Development and Degeneration of the Intervertebral Disc—Insights from Across Species
Abstract
:Simple Summary
Abstract
1. Introduction
2. A General Understanding of Anatomic and Molecular Features of the IVD
2.1. Importance of the Notochord
2.2. IVD Structure: Nucleus Pulposus
2.3. IVD Structure: Annulus Fibrosus
2.4. IVD Structure: Cartilage Endplates
2.5. Multi Species scRNA seq Supports Cell Heterogeneity and Clarifies Cell Identities in the IVD
Species | NC | NP | Inner AF | Outer AF | Method | Source |
---|---|---|---|---|---|---|
Human | - | C2ORF40, MGP, MSMP, CHI3L1, LGALS1, ID1, ID3 and TMED | MT1F, PLA2GA, EPYC, PRELP, C10ORF10, FGFBP2 and CHI3L1 | - | Human single-cell transcriptome analysis | [64] |
- | - | - | COL5A1 | spatiotemporal and single cell transcriptomic analysis | [29] | |
SOX10, CTSK | - | - | - | Mouse spatiotemporal transcriptional analysis, human embryonic single cell transcriptomic atlas, immunohistochemistry of mouse IVD | [50] | |
CD24, STMN2, RTN1, PRPH, CXCL-12, IGF-1, MAP1B, ISL1, CLDN1, and THBS2. | - | - | - | Microarray analysis and qPCR validation of human embryonic, fetal, and adult spine | [36] | |
Rat | - | Krrt7, Prrg4, Akap12, Cxcl3, Rab38 | Mmp3, Bpifb1, Bpifa1a, Mmp13, Il11, Inhba | Fibin, Igfbp5, Tnmd, Myoc, Cilp, Lum | Single-cell transcriptome analysis | [58] |
- | CD24, Basp1, Ncdn | CD90 | cDNA microarray, RT-PCR, IHC | [65] | ||
Mouse | - | Anxa3, Cdh2, Cd44, Ca3, Slc2a1, Krt8, Krt19, CD109, and CD81, of which Cdh2, CD44, Slc2a1, and CD81 are exclusive in the NP | Tnmd, Col5a1, Col5a2, Col12a1, and Lect1 of which Tnmd, Col5a2, and Col12a1 are exclusive in the AF | Proteomic analysis of mouse lumbar and tail IVD and comparison to human IVD | [66] | |
- | Gli1, Gli3, Noto, Scx, Ptpr, Sox2, Zscan10, Loc101904175 | - | Lam1, Thy1 | RISH | [67] | |
Krt8, Atp6v1g3, C1qtnf3, Cd55, Spp1 | Cp, S100b, H2ac18, Snorc, Creld2, Pdia4, Dnajc3, Chcd7, Rcn2 | Mgp, Comp, Spp1, Gsn, Sod2, Dcn, Fn1, Timp3, Wdr73 | Igfbp6, Ctsk, Lgals1, Ccn3 | Sc RNA seq | [68] | |
Bovine | - | T, Cd24 and Krt19 | - | Adamts17, Col5a1, Col12a1 and Sfrp2 | qPCR | [69] |
T | Cdh2, Krt8, Krt18, SNAP25, Sostdc1, Ibsp | - | - | qRT-PCR and Microarray Analysis | [70] | |
- | Gli1, Gli3, Noto, Ptprc, Scx, Sox2 and Zscan10 | - | Lam1, Thy1 | Fluorescent RISH, confocal microscopy, gaussian mixture modeling | [28] |
3. Stress and Inflammation in the IVD
3.1. Environmental Stress Factors
3.1.1. Mechanical Stress and Trauma
3.1.2. Metabolic Stress
3.2. Inflammation and Degeneration
3.2.1. Regulated Cell Death and Tissue Homeostasis
3.2.2. Protagonists and Antagonists in the Proinflammatory IVD
Species | Degenerating IVD | Method | Source |
---|---|---|---|
Humans | IL6 serum level is significantly higher In IVDD than disc herniation or control groups | Electrochemiluminescence immunoassays | [114] |
Elevated CCL5 and CXCL6 plasma levels in moderate to severe IVDD compared to healthy control | ELISA and MRI | [115] | |
Significant increase in IL18 for degenerated Grade IV/V IVD | IL18 ELISA kit | [116] | |
Degeneration: MT1G, SPP1, HMGA1, FN1, FBXO2, SPARC, VIM, CTGF, MGST1, TAF1D, CAPS, SPTSSB, S100A1, CHI3L2, PLA2G2A, TNRSF11B, FGFBP2, MGP, SLPI, DCN, MT-ND2, MTCYB, ADIRF, FRZB, CLEC3A, UPP1, S100A2, PRG4, COL2A1, SOD2 and MT2A Verified by protein and mRNA expression: MGST1, vimentin, SOD2 and SYF2 | scRNA seq, quantitative immunofluorescence and Western blotting | [64] | |
Shear stiffness in both NP and AF correlated with increased Pfirrmann Grade of degeneration | MR elastography shear stiffness measurement | [117] | |
Cox2+ cell number from Grade 2 IVDD onwards | IHC | [104] | |
Reduced GRB10 in lumbar IVDD compared to healthy controls. Not detected in piriformis syndrome, sacroiliac joint pain, entrapment neuropathy and lumbar disc herniation, suggesting a biomarker for lumbar IVDD. | miRNA qRT-PCR from plasma sample | [118] | |
CASP1, IL1β, NLRP3 | mRNA expression, IHC | [119] | |
SPP1 secreted by NC | Mouse spatiotemporal transcriptional analysis, human embryonic single cell transcriptomic atlas, IHC of mouse IVD | [50] | |
Increased sensitization of the disc: IL1β, IL6, IL8, IL10, TNFα, IFNy Upregulated in Disc herniation group compared to IVDD: IL4, IL6, IL12, IFNy | IHC | [112,113] | |
Increased levels in IVDD compared to herniated NP (HNP) groups: TNF-α and IL8 Increased expression levels in IVDD compared to herniated NP (HNP) groups: TGFb, VEGF, and NGF | Western Blot | [120] | |
