Review on PACAP-Induced Transcriptomic and Proteomic Changes in Neuronal Development and Repair
Abstract
1. General Overview
2. Involvement of PACAP in Neuronal Developmental Processes
3. Neuroprotective Effects of PACAP
Acknowledgments
Conflicts of Interest
References
- Jolivel, V.; Basille, M.; Aubert, N.; de Jouffrey, S.; Ancian, P.; Le Bigot, J.F.; Noack, P.; Massonneau, M.; Fournier, A.; Vaudry, H.; et al. Distribution and functional characterization of pituitary adenylate cyclase-activating polypeptide receptors in the brain of non-human primates. Neuroscience 2009, 160, 434–451. [Google Scholar] [CrossRef] [PubMed]
- Pirger, Z.; Krajcs, N.; Kiss, T. Occurrence, distribution, and physiological function of pituitary adenylyl cyclase-activating polypeptide in invertebrate species. In Pituitary Adenylate Cyclase Activating Polypeptide —PACAP; Reglodi, D., Tamas, A., Eds.; Springer: Cham, Switzerland, 2016; pp. 19–31. [Google Scholar]
- Egri, P.; Fekete, C.; Denes, A.; Reglodi, D.; Hashimoto, H.; Fulop, B.D.; Gereben, B. Pituitary adenylate cyclase-activating polypeptide (PACAP) regulates the hypothalamo-pituitary-thyroid (HPT) axis via type 2 deiodinase in male mice. Endocrinology 2016, 157, 2356–2366. [Google Scholar] [CrossRef] [PubMed]
- Kanasaki, H.; Oride, A.; Tselmeg, M.; Sukhbaatar, U.; Kyo, S. Role of PACAP and its PACAP type I receptor in the central control of reproductive hormones. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Reglodi, D., Tamas, A., Eds.; Springer: Cham, Switzerland, 2016; pp. 375–387. [Google Scholar]
- Garami, A.; Pakai, E.; Rumbus, Z.; Solymar, M. The role of pacap in the regulation of body temperature. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; pp. 239–257. [Google Scholar]
- Banki, E.; Kovacs, K.; Nagy, D.; Juhasz, T.; Degrell, P.; Csanaky, K.; Kiss, P.; Jancso, G.; Toth, G.; Tamas, A. Molecular mechanisms underlying the nephroprotective effects of PACAP in diabetes. J. Mol. Neurosci. 2014, 54, 300–309. [Google Scholar] [CrossRef] [PubMed]
- Sekar, R.; Wang, L.; Chow, B.K. Central control of feeding behavior by the secretin, PACAP, and glucagon family of peptides. Front. Endocrinol. 2017, 8, 18. [Google Scholar] [CrossRef] [PubMed]
- Hurley, M.M.; Maunze, B.; Block, M.E.; Frenkel, M.M.; Reilly, M.J.; Kim, E.; Chen, Y.; Li, Y.; Baker, D.A.; Liu, Q.-S. Pituitary adenylate-cyclase activating polypeptide regulates hunger-and palatability-induced binge eating. Front. Neurosci. 2016, 10, 383. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, M.; Nakamachi, T.; Watanabe, J.; Sugiyama, K.; Ohtaki, H.; Murai, N.; Sasaki, S.; Xu, Z.; Hashimoto, H.; Seki, T. Pituitary adenylate cyclase-activating polypeptide (PACAP) is involved in adult mouse hippocampal neurogenesis after stroke. J. Mol. Neurosci. 2016, 59, 270–279. [Google Scholar] [CrossRef] [PubMed]
- Pecoraro, V.; Sardone, L.M.; Chisari, M.; Licata, F.; Volsi, G.L.; Perciavalle, V.; Ciranna, L.; Costa, L. A subnanomolar concentration of pituitary adenylate cyclase-activating polypeptide (PACAP) pre-synaptically modulates glutamatergic transmission in the rat hippocampus acting through acetylcholine. Neuroscience 2017, 340, 551–562. [Google Scholar] [CrossRef] [PubMed]
