rodrguez et al., 1984a).
Fig. 23. Secretory processes of the toad SCO cells ending on the
Fig. 22. Transmission electron microscopy of the toad SCO (for external basal lamina of the brain (elm) (for orientation see rectangle
orientation, see rectangle in Fig. 21). Numerous secretory granules in Fig. 21). sg, Secretory granules; d, desmosome. 316,000. (From
(sg) are seen in the basal region of the ependymal cells and along the Rodrguez 1970b).
tory granules along the basal processes and their a close relationship with the local blood capillaries
accumulation at the terminals suggest that a release (Fernandez-Llebrez et al., 1987; Hofer, 1986; Legait,
into the subarachnoidal (leptomeningeal) CSF may 1949; Murakami and Tanizaki, 1963; Oksche, 1961,
occur. This could be the source of the soluble secretory 1969; Palkovits, 1965; Papacharalampous et al., 1968;
material detected in the subarachnoidal CSF (see CSF- Rodrguez, 1970b; Tulsi, 1983). These processes and
Soluble Secretory Material). their vascular endings contain granules immunoreac-
tive with anti-RF sera (Rodrguez et al., 1984b; Peruzzo
Blood Vessels of the Subcommissural Organ et al., 1990). Furthermore, RF-immunoreactive mate-
Ependymal and hypendymal cells, either through rial has been detected in large intercellular spaces
their basal region or through basal processes, establish located in the vicinity of the blood capillaries (Losecke
Fig. 24. Scanning electron micrograph of Reissners fiber (RF) isolated from the bovine spinal cord.
33,000.
et al., 1986; Rodrguez et al., 1987a) and in the perivas- vesicles of the endothelial cells of the dog SCO (Peruzzo,
cular space proper (Losecke et al., 1986). RF-immunore- 1995). All these findings support the view that the SCO
active material has been detected within transcytosis secretes into the blood a material that is recognized
Fig. 25. Reissners fiber (RF) of the lamprey Geotria australis. Fig. 26. Reissners fiber (RF) in the central canal (cc) of the rat
Immunoperoxidase staining using an anti-bovine RF serum. cc, cen- spinal cord, visualized after injection of peroxidase into the lateral
tral canal; E, ependyma of the central canal. 320,000. (From Peruzzo ventricle. DAB-H2O2 reaction, Vibrotome section. 3400. (Courtesy M.
et al., 1987). Cifuentes).
with anti-RF sera. However, in the dog SCO there are Pre-Reissners Fiber Stage
numerous perivascular secretory cells containing gran- The newly released RF glycoproteins aggregate in
ules that are not reactive with anti-RF sera (Peruzzo,
the form of a film on top of microvilli and cilia (Figs. 11,
1995; Rodrguez et al., 1987a), suggesting that in this
species the SCO would secrete into the blood a material 16). This film has been regarded as pre-RF material
different from RF glycoproteins. (Rodrguez et al., 1986, 1992). The pre-RF material and
the material stored in the apical secretory granules
REISSNERS FIBER share the same histochemical (Herrera and Rodrguez,
The material secreted by the SCO into the ventricle 1990; W. Naumann, 1968; Oksche, 1961; Olsson,
condenses first on the surface of the SCO and then 1958a,b; Rodrguez et al., 1986; Wingstrand, 1953), and
forms an RF proper (Figs. 11, 16, 19, 2426). Three immunocytochemical (Herrera and Rodrguez, 1990;
different spatial and temporal stages of the RF glycopro- Losecke et al., 1984; Rodrguez et al., 1986, 1987a,b)
teins released into the ventricular CFS may be distin- characteristics. Pre-RF is readily visualized with trans-
guished: pre-RF material, RF proper, and massa cauda- mission (Hofer et al., 1980; Krstic, 1973; Muller and
lis (Rodrguez et al., 1987b, 1992). Sterba, 1965; Rodrguez, 1970a) and scanning (Krstic,
1975; Sturrock, 1984; Weindl and Schinko, 1975) elec- of the amphioxus immunoreact with antisera against
tron microscopy. The existence of the pre-RF in the bovine RF glycoproteins (Olsson et al., 1994; Sterba et
living animal has been demonstrated by the injection al., 1983).