CCR7+ and CD163+ cells significantly increase with degeneration in NP, AF, and CEP, while CD206+ cells were present but did not significantly increase with further degeneration. CCR7+, CD163+, and CD206+ cells were not found in healthy IVD. | IHC | [99] | |
Upregulated in degeneration: SLC7A2, LIF, NAMPT, IL1β, NOD2, CCL20, CCL7, TNFRSF1B, LYN, and GCH1 Inflammatory genes proposed as biomarker of IVDD with positive correlation to infiltration of immune cells: IL1β, LYN, NAMPT | Statistical analysis of available gene expression profiles | [121] | |
Decreased expression in degenerate IVD: CDH2, KRT8, KRT Increased expression in degenerated AF: VCAN, TNMD, and BASP1 | qRT-PCR and Microarray analysis | [70] | |
Humans and Rats | Upregulated in dNP: COMP, MGP, FBLN1, BASP1, NCDN and CD155 Downregulated in dNP: SNAP25, KRT8, KRT18, CDH2, KRT19, NRP-1 and CD221 | Cumulative data from rat RT-PCR, human RT-PCR, and rat microarray | [122] |
Rat | Core genes in IVDD in TSZ-induced T1DM rats: Bmp7, Ripk4, Wnt4, Timp1, Col11a1, Acp5, Vdr, Col8a1, Aldh1a1, and Thbs4 | Microarray analysis and transcriptome sequencing of NP cells followed by interaction analysis | [123] |
Dog | Clusterin as a cerebrospinal fluid marker for chronic IVDD | Liquid chromatography, mass spectrometry, SDS-page, Western blot, and IHC | [124] |
Significantly lower GAG content in Grade IV and V degenerated discs | GAG assay | [125] | |
Cox2+ cell percentage in the NP and dorsal AF is significantly higher in Grade IV and V discs compared to Grades I and II | IHC | [125] | |
Significantly higher protein levels of IL8 and Tnfα in IVDD versus healthy discs. Significantly higher mRNA levels of IL6 and positive correlation between IL6 and pain severity | qPCR, ELISA, IHC | [103] | |
Increased levels of Tnfα in discs adjacent to IVDD or herniation | qPCR, ELISA, IHC | [103] | |
Cow | Lam1, Thy1 | RISH | [67] |
Significantly lower number of CD29+, CD44+, CD45+ and Tie2+ aged NP cells compared to younger NP cells | Flow cytometry, IHC | [126] |
4. Insights from Different Species
4.1. Primates
4.1.1. Humans
4.1.2. Non-Human Primates
4.2. Dogs
4.3. Rodents
4.3.1. Mice
4.3.2. Rats
4.3.3. Rabbits
4.4. Ungulates
4.4.1. Cows
4.4.2. Horses
Common Region of Degeneration | Clinical Presentation | Radiographic Findings | Biochemical Markers | Serum Analysis | Histological |
---|---|---|---|---|---|
Cervical sections (161 cervical degenerated discs (DD): 56 thoracic DD: 48 lumbosacral DD) [162] | Spinal ataxia, more severe in pelvic limbs [170] | Collapse of disc space [171] | Increase in pentosidine in AF and NP [11] | Elevated creatine phosphokinase [171] | Fiber degeneration of white matter [171] |
Caudo-cervical region showed significantly more severe degeneration compared to other regions. [162] | Limited range of motion in neck [11] | Endplate sclerosis [171] | Advanced glycation end product (AGE) crosslinking [11] | Serum glutamic-oxalocetictransaminase slightly elevated [171] | Poor myelin staining [171] |
Severe neck pain [11] | Disc protrusion [170,171] | Decrease in hydroxylysine moderate in AF, severe in NP [11] | Elevated blood urea nitrogen [171] | Necrosis of individual neurons in region of disc protrusion [171] | |
Lameness [170] | Increased Collagen type I in NP [11] | Elevated venous pH values [171] | Scattering of microglial cells [171] | ||
Spasticity [11] | No change in glycosaminoglycans in NP [11] | CSF showed elevated protein content of xanthochromia [172] | Swollen axons [171] | ||
Dysmetria [11] | Increased GFAP serum levels [169] | Degeneration of spinal cord in area of disc protrusion [172] | |||
Normal cutaneous sensation and cranial nerve function [11] | Increased pNF-H serum levels [171] | ||||
Positive sway response [11] | |||||
Proprioceptive deficits [11] |
4.5. Cats
4.5.1. Large Cats
4.5.2. Small Cats
4.6. Others
American Black Bear
5. Discussion
6. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Murphy, K.; Lufkin, T.; Kraus, P. Development and Degeneration of the Intervertebral Disc—Insights from Across Species. Vet. Sci. 2023, 10, 540. https://doi.org/10.3390/vetsci10090540
Murphy K, Lufkin T, Kraus P. Development and Degeneration of the Intervertebral Disc—Insights from Across Species. Veterinary Sciences. 2023; 10(9):540. https://doi.org/10.3390/vetsci10090540
Chicago/Turabian StyleMurphy, Kathryn, Thomas Lufkin, and Petra Kraus. 2023. "Development and Degeneration of the Intervertebral Disc—Insights from Across Species" Veterinary Sciences 10, no. 9: 540. https://doi.org/10.3390/vetsci10090540