Exploring the Role of Neuropeptide PACAP in Cytoskeletal Function Using Spectroscopic Methods
Abstract
:1. Introduction
2. Results
2.1. Steady-State Anisotropy and Fluorescence Emission
2.2. Actin Polymerization Assay
2.3. Fluorescence Quenching Study
3. Discussion
3.1. Cytoskeletal Considerations
3.2. Interpretation of the Results
3.3. The Future of In Vitro PACAP Studies
4. Materials and Methods
4.1. Actin Preparation
4.2. PACAP Synthesis and Preparation
4.3. Steady-State Anisotropy and Fluorescence Emission Studies
4.4. Actin Polymerization Assay
4.5. Fluorescence Quenching
4.6. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Arimura, A. Perspectives on Pituitary Adenylate Cyclase Activating Polypeptide (PACAP) in the Neuroendocrine, Endocrine, and Nervous Systems. Jpn. J. Physiol. 1998, 48, 301–331. [Google Scholar] [CrossRef] [PubMed]
- Miyata, A.; Arimura, A.; Dahl, R.R.; Minamino, N.; Uehara, A.; Jiang, L.; Culler, M.D.; Coy, D.H. Isolation of a Novel 38 Residue-Hypothalamic Polypeptide Which Stimulates Adenylate Cyclase in Pituitary Cells. Biochem. Biophys. Res. Commun. 1989, 164, 567–574. [Google Scholar] [CrossRef]
- Basille, M.; Vaudry, D.; Coulouarn, Y.; Jegou, S.; Lihrmann, I.; Fournier, A.; Vaudry, H.; Gonzalez, B. Comparative Distribution of Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) Binding Sites and PACAP Receptor mRNAs in the Rat Brain during Development. J. Comp. Neurol. 2000, 425, 495–509. [Google Scholar] [CrossRef]
- Miyata, A.; Jiang, L.; Dahl, R.D.; Kitada, C.; Kubo, K.; Fujino, M.; Minamino, N.; Arimura, A. Isolation of a Neuropeptide Corresponding to the N-Terminal 27 Residues of the Pituitary Adenylate Cyclase Activating Polypeptide with 38 Residues (PACAP38). Biochem. Biophys. Res. Commun. 1990, 170, 643–648. [Google Scholar] [CrossRef]
- Freson, K.; Hashimoto, H.; Thys, C.; Wittevrongel, C.; Danloy, S.; Morita, Y.; Shintani, N.; Tomiyama, Y.; Vermylen, J.; Hoylaerts, M.F.; et al. The Pituitary Adenylate Cyclase-Activating Polypeptide Is a Physiological Inhibitor of Platelet Activation. J. Clin. Investig. 2004, 113, 905–912. [Google Scholar] [CrossRef]
- Van Eps, N.; Altenbach, C.; Caro, L.N.; Latorraca, N.R.; Hollingsworth, S.A.; Dror, R.O.; Ernst, O.P.; Hubbell, W.L. Gi- and Gs-Coupled GPCRs Show Different Modes of G-Protein Binding. Proc. Natl. Acad. Sci. USA 2018, 115, 2383–2388. [Google Scholar] [CrossRef]
- Arimura, A. Pituitary Adenylate Cyclase Activating Polypeptide (PACAP): Discovery and Current Status of Research. Regul. Pept. 1992, 37, 285–303. [Google Scholar] [CrossRef]
- Sokolov, M.V.; Kleschevnikov, A.M. Atropine Suppresses Associative LTP in the CA1 Region of Rat Hippocampal Slices. Brain Res. 1995, 672, 281–284. [Google Scholar] [CrossRef] [PubMed]
- Moody, T.W.; Lee, L.; Jensen, R.T. The G Protein-Coupled Receptor PAC1 Regulates Transactivation of the Receptor Tyrosine Kinase HER3. J. Mol. Neurosci. 2021, 71, 1589–1597. [Google Scholar] [CrossRef]
- Sureshkumar, K.; Saenz, A.; Ahmad, S.M.; Lutfy, K. The PACAP/PAC1 Receptor System and Feeding. Brain Sci. 2021, 12, 13. [Google Scholar] [CrossRef]
- Choi, J.E.; Di Nardo, A. Skin Neurogenic Inflammation. Semin. Immunopathol. 2018, 40, 249–259. [Google Scholar] [CrossRef] [PubMed]