- Han, P.; Caselli, R.J.; Baxter, L.; Serrano, G.; Yin, J.; Beach, T.G.; Reiman, E.M.; Shi, J. Association of pituitary adenylate cyclase–activating polypeptide with cognitive decline in mild cognitive impairment due to Alzheimer disease. JAMA Neurol. 2015, 72, 333–339. [Google Scholar] [CrossRef] [PubMed]
- Kirry, A.J.; Herbst, M.R.; Poirier, S.E.; Maskeri, M.M.; Rothwell, A.C.; Twining, R.C.; Gilmartin, M.R. Pituitary adenylate-cyclase activating-polypeptide (PACAP) signaling in the prefrontal cortex modulates cued fear learning, but not spatial working memory, in female rats. Neuropharmacology 2018, 133, 145–154. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, J.; Seki, T.; Shioda, S. Pacap and neural development. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; pp. 65–82. [Google Scholar]
- Nakamachi, T.; Farkas, J.; Watanabe, J.; Ohtaki, H.; Dohi, K.; Arata, S.; Shioda, S. Role of PACAP in neural stem/progenitor cell and astrocyte: From neural development to neural repair. Curr. Pharm. Des. 2011, 17, 973–984. [Google Scholar] [CrossRef] [PubMed]
- Waschek, J.A. Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration. Dev. Neurosci. 2002, 24, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Somogyvari-Vigh, A.; Reglodi, D. Pituitary adenylate cyclase activating polypeptide: A potential neuroprotective peptide. Curr. Pharm. Des. 2004, 10, 2861–2889. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Kiss, P.; Lubics, A.; Tamas, A. Review on the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo. Curr. Pharm. Des. 2011, 17, 962–972. [Google Scholar] [CrossRef] [PubMed]
- Shioda, S.; Nakamachi, T. PACAP as a neuroprotective factor in ischemic neuronal injuries. Peptides 2015, 72, 202–207. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Kiss, P.; Szabadfi, K.; Atlasz, T.; Gabriel, R.; Horvath, G.; Szakaly, P.; Sandor, B.; Lubics, A.; Laszlo, E. PACAP is an endogenous protective factor—Insights from PACAP-deficient mice. J. Mol. Neurosci. 2012, 48, 482–492. [Google Scholar] [CrossRef] [PubMed]
- Ohtaki, H.; Nakamachi, T.; Dohi, K.; Aizawa, Y.; Takaki, A.; Hodoyama, K.; Yofu, S.; Hashimoto, H.; Shintani, N.; Baba, A. Pituitary adenylate cyclase-activating polypeptide (PACAP) decreases ischemic neuronal cell death in association with IL-6. Proc. Natl. Acad. Sci. USA 2006, 103, 7488–7493. [Google Scholar] [CrossRef] [PubMed]
- Tsuchikawa, D.; Nakamachi, T.; Tsuchida, M.; Wada, Y.; Hori, M.; Farkas, J.; Yoshikawa, A.; Kagami, N.; Imai, N.; Shioda, S. The neuroprotective effect of endogenous PACAP on spinal cord injury. J. Mol. Neurosci. 2012, 48, 508–517. [Google Scholar] [CrossRef] [PubMed]
- Szabadfi, K.; Atlasz, T.; Kiss, P.; Danyadi, B.; Tamas, A.; Helyes, Z.; Hashimoto, H.; Shintani, N.; Baba, A.; Toth, G. Mice deficient in pituitary adenylate cyclase activating polypeptide (PACAP) are more susceptible to retinal ischemic injury in vivo. Neurotox. Res. 2012, 21, 41–48. [Google Scholar] [CrossRef] [PubMed]
- Manavalan, S.; Getachew, B.; Manaye, K.F.; Khundmiri, S.J.; Csoka, A.B.; McKinley, R.; Tamas, A.; Reglodi, D.; Tizabi, Y. PACAP protects against ethanol and nicotine toxicity in SH-SY5Y cells: Implications for drinking-smoking co-morbidity. Neurotox. Res. 2017, 32, 8–13. [Google Scholar] [CrossRef] [PubMed]