into the CSF of anti-RF sera, followed by the demonstra- At early developmental stages of vertebrates, the
tion in tissue sections of the specifically bound IgG (S. floor plate cells, especially those located in the hind-
Rodrguez et al., 1990). brain, secrete a material that reacts with the anti-RF
Biosynthetic labeling using radioactive cysteine shows sera (Rodrguez et al., 1995; Schoebitz et al., 1993).
that pre-RF becomes labeled 1 hour after the adminis- According to Olsson (1956), this material is released
tration of the precursor, whereas the RF proper be- into the embryonic ventricle and forms an early RF.
comes labeled 1 hour later; thus, transformation of Olsson (1956) designated this secretory floor plate of
pre-RF material into RF may occur within 1 hour. The the hindbrain as flexural organ.
nature of the molecular events that lead first to the
formation of a pre-RF and then to the formation of the The Massa Caudalis
RF proper is not known. There is some evidence suggest- At its distal end, the central canal of the spinal cord
ing that there may be a postrelease processing of the becomes dilated; this dilatation is known as the termi-
secreted glycoproteins and that in pre-RF and RF there nal ventricle or ampulla caudalis (Figs. 20, 2729)
would be different degrees of aggregation of the consti- (Olsson, 1958b). At the terminal ventricle, RF ends as
tutive molecules (Nualart et al., 1991; Rodrguez et al., an irregular mass known as massa caudalis (Oksche,
1992). 1969; Olsson, 1955, 1958a,b; Studnicka, 1899). Under
Factors other than the ventricular release of secre- the electron microscope, the massa caudalis is visual-
tory material would be required for the formation of RF ized as a fibrillar material, less packed that in RF, and
(Schoebitz et al., 1986). Olsson (1958a) and Oksche in close aposition to the dorsal wall of the terminal
(1961) postulated that the hydrodynamic of the aqueduc- ventricle (Figs. 27, 28) (Hofer et al., 1984; S. Rodrguez
tal CSF plays a role in the aggregation of the secreted et al., 1987; Sterba and Naumann, 1966).
material in the form of a typical RF. This hypothesis is RF material arrives at the terminal ventricle at a
supported by the fact that hydrocephalic rats do not fixed rate that is determined by the growth rate of RF.
form an RF (Irigoin et al., 1990). However, a recent The volume of the massa caudalis is rather constant;
finding in our laboratory supports the view that a CSF consequently, the mechanism responsible for the escape
factor different from its hydrodinamic would partici- of RF material from the ampulla must operate continu-
pate in the assembly of the proteins into RF: the rat ously. An equilibrium between the rate of arrival of RF
SCO grafted into a lateral ventricle of an intact rat material to the ampulla and the rate of escape of this
forms a typical RF (unpublished observation). material may be envisioned. When passing from the RF
stage to the massa caudalis stage, the secretory mate-
Reissners Fiber Proper rial undergoes changes. (1) It becomes more strongly
RF grows caudally by the addition to its caphalic end reactive with anti-RF sera than with RF proper (S.
of newly released glycoproteins (Fig. 20). Thus, 2 hours Rodrguez et al., 1987; Yulis et al., 1990); this and the
after the administration of radioactive cysteine, the ultrastructural appearance of the massa caudalis sug-
label is found in the proximal portion of RF; as the gest that, at this level, RF glycoproteins become par-
postinjection time increases, the label is found in more tially unpacked. (2) At the massa caudalis, the RF
distal segments of RF (Sterba et al., 1967b). This glycoproteins lose their sialic acid residue, displaying
experimental approach has allowed us to determine the galactose as a terminal residue (S. Rodrguez et al.,
growth rate of RF. In the mouse, RF grows 10% of its 1987). This chemical modification is of high physiologi-
length per day (Ermisch, 1973); in the rat, 7% per day cal significance; indeed, it is known that sialoglycopro-
(Herrera, 1988); and in the carp and lamprey, about 1% teins become degradable by macrophages after the loss
per day (Ermisch et al., 1968; Sterba et al., 1967b). of their sialic acid residue (Sharon and Lis, 1982).