- Helyes, Z.; Kun, J.; Dobrosi, N.; Sándor, K.; Németh, J.; Perkecz, A.; Pintér, E.; Szabadfi, K.; Gaszner, B.; Tékus, V.; et al. Pituitary Adenylate Cyclase-Activating Polypeptide Is Upregulated in Murine Skin Inflammation and Mediates Transient Receptor Potential Vanilloid-1-Induced Neurogenic Edema. J. Investg. Dermatol. 2015, 135, 2209–2218. [Google Scholar] [CrossRef]
- Sasaki, S.; Watanabe, J.; Ohtaki, H.; Matsumoto, M.; Murai, N.; Nakamachi, T.; Hannibal, J.; Fahrenkrug, J.; Hashimoto, H.; Watanabe, H.; et al. Pituitary Adenylate Cyclase-Activating Polypeptide Promotes Eccrine Gland Sweat Secretion. Br. J. Dermatol. 2017, 176, 413–422. [Google Scholar] [CrossRef]
- Steinhoff, M.; McGregor, G.P.; Radleff-Schlimme, A.; Steinhoff, A.; Jarry, H.; Schmidt, W.E. Identification of Pituitary Adenylate Cyclase Activating Polypeptide (PACAP) and PACAP Type 1 Receptor in Human Skin: Expression of PACAP-38 Is Increased in Patients with Psoriasis. Regul. Pept. 1999, 80, 49–55. [Google Scholar] [CrossRef] [PubMed]
- Warren, J.B.; Larkin, S.W.; Coughlan, M.; Kajekar, R.; Williams, T.J. Pituitary Adenylate Cyclase Activating Polypeptide Is a Potent Vasodilator and Oedema Potentiator in Rabbit Skin in Vivo. Br. J. Pharmacol. 1992, 106, 331–334. [Google Scholar] [CrossRef] [PubMed]
- Toth, D.; Tamas, A.; Reglodi, D. The Neuroprotective and Biomarker Potential of PACAP in Human Traumatic Brain Injury. Int. J. Mol. Sci. 2020, 21, 827. [Google Scholar] [CrossRef] [PubMed]
- Ji, H.; Zhang, Y.; Shen, X.; Gao, F.; Huang, C.Y.; Abad, C.; Busuttil, R.W.; Waschek, J.A.; Kupiec-Weglinski, J.W. Neuropeptide PACAP in Mouse Liver Ischemia and Reperfusion Injury: Immunomodulation via cAMP-PKA Pathway. Hepatology 2013, 57, 1225–1237. [Google Scholar] [CrossRef]
- Le, S.V.; Yamaguchi, D.J.; McArdle, C.A.; Tachiki, K.; Pisegna, J.R.; Germano, P. PAC1 and PACAP Expression, Signaling, and Effect on the Growth of HCT8, Human Colonic Tumor Cells. Regul. Pept. 2002, 109, 115–125. [Google Scholar] [CrossRef]
- Banki, E.; Sosnowska, D.; Tucsek, Z.; Gautam, T.; Toth, P.; Tarantini, S.; Tamas, A.; Helyes, Z.; Reglodi, D.; Sonntag, W.E.; et al. Age-Related Decline of Autocrine Pituitary Adenylate Cyclase-Activating Polypeptide Impairs Angiogenic Capacity of Rat Cerebromicrovascular Endothelial Cells. J. Gerontol. A Biol. Sci. Med. Sci. 2015, 70, 665–674. [Google Scholar] [CrossRef]
- Bian, N.; Du, G.; Ip, M.F.; Ding, J.; Chang, Q.; Li, Z. Pituitary Adenylate Cyclase-Activating Polypeptide Attenuates Tumor Necrosis Factor-α-Induced Apoptosis in Endothelial Colony-Forming Cells. Biomed. Rep. 2017, 7, 11–16. [Google Scholar] [CrossRef]
- Ivic, I.; Fulop, B.D.; Juhasz, T.; Reglodi, D.; Toth, G.; Hashimoto, H.; Tamas, A.; Koller, A. Backup Mechanisms Maintain PACAP/VIP-Induced Arterial Relaxations in Pituitary Adenylate Cyclase-Activating Polypeptide-Deficient Mice. J. Vasc. Res. 2017, 54, 180–192. [Google Scholar] [CrossRef] [PubMed]
- Rácz, B.; Gasz, B.; Borsiczky, B.; Gallyas, F.; Tamás, A.; Józsa, R.; Lubics, A.; Kiss, P.; Roth, E.; Ferencz, A.; et al. Protective Effects of Pituitary Adenylate Cyclase Activating Polypeptide in Endothelial Cells against Oxidative Stress-Induced Apoptosis. Gen. Comp. Endocrinol. 2007, 153, 115–123. [Google Scholar] [CrossRef] [PubMed]