- Vaudry, D.; Falluel-Morel, A.; Bourgault, S.; Basille, M.; Burel, D.; Wurtz, O.; Fournier, A.; Chow, B.K.; Hashimoto, H.; Galas, L.; et al. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol. Rev. 2009, 61, 283–357. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Renaud, J.; Tamas, A.; Tizabi, Y.; Socias, S.B.; del-Bel, E.; Raisman-Vozari, R. Novel tactics for neuroprotection in Parkinson’s disease: Role of antibiotics, polyphenols and neuropeptides. Prog. Neurobiol. 2017, 155, 120–148. [Google Scholar] [CrossRef] [PubMed]
- Vaudry, D.; Gonzalez, B.J.; Basille, M.; Yon, L.; Fournier, A.; Vaudry, H. Pituitary adenylate cyclase-activating polypeptide and its receptors: From structure to functions. Pharmacol. Rev. 2000, 52, 269–324. [Google Scholar] [PubMed]
- Manecka, D.-L.; Boukhzar, L.; Falluel-Morel, A.; Lihrmann, I.; Anouar, Y. PACAP signaling in neuroprotection. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; pp. 549–561. [Google Scholar]
- Vaczy, A.; Reglodi, D.; Somoskeoy, T.; Kovács, K.; Lokos, E.; Szabo, E.; Tamas, A.; Atlasz, T. The protective role of PAC1-receptor agonist maxadilan in BCCAO-induced retinal degeneration. J. Mol. Neurosci. 2016, 60, 186–194. [Google Scholar] [CrossRef] [PubMed]
- Ohtaki, H.; Shioda, S. PACAP regulation of inflammatory and free radical networks in neuronal and nonneuronal diseases. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Reglodi, D., Tamas, A., Eds.; Springer: Cham, Switzerland, 2016; pp. 671–690. [Google Scholar]
- Moody, T.W.; Nuche-Berenguer, B.; Jensen, R.T. Vasoactive intestinal peptide/pituitary adenylate cyclase activating polypeptide, and their receptors and cancer. Curr. Opin. Endocrinol. Diabetes Obes. 2016, 23, 38–47. [Google Scholar] [CrossRef] [PubMed]
- Doan, N.-D.; Chatenet, D.; Létourneau, M.; Vaudry, H.; Vaudry, D.; Fournier, A. Receptor-independent cellular uptake of pituitary adenylate cyclase-activating polypeptide. Biochim. Biophys. Acta 2012, 1823, 940–949. [Google Scholar] [CrossRef] [PubMed]
- Samal, B.; Gerdin, M.J.; Huddleston, D.; Hsu, C.-M.; Elkahloun, A.G.; Stroth, N.; Hamelink, C.; Eiden, L.E. Meta-analysis of microarray-derived data from PACAP-deficient adrenal gland in vivo and PACAP-treated chromaffin cells identifies distinct classes of PACAP-regulated genes. Peptides 2007, 28, 1871–1882. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Eiden, L.E.; Samal, B.; Gerdin, M.J.; Mustafa, T.; Vaudry, D.; Stroth, N. Discovery of pituitary adenylate cyclase-activating polypeptide-regulated genes through microarray analyses in cell culture and in vivo. Ann. N. Y. Acad. Sci. 2008, 1144, 6–20. [Google Scholar] [CrossRef] [PubMed]
- Ait-Ali, D.; Samal, B.; Mustafa, T.; Eiden, L.E. Neuropeptides, growth factors, and cytokines: A cohort of informational molecules whose expression is up-regulated by the stress-associated slow transmitter PACAP in chromaffin cells. Cell. Mol. Neurobiol. 2010, 30, 1441–1449. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Samal, B.; Ait-Ali, D.; Bunn, S.; Mustafa, T.; Eiden, L.E. Discrete signal transduction pathway utilization by a neuropeptide (PACAP) and a cytokine (TNF-α) first messenger in chromaffin cells, inferred from coupled transcriptome-promoter analysis of regulated gene cohorts. Peptides 2013, 45, 48–60. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Dejda, A.; Seaborn, T.; Bourgault, S.; Touzani, O.; Fournier, A.; Vaudry, H.; Vaudry, D. PACAP and a novel stable analog protect rat brain from ischemia: Insight into the mechanisms of action. Peptides 2011, 32, 1207–1216. [Google Scholar] [CrossRef] [PubMed]