RF is formed by densely packed filaments 515 nm in
diameter (Afzelius and Olsson, 1957; Rodrguez, 1970a). Fate of Reissners Fiber Material
This ultrastructure agrees well with observations made In the lamprey, in which an ultrastructural study of
under the polarizing microscope. the ampulla has been performed, it is clear that,
Only few vertebrate species have been reported to whereas the ventral wall is lined by a continuous
lack an RF, namely, the bat (Rodrguez et al., 1987b; ependyma, the dorsal wall presents large openings that
Wislocki et al., 1956); camel (Afifi, 1964); chimpanzee communicate with a lacunar system that in turn com-
(Dendy and Nicholls, 1910), and man (see Leonhardt, municates with blood capillaries (Figs. 27, 29) (Hofer et
1980). al., 1984; S. Rodrguez et al., 1987). RF-immunoreac-
Invertebrates displaying a hollowed neural cord dis- tive material has been detected by ultrastructural
play an RF-like structure. Thus, an RF-like structure immunocytochemistry in all these cavities, including
already exists in Oikopleura; in this species, a single the local blood capillaries (Peruzzo et al., 1987). This
fibrogenic cell is the source of the secretory material finding gives strong support to previous studies suggest-
(Holmberg and Olsson, 1984). The acranian chordate ing the passage of RF material from the ampulla to
Branchiostoma lanceolatum (amphioxus) does not have local blood vessels (Hofer, 1964; W. Naumann, 1968;
an SCO but it does display an RF (Olsson and Wing- Oksche, 1969; Olsson, 1955; Sterba and Naumann,
strand, 1954). In amphioxus, the material forming RF 1966).
is secreted by a small group of ventrally localed cells In higher vertebrates, the microanatomy of the cau-
known as the infundibular organ (Hofer, 1959; Olsson dal end of the central canal shows differences with
and Wingstrand, 1954). The infundibular organ and RF respect to that of lower vertebrates (Tulsi, 1982; Wis-
Figs. 2728.
Fig. 29. Three-dimensional reconstruction of the ampulla caudalis through large intercellular spaces of the dorsal wall (arrowhead) and
and adjacent structures in the lamprey Geotria australis. Note the through a large dorsal opening (double arrows) into the lacunae (L),
Reissners fiber (RF) in the central canal and its massa caudalis from where it finally reaches blood capillaries (arrow, BV). N, noto-
(asterisk) occupying the ampulla caudalis, where it is contacted by the chord. (From Peruzzo et al., 1987).
tip of the cilia of the ventral wall. RF material is shown escaping
locki et al., 1956). However, ultrastructural studies of the existence of a dense plexus of serotonergic fibers
this region in higher vertebrates, especially in mam- along the basal region of the SCO (Bouchaud and
mals, are missing. Thus, the important question of the Bosler, 1986; Bjorklund et al., 1972; Fuxe, 1965; Mat-
fate of RF glycoproteins in these species is completely suura and Sano, 1987; Mllgard and Wiklund, 1979;
uncertain. The possibility that the RF glycoproteins of Wiklund et al., 1977). The administration of 5[3H]-HT
the massa caudalis reach the subarachnoidal CSF at or the specific neurotoxic destruction of the serotonergic
the filum has been discussed (Rodrguez et al., 1992). innervation have revealed that serotonergic fibers estab-
MECHANISMS CONTROLLING lish well-differentiated axoglandular synapses on the
THE SECRETORY ACTIVITY basal processes and at the laterobasal aspects of the
OF THE SUBCOMMISSURAL ORGAN ependymal cells (Bouchaud, 1979, 1993; Bouchaud and
Arluisson, 1977; Mllgard et al., 1978; Mllgard and
Formaldehyde-induced fluorescence, radioautogra- Wiklund, 1979). Bouchaud (1979, 1993), using high-
phy, and immunocytochemical studies have established resolution radioautography after administration of
5[3H]-HT, observed populations of labeled and unla-
beled terminals establishing synapatic contacts with
ependymocytes of the rat SCO. This finding together
Fig. 27. Sagittal section through the ampulla caudalis of the
lamprey larvae Geotria australis containing the massa caudalis. The with morphological differences between labeled (seroton-
massa caudalis is dettached from the ventral wall of the ampulla ergic) and unlabeled terminals allowed Bouchaud to
(asterisk) by the cilia (C) of the ependymal cells and attached to the propose a multiple innervation of the rat SCO. Findings