- Solymar, M.; Ivic, I.; Balasko, M.; Fulop, B.D.; Toth, G.; Tamas, A.; Reman, G.; Koller, A.; Reglodi, D. Pituitary Adenylate Cyclase-Activating Polypeptide Ameliorates Vascular Dysfunction Induced by Hyperglycaemia. Diab. Vasc. Dis. Res. 2018, 15, 277–285. [Google Scholar] [CrossRef] [PubMed]
- Borboni, P.; Porzio, O.; Pierucci, D.; Cicconi, S.; Magnaterra, R.; Federici, M.; Sesti, G.; Lauro, D.; D’Agata, V.; Cavallaro, S.; et al. Molecular and Functional Characterization of Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP-38)/Vasoactive Intestinal Polypeptide Receptors in Pancreatic Beta-Cells and Effects of PACAP-38 on Components of the Insulin Secretory System. Endocrinology 1999, 140, 5530–5537. [Google Scholar] [CrossRef] [PubMed]
- Fehmann, H.C.; Göke, R.; Göke, B. Cell and Molecular Biology of the Incretin Hormones Glucagon-like Peptide-I and Glucose-Dependent Insulin Releasing Polypeptide. Endocr. Rev. 1995, 16, 390–410. [Google Scholar] [CrossRef] [PubMed]
- Inagaki, N.; Yoshida, H.; Mizuta, M.; Mizuno, N.; Fujii, Y.; Gonoi, T.; Miyazaki, J.; Seino, S. Cloning and Functional Characterization of a Third Pituitary Adenylate Cyclase-Activating Polypeptide Receptor Subtype Expressed in Insulin-Secreting Cells. Proc. Natl. Acad. Sci. USA 1994, 91, 2679–2683. [Google Scholar] [CrossRef]
- Kulkarni, R.N.; Smith, D.M.; Ghatei, M.A.; Bloom, S.R. A 67 kDa Protein Mediates Pituitary Adenylate Cyclase-Activating Polypeptide and Vasoactive Intestinal Peptide-Stimulated Insulin Secretion in a Hamster Clonal Beta-Cell Line. J. Endocrinol. 1995, 147, 121–130. [Google Scholar] [CrossRef]
- Yada, T.; Sakurada, M.; Ihida, K.; Nakata, M.; Murata, F.; Arimura, A.; Kikuchi, M. Pituitary Adenylate Cyclase Activating Polypeptide Is an Extraordinarily Potent Intra-Pancreatic Regulator of Insulin Secretion from Islet Beta-Cells. J. Biol. Chem. 1994, 269, 1290–1293. [Google Scholar] [CrossRef]
- Józsa, G.; Szegeczki, V.; Pálfi, A.; Kiss, T.; Helyes, Z.; Fülöp, B.; Cserháti, C.; Daróczi, L.; Tamás, A.; Zákány, R.; et al. Signalling Alterations in Bones of Pituitary Adenylate Cyclase Activating Polypeptide (PACAP) Gene Deficient Mice. Int. J. Mol. Sci. 2018, 19, 2538. [Google Scholar] [CrossRef]
- Juhász, T.; Matta, C.; Katona, É.; Somogyi, C.; Takács, R.; Hajdú, T.; Helgadottir, S.L.; Fodor, J.; Csernoch, L.; Tóth, G.; et al. Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) Signalling Enhances Osteogenesis in UMR-106 Cell Line. J. Mol. Neurosci. 2014, 54, 555–573. [Google Scholar] [CrossRef]
- Arms, L.; Vizzard, M.A. Neuropeptides in Lower Urinary Tract (LUT) Function. Handb. Exp. Pharmacol. 2011, 395–423. [Google Scholar] [CrossRef]
- Horvath, G.; Opper, B.; Reglodi, D. The Neuropeptide Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) Is Protective in Inflammation and Oxidative Stress-Induced Damage in the Kidney. Int. J. Mol. Sci. 2019, 20, 4944. [Google Scholar] [CrossRef] [PubMed]
- Ojala, J.; Tooke, K.; Hsiang, H.; Girard, B.M.; May, V.; Vizzard, M.A. PACAP/PAC1 Expression and Function in Micturition Pathways. J. Mol. Neurosci. 2019, 68, 357–367. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Kiss, P.; Horvath, G.; Lubics, A.; Laszlo, E.; Tamas, A.; Racz, B.; Szakaly, P. Effects of Pituitary Adenylate Cyclase Activating Polypeptide in the Urinary System, with Special Emphasis on Its Protective Effects in the Kidney. Neuropeptides 2012, 46, 61–70. [Google Scholar] [CrossRef] [PubMed]