- Hori, M.; Nakamachi, T.; Shibato, J.; Rakwal, R.; Shioda, S.; Numazawa, S. Unraveling the specific ischemic core and penumbra transcriptome in the permanent middle cerebral artery occlusion mouse model brain treated with the neuropeptide PACAP38. Microarrays 2015, 4, 2–24. [Google Scholar] [CrossRef] [PubMed]
- Lebon, A.; Seyer, D.; Cosette, P.; Coquet, L.; Jouenne, T.; Chan, P.; Leprince, J.; Fournier, A.; Vaudry, H.; Gonzalez, B.J.; et al. Identification of proteins regulated by PACAP in PC12 cells by 2D gel electrophoresis coupled to mass spectrometry. Ann. N. Y. Acad. Sci. 2006, 1070, 380–387. [Google Scholar] [CrossRef] [PubMed]
- Gasperini, L.; Piubelli, C.; Carboni, L. Proteomics of rat hypothalamus, hippocampus and pre-frontal/frontal cortex after central administration of the neuropeptide PACAP. Mol. Biol. Rep. 2012, 39, 2921–2935. [Google Scholar] [CrossRef] [PubMed]
- Maasz, G.; Pirger, Z.; Reglodi, D.; Petrovics, D.; Schmidt, J.; Kiss, P.; Rivnyak, A.; Hashimoto, H.; Avar, P.; Jambor, E.; et al. Comparative protein composition of the brains of PACAP-deficient mice using mass spectrometry-based proteomic analysis. J. Mol. Neurosci. 2014, 54, 310–319. [Google Scholar] [CrossRef] [PubMed]
- Maasz, G.; Zrinyi, Z.; Reglodi, D.; Petrovics, D.; Rivnyak, A.; Kiss, T.; Jungling, A.; Tamas, A.; Pirger, Z. Pituitary adenylate cyclase-activating polypeptide (PACAP) has a neuroprotective function in dopamine-based neurodegeneration in rat and snail parkinsonian models. Dis. Model. Mech. 2017, 10, 127–139. [Google Scholar] [CrossRef] [PubMed]
- Cabezas-Llobet, N.; Vidal-Sancho, L.; Masana, M.; Fournier, A.; Albrech, J.; Vaudry, D.; Xifró, X. Pituitary adenylate cyclase-activating polypeptide (PACAP) enhances hippocampal synaptic plasticity and improves memory performance in Huntington’s disease. Mol. Neurobiol. 2018, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Hori, M.; Nakamachi, T.; Shibato, J.; Rakwal, R.; Tsuchida, M.; Shioda, S.; Numazawa, S. PACAP38 differentially effects genes and CRMP2 protein expression in ischemic core and penumbra regions of permanent middle cerebral artery occlusion model mice brain. Int. J. Mol. Sci. 2014, 15, 17014–17034. [Google Scholar] [CrossRef] [PubMed]
- Fahrenkrug, J.; Hannibal, J.; Honore, B.; Vorum, H. Altered calmodulin response to light in the suprachiasmatic nucleus of PAC1 receptor knockout mice revealed by proteomic analysis. J. Mol. Neurosci. 2005, 25, 251–258. [Google Scholar] [CrossRef]
- Waschek, J.A.; Baca, S.M.; Akerman, S. PACAP and migraine headache: Immunomodulation of neural circuits in autonomic ganglia and brain parenchyma. J. Headache Pain 2018, 19, 23. [Google Scholar] [CrossRef] [PubMed]
- Ishido, M.; Masuo, Y. Transcriptome of pituitary adenylate cyclase-activating polypeptide-differentiated PC12 cells. Regul. Pept. 2004, 123, 15–21. [Google Scholar] [CrossRef] [PubMed]
- Nicot, A.; DiCicco-Bloom, E. Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc. Natl. Acad. Sci. USA 2001, 98, 4758–4763. [Google Scholar] [CrossRef] [PubMed]
- Basille, M.; Gonzalez, B.; Leroux, P.; Jeandel, L.; Fournier, A.; Vaudry, H. Localization and characterization of PACAP receptors in the rat cerebellum during development: Evidence for a stimulatory effect of PACAP on immature cerebellar granule cells. Neuroscience 1993, 57, 329–338. [Google Scholar] [CrossRef]