dorsal wall of the ampulla (arrowheads). Large arrows, massa cauda- reported by Matsuura and Sano (1987) in the dog and
lis material escaping through large openings of the dorsal wall of
ampulla. 34,000. Inset: Semithin section adjacent to the ultrathin by Jimenez et al. (1993) in the frog also support a
section shown in figure. Toluidine blue staining. The massa caudalis multiple innervation of the SCO. Ontogenetic studies
(mc) appears faintly stained. d, dorsal wall of ampulla; v, ventral wall have indicated an absence of serotonergic innervation
of ampulla; arrow, massa caudalis material escaping through opening
of the dorsal wall of ampulla; S, skin. 3800. in neonatal specimens of the rat, gerbil, mouse, rabbit,
and cat (Marcinkiewicz and Bouchaud, 1986; Matsuura
Fig. 28. Protein A-gold immunostaing of the massa caudalis (MC) et al., 1989; Wiklund, 1974; Wiklund et al., 1977).
of the lamprey using an anti-RF serum. The secretory material is
separated from the ependyma (E) of the ventral wall of ampulla by the Serotonin-immunoreactive fibers reach the rat SCO as
action of cilia. 320,000. early as the third postnatal day. Electrolytic lesions of
different raphe nuclei revealed that the serotonergic differentiates very early in ontogeny and may represent
innervation of the rat SCO is mainly derived from one of the first secretory structures of the brain to
nuclei raphe centralis superior and raphe dorsalis, each develop. (2) Factors other than the ventricular release
nucleus contributing about one-third of the input; the of the SCO secretion are necessary for the formation of
remainder is suggested to originate from the nucleus RF. (3) The first (embryonic) RF grows at a rate of about
raphe pontis (Leger et al., 1983). The pathways of 70% of total length per day, which is a much faster rate
sertonergic fibers from the mesencephalic raphe nuclei than that of RF of adult animals (see Reissners Fiber
to the SCO have not been established. Proper). These conclusions apply to other species, al-
The neurotoxic destruction of the serotonergic input though some species differences may be found. In the
to the SCO of the adult rat results in an increase in the rat, with a gestational period of 21 days, the neural
histochemically detectable amount of the secretory tube is formed relatively late at E-10; the SCO cells
material (Mllgard et al., 1978). Mllgard et al. con- start to display RF-immunoreactive material at E-15
cluded that the secretory activity of the SCO is under a (Schoebitz et al., 1993), and the SCO is well developed
strong inhibition by serotonergic fibers. The SCO of at E-17 (Marcinkiewicz and Bouchaud, 1983); the first
mammals during the embryonic development and the RF appears several days after birth (Schoebitz et al.,
SCO of adult nonmammalian species do not receive a 1993). Thus, rat embryos, although having a well-
serotonergic neural input. developed strongly immunoreactive SCO, lack a RF. In
Several types of peptidergic fibers have been found the bovine, with a gestational period of 9 months,
within the ependyma of the SCO (see Rodrguez et al., 2-month-old embryos display a distinct SCO containing
1992). In the frog, fibers from the pineal tract establish immunoreactive material; 2 months later, the first RF
synapatic contacts with the secretory cells of the SCO; is visualized (R. Meiniel et al., 1990, 1993).
these cells receive a second neural input of unknown The very early ontogenetic differentiation of the SCO
source and nature (Jimenez et al., 1993). secretory cells and the relatively late appearance of RF
The role of the nonserotonergic fibers innervating the could be an indication that the immunoreactive mate-
SCO is unknown. rial secreted by the early SCO cells play a role in the
The function of RF is still an enigma. Considerations first developmental stages of the CNS. This possibility
on the probable mechanisms controlling the production is supported by the appearance of RF-immunoreactive
rate and the composition of the SCO secretion are based material covering the surface of the rat neuroepithe-
on structural findings and not on biological actions of lium (Naumann et al., 1993) and within the floor plate
the RF material. A population of CSF-contacting neu- cells (Rodrguez et al., 1996) at stages prior to the
rons has been described in the medulla oblongata and differentiation of the SCO (E-12).