- Horvath, G.; Illes, A.; Heimesaat, M.M.; Bardosi, A.; Bardosi, S.; Tamas, A.; Fulop, B.D.; Opper, B.; Nemeth, J.; Ferencz, A.; et al. Protective Intestinal Effects of Pituitary Adenylate Cyclase Activating Polypeptide. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP.; Reglodi, D., Tamas, A., Eds.; Current Topics in Neurotoxicity; Springer International Publishing: Cham, Switzerland, 2016; Volume 11, pp. 271–288. ISBN 978-3-319-35133-9. [Google Scholar]
- Reglodi, D.; Illes, A.; Opper, B.; Schafer, E.; Tamas, A.; Horvath, G. Presence and Effects of Pituitary Adenylate Cyclase Activating Polypeptide Under Physiological and Pathological Conditions in the Stomach. Front. Endocrinol. 2018, 9, 90. [Google Scholar] [CrossRef]
- Kaiser, E.A.; Russo, A.F. CGRP and Migraine: Could PACAP Play a Role Too? Neuropeptides 2013, 47, 451–461. [Google Scholar] [CrossRef] [PubMed]
- Rustichelli, C.; Lo Castro, F.; Baraldi, C.; Ferrari, A. Targeting Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) with Monoclonal Antibodies in Migraine Prevention: A Brief Review. Expert. Opin. Investig. Drugs 2020, 29, 1269–1275. [Google Scholar] [CrossRef] [PubMed]
- Fabian, E.; Reglodi, D.; Horvath, G.; Opper, B.; Toth, G.; Fazakas, C.; Vegh, A.G.; Wilhelm, I.; Krizbai, I.A. Pituitary Adenylate Cyclase Activating Polypeptide Acts against Neovascularization in Retinal Pigment Epithelial Cells. Ann. N.Y. Acad. Sci. 2019, 1455, 160–172. [Google Scholar] [CrossRef] [PubMed]
- Sakai, Y.; Hashimoto, H.; Shintani, N.; Katoh, H.; Negishi, M.; Kawaguchi, C.; Kasai, A.; Baba, A. PACAP Activates Rac1 and Synergizes with NGF to Activate ERK1/2, Thereby Inducing Neurite Outgrowth in PC12 Cells. Brain Res. Mol. Brain Res. 2004, 123, 18–26. [Google Scholar] [CrossRef]
- Fukuchi, M.; Tabuchi, A.; Tsuda, M. Transcriptional Regulation of Neuronal Genes and Its Effect on Neural Functions: Cumulative mRNA Expression of PACAP and BDNF Genes Controlled by Calcium and cAMP Signals in Neurons. J. Pharmacol. Sci. 2005, 98, 212–218. [Google Scholar] [CrossRef]
- Ogata, K.; Shintani, N.; Hayata-Takano, A.; Kamo, T.; Higashi, S.; Seiriki, K.; Momosaki, H.; Vaudry, D.; Vaudry, H.; Galas, L.; et al. PACAP Enhances Axon Outgrowth in Cultured Hippocampal Neurons to a Comparable Extent as BDNF. PLoS ONE 2015, 10, e0120526. [Google Scholar] [CrossRef]
- Hirabayashi, T.; Nakamachi, T.; Shioda, S. Discovery of PACAP and Its Receptors in the Brain. J. Headache Pain 2018, 19, 28. [Google Scholar] [CrossRef] [PubMed]
- Hori, M.; Nakamachi, T.; Rakwal, R.; Shibato, J.; Ogawa, T.; Aiuchi, T.; Tsuruyama, T.; Tamaki, K.; Shioda, S. Transcriptomics and Proteomics Analyses of the PACAP38 Influenced Ischemic Brain in Permanent Middle Cerebral Artery Occlusion Model Mice. J. Neuroinflammation 2012, 9, 256. [Google Scholar] [CrossRef] [PubMed]
- Czeiter, E.; Pal, J.; Kovesdi, E.; Bukovics, P.; Luckl, J.; Doczi, T.; Buki, A. Traumatic Axonal Injury in the Spinal Cord Evoked by Traumatic Brain Injury. J. Neurotrauma 2008, 25, 205–213. [Google Scholar] [CrossRef] [PubMed]
- Kövesdi, E.; Tamás, A.; Reglodi, D.; Farkas, O.; Pál, J.; Tóth, G.; Bukovics, P.; Dóczi, T.; Büki, A. Posttraumatic Administration of Pituitary Adenylate Cyclase Activating Polypeptide in Central Fluid Percussion Injury in Rats. Neurotox. Res. 2008, 13, 71–78. [Google Scholar] [CrossRef]
- Bukovics, P.; Czeiter, E.; Amrein, K.; Kovacs, N.; Pal, J.; Tamas, A.; Bagoly, T.; Helyes, Z.; Buki, A.; Reglodi, D. Changes of PACAP Level in Cerebrospinal Fluid and Plasma of Patients with Severe Traumatic Brain Injury. Peptides 2014, 60, 18–22. [Google Scholar] [CrossRef]
- Tamas, A.; Reglodi, D.; Farkas, O.; Kovesdi, E.; Pal, J.; Povlishock, J.T.; Schwarcz, A.; Czeiter, E.; Szanto, Z.; Doczi, T.; et al. Effect of PACAP in Central and Peripheral Nerve Injuries. Int. J. Mol. Sci. 2012, 13, 8430–8448. [Google Scholar] [CrossRef]
- Hayden, S.M.; Miller, P.S.; Brauweiler, A.; Bamburg, J.R. Analysis of the Interactions of Actin Depolymerizing Factor with G-and F-Actin. Biochemistry 1993, 32, 9994–10004. [Google Scholar] [CrossRef]
- Stricker, J.; Falzone, T.; Gardel, M.L. Mechanics of the F-Actin Cytoskeleton. J. Biomech. 2010, 43, 9–14. [Google Scholar] [CrossRef]
- Bezanilla, M.; Gladfelter, A.S.; Kovar, D.R.; Lee, W.-L. Cytoskeletal Dynamics: A View from the Membrane. J. Cell Biol. 2015, 209, 329–337. [Google Scholar] [CrossRef]
- Robaszkiewicz, K.; Ostrowska, Z.; Marchlewicz, K.; Moraczewska, J. Tropomyosin Isoforms Differentially Modulate the Regulation of Actin Filament Polymerization and Depolymerization by Cofilins. FEBS J. 2016, 283, 723–737. [Google Scholar] [CrossRef] [PubMed]
- Lemieux, M.G.; Janzen, D.; Hwang, R.; Roldan, J.; Jarchum, I.; Knecht, D.A. Visualization of the Actin Cytoskeleton: Different F-Actin-Binding Probes Tell Different Stories. Cytoskeleton 2014, 71, 157–169. [Google Scholar] [CrossRef] [PubMed]
- Maruthamuthu, V.; Aratyn-Schaus, Y.; Gardel, M.L. Conserved F-Actin Dynamics and Force Transmission at Cell Adhesions. Curr. Opin. Cell Biol. 2010, 22, 583–588. [Google Scholar] [CrossRef] [PubMed]
- Falluel-Morel, A.; Vaudry, D.; Aubert, N.; Galas, L.; Benard, M.; Basille, M.; Fontaine, M.; Fournier, A.; Vaudry, H.; Gonzalez, B.J. PACAP and Ceramides Exert Opposite Effects on Migration, Neurite Outgrowth, and Cytoskeleton Remodeling. Ann. N.Y. Acad. Sci. 2006, 1070, 265–270. [Google Scholar] [CrossRef]
- Fletcher, D.A.; Mullins, R.D. Cell Mechanics and the Cytoskeleton. Nature 2010, 463, 485–492. [Google Scholar] [CrossRef] [PubMed]
- Perez, V.; Bouschet, T.; Fernandez, C.; Bockaert, J.; Journot, L. Dynamic Reorganization of the Astrocyte Actin Cytoskeleton Elicited by cAMP and PACAP: A Role for phosphatidylInositol 3-Kinase Inhibition. Eur. J. Neurosci. 2005, 21, 26–32. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Atlasz, T.; Szabo, E.; Jungling, A.; Tamas, A.; Juhasz, T.; Fulop, B.D.; Bardosi, A. PACAP Deficiency as a Model of Aging. Geroscience 2018, 40, 437–452. [Google Scholar] [CrossRef]
- Reglodi, D.; Tamas, A.; Jungling, A.; Vaczy, A.; Rivnyak, A.; Fulop, B.D.; Szabo, E.; Lubics, A.; Atlasz, T. Protective Effects of Pituitary Adenylate Cyclase Activating Polypeptide against Neurotoxic Agents. Neurotoxicology 2018, 66, 185–194. [Google Scholar] [CrossRef]
- Lee, E.H.; Seo, S.R. Neuroprotective Roles of Pituitary Adenylate Cyclase-Activating Polypeptide in Neurodegenerative Diseases. BMB Rep. 2014, 47, 369–375. [Google Scholar] [CrossRef]