spinal cord of several species (Vigh and Vigh-Teichman, The SCO of human embryos offers some special
1973). These cells project their dendrites to the lumen characteristics. In the human, the SCO reaches its
of the central canal; the terminal region of these maximum development during the embryonic period
dendrites is dilated and project an atypical cilium and (Dendy and Nicholls, 1910; Oksche, 1956, 1961, 1964;
numerous stereocilia that touch the surface of the RF Olsson, 1961; Palkovits, 1965; Pesonen, 1940). After
(Vigh and Vigh-Teichman, 1973; Vigh et al., 1977). birth, the SCO undergoes regression, so that in adult
These dendrites contacting the RF could be engaged in humans only remnants of the SCO parenchyma remain
a feedback mechanism controlling the activity of the (Oksche, 1961, 1964). Although the SCO of human
SCO (Yulis et al., 1990). In teleosts, some of the spinal embryos has a histochemically detectable material
CSF-contacting neurons contain immunoreactive uro- (Oksche, 1954, 1961, 1969; Olsson 1961; Wislocki and
tensin II, whereas others display immunoreactive so- Roth, 1958), this material is not reactive with any of the
matostatine. These two populations of CSF-contacting, antibodies raised against the glycoproteins secreted by
RF-touching neurons project their axons to several the bovine SCO (Rodrguez et al., 1984a, 1990). Because
regions of the brain (Yulis and Lederis, 1986, 1988). the ultrastructural (Oksche, 1969) and lectin binding
Such neuronal systems in teleosts could establish the (Rodrguez et al., 1990) properties of the SCO of human
structural basis of a mechanism controlling the SCO embryos suggest that this organ secretes glycoproteins,
activity in response to signals originating in the central the lack of reactivity of the human SCO to anti-RF sera
canal. should be ascribed to the different nature of the human
SCO secretion. The following finding supports this
ONTOGENY OF THE view: antibodies against CSF-specific glycoproteins
SUBCOMMISSURAL ORGAN (present in CSF and missing from plasma) purified
In the chick, with an ontogenetical period of 21 days, from CSF of hydrocephalic newborn children immunos-
already at the third embryonic day (E-3), a group of tain the SCO of human embryos and the SCO of adult
cells located in the dorsal wall of the diencephalic rats (Rodrguez et al., 1993). Because the human lacks
vesicle display a material reactive with anti-RF sera an RF (see Leonhardt, 1980), it could be postulated that
(Karoumi et al., 1990; R. Meiniel et al., 1993; Naumann in this species the SCO has only kept the property to
et al., 1987; Schoebitz et al., 1986). The first signs of secrete a CSF-soluble material (see CSF-Soluble Secre-
ventricular release of secretion are detected at E-7 tory Material).
(Schoebitz et al., 1986; Wingstrand, 1953). The first
RF is seen at E-11 along the aqueduct and fourth PHYLOGENY OF THE
ventricle (R. Meiniel et al., 1993; Schoebitz et al., 1986, SUBCOMMISSURAL ORGAN
1993). At E-12, RF is already found in the lumbar spinal The SCO is an ancient and conserved brain structure.
cord (Schoebitz et al., 1986, 1993). These observations Already in cyclostomes, either lampreys or hagfish, the
lead to three important conclusions. (1) The SCO SCO-RF complex presents the basic characteristics
found throughout the vertebrate phylum, namely, tall to the central canal of the spinal cord, suggesting that
ependymal cells displaying dilated RER cisternae and the RF may be involved in the regulation of the
secreting into the ventricle, hypendymal cells project- composition of the CSF by releasing biogenic amines to
ing to the leptomeninges, and an RF extending along or removing them from the CSF.
the central canal and ending as a distinct massa
caudalis, from where the RF material escapes through Participation of the SCO
openings in the dorsal wall of the ampulla to reach the in the Hydromineral Balance
local blood vessels (Adam, 1957; Hofer et al., 1984; The SCO has been linked to various aspects of the
Peruzzo et al., 1987; S. Rodrguez et al., 1987; Sterba, hydromineral metabolism, such as aldosterone secre-
1962; Sterba et al., 1967a). Invertebrate chordates lack tion, volume reception, thirst, sodium excretion, and
an SCO but possess an RF, a phenomenon that raises diuresis (for references, see Leonhardt, 1980; Palkovits,
the question of the source of RF material in these 1965; Rodrguez et al., 1992). Foldvari and Palkovits
species (Olsson, 1993). In the lancelet Branchiostoma, (1964) showed that the SCO responds to sodium and
the RF material is secreted by the infundibular organ, a potassium deficiences. Attila and Talanti (1973) showed
group of cells located in the ventral wall of the brain that hydrocortisone treatment elevated and adrenalec-
vesicle, near the origin of the central canal (Olsson and tomy retarded the incorporation of radioactive cysteine
Wingstrand, 1954). The infundibular organRF com- into the SCO. Palkovits (1968) concluded that the
plex, including its distinct massa caudalis, immunore- administration of aldosterone reduces the SCO nuclear
acts with antibodies against the bovine RF glycopro- volume, whereas adrenalectomy or chronic dehydrata-
teins (Olsson et al., 1994; Sterba et al., 1983). In the tion produces a marked increase in nuclear volume.
appendicularian Oikopleura, a vary small RF origi- According to some researchers, the destruction of the
nates from a single fibrogen cell with ultrastructural SCO would be followed by an increase in water excre-
characteristics similar to the other RF-producing cells tion (Brown and Afifi, 1965; Gilbert, 1956), a decrease
(Holmberg and Olsson, 1984). The ascidian tadpoles in water consumption (Gilbert, 1956, 1957), changes in
also display a fine RF, but its cellular source has not the zona glomerulosa of the adrenal gland, and a fall in
been established (Olsson, 1972). In all these species, the aldosterone production (Palkovits, 1965). However,
the cells producing RF material are ventrally located the intravenous injection of SCO extracts would de-
and are floor plate descendant (Olsson, 1993). Interest- crease the urine flow (Palkovits et al, 1965). However,
ingly, the floor plate cells of vertebrate embryos secrete none of these changes were found by other researchers
a material that immunoreacts with anti-RF sera (Nau- after the destruction of the SCO or the administration
mann, 1986; Rodrguez et al., 1995; Schoebitz et al., of SCO extracts (Bugnon and Lenys, 1966; Bugnon et
1993). This immunoreactivity becomes especially strong al., 1965, 1966).
in the floor plate of the hindbrain, an area correspond- The major problems concerning studies of the SCO
ing to the flexural organ described by Olsson (1956). involving the use of extracts or lesion experiments have
The flexural organ, a glandular structure of the embry- been reviewed critically by Severs et al. (1987). Severs
onic brain, appears to be the source of RF material prior and others (Dundore et al., 1984, 1987; Severs et al.,
to the differentiation of the SCO (Olsson, 1956, 1993). 1987, 1993) used a more reliable experimental ap-
proach, i.e., microinfusions of aldosterone in the vicin-
FUNCTIONAL CONSIDERATIONS ity of the rat SCO followed by the recording of several
Although the SCO-RF complex was first described a physiological parameters. They concluded that aldoste-
century ago, its function remains enigmatic. Several rone has an effect on the SCO and/or adjacent areas
functional hypotheses have been proposed based on excluding the pineal, leading to an increase in sodium
indirect evidence. It has been proposed that the SCO-RF excretion without affecting the plasma levels of sodium
complex is involved in osmoregulation (Leatherland and potassium.
and Dodd 1968; Palkovits et al., 1965), detoxification of A recent experimental approach has been the admin-
the CSF (Diederen et al., 1983; Hess and Sterba, 1973; istration into the CSF of antibodies against RF glycopro-
Olsson, 1958a), mechanoreception (Kolmer 1921), and teins. A single injection of these antibodies leads to an
morphogenesis of the vertebral column and the spinal immediate disruption of RF and to the formation of a
cord (Hauser, 1969; Ruhle 1971). However, none of new RF several days later (S. Rodrguez et al., 1990).
these hypotheses has been convincingly substantiated These immunologically RF-deprived rats show a distur-
(see Rodrguez and Oksche, 1993; Rodrguez et al., bance in the urine flow and water intake (S. Rodrguez,
1992). Hypotheses that are based on a variety of 1991) and to severe alterations in the circulation of the
experimental designs and methodologies will be dis- CSF in the central canal (Cifuentes et al., 1994; Fernan-
cussed. dez-Llebrez et al., 1993).