- Maugeri, G.; D’Amico, A.G.; Musumeci, G.; Reglodi, D.; D’Agata, V. Effects of PACAP on Schwann Cells: Focus on Nerve Injury. Int. J. Mol. Sci. 2020, 21, 8233. [Google Scholar] [CrossRef]
- Woodley, P.K.; Min, Q.; Li, Y.; Mulvey, N.F.; Parkinson, D.B.; Dun, X. Distinct VIP and PACAP Functions in the Distal Nerve Stump During Peripheral Nerve Regeneration. Front. Neurosci. 2019, 13, 1326. [Google Scholar] [CrossRef] [PubMed]
- Fukiage, C.; Nakajima, T.; Takayama, Y.; Minagawa, Y.; Shearer, T.R.; Azuma, M. PACAP Induces Neurite Outgrowth in Cultured Trigeminal Ganglion Cells and Recovery of Corneal Sensitivity after Flap Surgery in Rabbits. Am. J. Ophthalmol. 2007, 143, 255–262. [Google Scholar] [CrossRef] [PubMed]
- Suarez, V.; Guntinas-Lichius, O.; Streppel, M.; Ingorokva, S.; Grosheva, M.; Neiss, W.F.; Angelov, D.N.; Klimaschewski, L. The Axotomy-Induced Neuropeptides Galanin and Pituitary Adenylate Cyclase-Activating Peptide Promote Axonal Sprouting of Primary Afferent and Cranial Motor Neurones. Eur. J. Neurosci. 2006, 24, 1555–1564. [Google Scholar] [CrossRef]
- Armstrong, B.; Abad, C.; Chhith, S.; Cheung-Lau, G.; Hajji, O.; Nobuta, H.; Waschek, J. Impaired Nerve Regeneration and Enhanced Neuroinflammatory Response in Mice Lacking Pituitary Adenylyl Cyclase Activating Peptide (PACAP). Neuroscience 2008, 151, 63–73. [Google Scholar] [CrossRef] [PubMed]
- Baskozos, G.; Sandy-Hindmarch, O.; Clark, A.J.; Windsor, K.; Karlsson, P.; Weir, G.A.; McDermott, L.A.; Burchall, J.; Wiberg, A.; Furniss, D.; et al. Molecular and Cellular Correlates of Human Nerve Regeneration: ADCYAP1/PACAP Enhance Nerve Outgrowth. Brain 2020, 143, 2009–2026. [Google Scholar] [CrossRef] [PubMed]
- Tsuchida, M.; Nakamachi, T.; Sugiyama, K.; Tsuchikawa, D.; Watanabe, J.; Hori, M.; Yoshikawa, A.; Imai, N.; Kagami, N.; Matkovits, A.; et al. PACAP Stimulates Functional Recovery after Spinal Cord Injury through Axonal Regeneration. J. Mol. Neurosci. 2014, 54, 380–387. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Rojas, V.A.; Jiménez-Garduño, A.M.; Michelatti, D.; Tosatto, L.; Marchioretto, M.; Arosio, D.; Basso, M.; Pennuto, M.; Musio, C. ClC-2-like Chloride Current Alterations in a Cell Model of Spinal and Bulbar Muscular Atrophy, a Polyglutamine Disease. J. Mol. Neurosci. 2021, 71, 662–674. [Google Scholar] [CrossRef] [PubMed]
- Toth, D.; Szabo, E.; Tamas, A.; Juhasz, T.; Horvath, G.; Fabian, E.; Opper, B.; Szabo, D.; Maugeri, G.; D’Amico, A.G.; et al. Protective Effects of PACAP in Peripheral Organs. Front. Endocrinol. 2020, 11, 377. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.-Y.; Du, Y.-F.; Chen, L. Neuropeptides Exert Neuroprotective Effects in Alzheimer’s Disease. Front. Mol. Neurosci. 2019, 11, 493. [Google Scholar] [CrossRef]
- Nonaka, N.; Banks, W.A.; Shioda, S. Pituitary Adenylate Cyclase-Activating Polypeptide: Protective Effects in Stroke and Dementia. Peptides 2020, 130, 170332. [Google Scholar] [CrossRef]
- Cherait, A.; Maucotel, J.; Lefranc, B.; Leprince, J.; Vaudry, D. Intranasal Administration of PACAP Is an Efficient Delivery Route to Reduce Infarct Volume and Promote Functional Recovery After Transient and Permanent Middle Cerebral Artery Occlusion. Front. Endocrinol. 2021, 11, 585082. [Google Scholar] [CrossRef] [PubMed]
- Jungling, A.; Reglodi, D.; Maasz, G.; Zrinyi, Z.; Schmidt, J.; Rivnyak, A.; Horvath, G.; Pirger, Z.; Tamas, A. Alterations of Nigral Dopamine Levels in Parkinson’s Disease after Environmental Enrichment and PACAP Treatment in Aging Rats. Life 2021, 11, 35. [Google Scholar] [CrossRef] [PubMed]
- Pham, D.; Polgar, B.; Toth, T.; Jungling, A.; Kovacs, N.; Balas, I.; Pal, E.; Szabo, D.; Fulop, B.D.; Reglodi, D.; et al. Examination of Pituitary Adenylate Cyclase-Activating Polypeptide in Parkinson’s Disease Focusing on Correlations with Motor Symptoms. GeroScience 2022, 44, 785–803. [Google Scholar] [CrossRef] [PubMed]
- Tamás, A.; Lubics, A.; Lengvári, I.; Reglódi, D. Protective Effects of PACAP in Excitotoxic Striatal Lesion. Ann. N.Y. Acad. Sci. 2006, 1070, 570–574. [Google Scholar] [CrossRef] [PubMed]
- Kiss, P.; Banki, E.; Gaszner, B.; Nagy, D.; Helyes, Z.; Pal, E.; Reman, G.; Toth, G.; Tamas, A.; Reglodi, D. Protective Effects of PACAP in a Rat Model of Diabetic Neuropathy. Int. J. Mol. Sci. 2021, 22, 10691. [Google Scholar] [CrossRef] [PubMed]
- Cersosimo, M.G.; Benarroch, E.E. Pathological Correlates of Gastrointestinal Dysfunction in Parkinson’s Disease. Neurobiol. Dis. 2012, 46, 559–564. [Google Scholar] [CrossRef]
- Yan, F.; Chen, Y.; Li, M.; Wang, Y.; Zhang, W.; Chen, X.; Ye, Q. Gastrointestinal Nervous System α-Synuclein as a Potential Biomarker of Parkinson Disease. Medicine 2018, 97, e11337. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, B.J.; Vaudry, D.; Basille, M.; Rousselle, C.; Falluel-Morel, A.; Vaudry, H. Function of PACAP in the Central Nervous System. In Pituitary Adenylate Cyclase-Activating Polypeptide; Vaudry, H., Arimura, A., Eds.; Springer US: Boston, MA, USA, 2003; pp. 125–151. ISBN 978-1-4615-0243-2. [Google Scholar]
- Manecka, D.-L.; Boukhzar, L.; Falluel-Morel, A.; Lihrmann, I.; Anouar, Y. PACAP Signaling in Neuroprotection. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Reglodi, D., Tamas, A., Eds.; Springer International Publishing: Cham, Switzerland, 2016; pp. 549–561. ISBN 978-3-319-35135-3. [Google Scholar]
- Bukovics, P.; Lőrinczy, D. Exploring the Response of PACAP on Thermal Endurance of F-Actin by Differential Scanning Calorimetry. J. Therm. Anal. Calorim. 2024. [Google Scholar] [CrossRef]
- Bukovics, P.; Tamás, A.; Tóth, G.; Lőrinczy, D. Investigating the Impact of PACAP on Thermal Stability of G-Actin by Differential Scanning Calorimetry. J. Therm. Anal. Calorim. 2024. [Google Scholar] [CrossRef]
- Wang, J.; Song, X.; Zhang, D.; Chen, X.; Li, X.; Sun, Y.; Li, C.; Song, Y.; Ding, Y.; Ren, R.; et al. Cryo-EM Structures of PAC1 Receptor Reveal Ligand Binding Mechanism. Cell Res. 2020, 30, 436–445. [Google Scholar] [CrossRef]
- Blanquie, O.; Bradke, F. Cytoskeleton Dynamics in Axon Regeneration. Curr. Opin. Neurobiol. 2018, 51, 60–69. [Google Scholar] [CrossRef] [PubMed]
- Hur, E.-M.; Saijilafu; Zhou, F.-Q. Growing the Growth Cone: Remodeling the Cytoskeleton to Promote Axon Regeneration. Trends Neurosci. 2012, 35, 164–174. [Google Scholar] [CrossRef] [PubMed]
- Lesk, A.M.; Ross Boswell, D. What the Papers Say: Does Protein Structure Determine Amino Acid Sequence? BioEssays 1992, 14, 407–410. [Google Scholar] [CrossRef]