The RF and the Composition of the CSF Probable Participation of the SCO
Olsson (1958a) was the first investigator to describe in Morphogenetic Mechanisms
the presence of sialic acid in the secretion of the SCO In amphibians, the normal growth of the regenerat-
and RF; he suggested that it may participate in the ing tail tissue appears to depend on the secretory
detoxifying function of RF. Sterba and Wolf (1969) activity of the SCO and on the presence of RF in the
indicated that, because of its high content of sialic acid, regenerating neural tube (Hauser, 1969; Kirsche 1956,
RF may balance the CSF concentration of biogenic Winkelmann 1960). Ruhle (1971) demonstrated that
amines by cation exchange. Diederen et al. (1983) elimination of the SCO of Pleurodeles waltii results in
demonstrated that the RF binds adrenaline and nor- deformations of the entire body axis. A similar effect
adrenaline and then transports these catecholamines was observed after destruction of the SCO in amphib-
ians (Murbach and Hauser, 1974; Hauser 1976). In E.M., and Fernandez-Llebrez, P. (1994) Decreased cerebrospinal
these experiments, however, a possible damage to the fluid flow through the central canal of the spinal cord of rats
immunologically deprived of Reissners fibre. Exp. Brain Res.,
posterior commissure and adjacent reticular forma- 98:431440.
tions should be considered. At variance is the finding Dendy, A., and Nicholls, G.E. (1910) On the occurrence of a mesocoelic
that the transection of the distal portion of the rat RF recess in the human brain, and its relation to the subcommissural
during the first 2 postnatal weeks does not interfere organ of lower vertebrates; with special reference to the distribution
of Reissners fibre in the vertebrates series and its possible function.
with normal tail growth (Sterba and Wolf, 1970). The Anat. Anz., 32:496509.
property of RF glycoproteins to aggregate embryonic Didier, R., Dastugue, B., and Meiniel, A. (1995) The secretory material
brain cells has been shown by Naumann et al. (1993). of the subcommissural organ of the chick embryo. Characterization
The question as to whether SCO-RF complex may play of a specific polypeptide by two-dimensional electrophoresis. Int. J.
a role in basic morphogenetic mechanisms of the CNS, Dev. Biol., 39:493499.
Didier, M., Harandi, M., Aguera, M., Bancel, B., Tardy, M., Fages, C.,
as suggested by the early and full development of the Calas, A., Stagaard, M., Mllgard, D.K., and Belin, M.F. (1986)
SCO during embryonic life, remains open to future Differential immunocytochemical staining for glial fibrillary acidic
investigations. (GFA) protein, S100 protein and glutamine synthetase in the rat
subcommissural organ and non specialized ventricular ependyma
ACKNOWLEDGMENTS and adjacent neuropil. Cell Tissue Res., 245:343351.
Didier-Bazes, M., Chouaf, L., Lepetit, P., Aguera, M., Belin, M.F.
We are grateful to Prof. A. Oksche, with whom we (1993) The subcommissural of the rat: An in vivo model of neuron-
have shared many of our investigations. glia interactions. In: The Subcommissural Organ. A. Oksche, E.M.
Rodrguez, and P. Fernandez-Llebrez, eds. Springer-Verlag, New
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MICROSCOPY RESEARCH AND TECHNIQUE 41:98123 (1998)

The Subcommissural Organ

KEY WORDS subcommissural organ; glycoproteins; Reissners fiber; cerebrospinal fluid

INTRODUCTION (Oksche, 1969; Olsson 1958a,b). These glycoproteins

r 1998 WILEY-LISS, INC.

SITES OF RELEASE Subarachnoidal (Leptomeningeal)

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