- Wang, Z.; Liu, J.; Huang, Y.; Liu, Q.; Chen, M.; Ji, C.; Feng, J.; Ma, Y. Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP) -Derived Peptide MPAPO Stimulates Adipogenic Differentiation by Regulating the Early Stage of Adipogenesis and ERK Signaling Pathway. Stem Cell Rev. Rep. 2023, 19, 516–530. [Google Scholar] [CrossRef] [PubMed]
- Spudich, J.A.; Watt, S. The Regulation of Rabbit Skeletal Muscle Contraction. I. Biochemical Studies of the Interaction of the Tropomyosin-Troponin Complex with Actin and the Proteolytic Fragments of Myosin. J. Biol. Chem. 1971, 246, 4866–4871. [Google Scholar] [CrossRef] [PubMed]
- Mossakowska, M.; Belágyi, J.; Strzelecka-Golaszewska, H. An EPR Study of the Rotational Dynamics of Actins from Striated and Smooth Muscle and Their Complexes with Heavy Meromyosin. Eur. J. Biochem. 1988, 175, 557–564. [Google Scholar] [CrossRef] [PubMed]
- Tóth, M.Á.; Majoros, A.K.; Vig, A.T.; Migh, E.; Nyitrai, M.; Mihály, J.; Bugyi, B. Biochemical Activities of the Wiskott-Aldrich Syndrome Homology Region 2 Domains of Sarcomere Length Short (SALS) Protein. J. Biol. Chem. 2016, 291, 667–680. [Google Scholar] [CrossRef]
- Vig, A.T.; Földi, I.; Szikora, S.; Migh, E.; Gombos, R.; Tóth, M.Á.; Huber, T.; Pintér, R.; Talián, G.C.; Mihály, J.; et al. The Activities of the C-Terminal Regions of the Formin Protein Disheveled-Associated Activator of Morphogenesis (DAAM) in Actin Dynamics. J. Biol. Chem. 2017, 292, 13566–13583. [Google Scholar] [CrossRef]
- Gasz, B.; Rácz, B.; Roth, E.; Borsiczky, B.; Ferencz, A.; Tamás, A.; Cserepes, B.; Lubics, A.; Gallyas, F.; Tóth, G.; et al. Pituitary Adenylate Cyclase Activating Polypeptide Protects Cardiomyocytes against Oxidative Stress-Induced Apoptosis. Peptides 2006, 27, 87–94. [Google Scholar] [CrossRef]
- Merrifield, R.B. Solid Phase Peptide Synthesis. I. The Synthesis of a Tetrapeptide. J. Am. Chem. Soc. 1963, 85, 2149–2154. [Google Scholar] [CrossRef]
- Józsa, R.; Hollósy, T.; Tamás, A.; Tóth, G.; Lengvári, I.; Reglodi, D. Pituitary Adenylate Cyclase Activating Polypeptide Plays a Role in Olfactory Memory Formation in Chicken. Peptides 2005, 26, 2344–2350. [Google Scholar] [CrossRef] [PubMed]
Intrinsic Fluorophore | PACAP38 | PACAP27 | PACAP6-38 |
---|---|---|---|
Trp | 0 | 0 | 0 |
Tyr | 4 | 3 | 4 |
Phe | 1 | 1 | 1 |
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Vékony, R.G.; Tamás, A.; Lukács, A.; Ujfalusi, Z.; Lőrinczy, D.; Takács-Kollár, V.; Bukovics, P. Exploring the Role of Neuropeptide PACAP in Cytoskeletal Function Using Spectroscopic Methods. Int. J. Mol. Sci. 2024, 25, 8063. https://doi.org/10.3390/ijms25158063
Vékony RG, Tamás A, Lukács A, Ujfalusi Z, Lőrinczy D, Takács-Kollár V, Bukovics P. Exploring the Role of Neuropeptide PACAP in Cytoskeletal Function Using Spectroscopic Methods. International Journal of Molecular Sciences. 2024; 25(15):8063. https://doi.org/10.3390/ijms25158063
Chicago/Turabian StyleVékony, Roland Gábor, Andrea Tamás, András Lukács, Zoltán Ujfalusi, Dénes Lőrinczy, Veronika Takács-Kollár, and Péter Bukovics. 2024. "Exploring the Role of Neuropeptide PACAP in Cytoskeletal Function Using Spectroscopic Methods" International Journal of Molecular Sciences 25, no. 15: 8063. https://doi.org/10.3390/ijms25158063