- Vaudry, D.; Gonzalez, B.; Basille, M.; Pamantung, T.; Fournier, A.; Vaudry, H. PACAP acts as a neurotrophic factor during histogenesis of the rat cerebellar cortex. Ann. N. Y. Acad. Sci. 2000, 921, 293–299. [Google Scholar] [CrossRef] [PubMed]
- Dénes, V.; Czotter, N.; Lakk, M.; Berta, G.; Gábriel, R. PAC1-expressing structures of neural retina alter their PAC1 isoform splicing during postnatal development. Cell Tissue Res. 2014, 355, 279–288. [Google Scholar] [CrossRef] [PubMed]
- Atlasz, T.; Vaczy, A.; Werling, D.; Kiss, P.; Tamas, A.; Kovacs, K.; Fabian, E.; Kvarik, T.; Mammel, B.; Danyadi, B. Protective effects of PACAP in the retina. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; pp. 501–527. [Google Scholar]
- Spengler, D.; Waeber, C.; Pantaloni, C.; Holsboer, F.; Bockaert, J.; Seeburg, P.H.; Journot, L. Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993, 365, 170–175. [Google Scholar] [PubMed]
- Lucero, M.T. Sniffing out a role for PACAP in the olfactory system. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; pp. 483–499. [Google Scholar]
- Yuan, Z.; Guan, Y.; Wang, L.; Wei, W.; Kane, A.B.; Chin, Y.E. Central role of the threonine residue within the P+1 loop of receptor tyrosine kinase in Stat3 constitutive phosphorylation in metastatic cancer cells. Mol. Cell. Biol. 2004, 24, 9390–9400. [Google Scholar] [CrossRef] [PubMed]
- Kisseleva, T.; Bhattacharya, S.; Braunstein, J.; Schindler, C.W. Signaling through the JAK/Stat pathway, recent advances and future challenges. Gene 2002, 285, 1–24. [Google Scholar] [CrossRef]
- Nishimoto, M.; Furuta, A.; Aoki, S.; Kudo, Y.; Miyakawa, H.; Wada, K. PACAP/PAC1 autocrine system promotes proliferation and astrogenesis in neural progenitor cells. Glia 2007, 55, 317–327. [Google Scholar] [CrossRef] [PubMed]
- Erhardt, N.M.; Sherwood, N.M. PACAP maintains cell cycling and inhibits apoptosis in chick neuroblasts. Mol. Cell. Endocrinol. 2004, 221, 121–134. [Google Scholar] [CrossRef] [PubMed]
- Nicot, A.; Lelievre, V.; Tam, J.; Waschek, J.A.; DiCicco-Bloom, E. Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J. Neurosci. 2002, 22, 9244–9254. [Google Scholar] [PubMed]
- Yan, Y.; Zhou, X.; Pan, Z.; Ma, J.; Waschek, J.A.; DiCicco-Bloom, E. Pro-and anti-mitogenic actions of pituitary adenylate cyclase-activating polypeptide in developing cerebral cortex: Potential mediation by developmental switch of PAC1 receptor mRNA isoforms. J. Neurosci. 2013, 33, 3865–3878. [Google Scholar] [CrossRef] [PubMed]
- Cohen, J.R.; Resnick, D.Z.; Niewiadomski, P.; Dong, H.; Liau, L.M.; Waschek, J.A. Pituitary adenylyl cyclase activating polypeptide inhibits gli1 gene expression and proliferation in primary medulloblastoma derived tumorsphere cultures. BMC Cancer 2010, 10, 676. [Google Scholar] [CrossRef] [PubMed]
- Wojcieszak, J.; Zawilska, J.B. PACAP38 and PACAP6-38 exert cytotoxic activity against human retinoblastoma Y79 cells. J. Mol. Neurosci. 2014, 54, 463–468. [Google Scholar] [CrossRef] [PubMed]
- Hegarty, S.V.; O’Keeffe, G.W.; Sullivan, A.M. Neurotrophic factors: From neurodevelopmental regulators to novel therapies for Parkinson’s disease. Neural Regen. Res. 2014, 9, 1708–1711. [Google Scholar] [PubMed]
- Harada, T.; Morooka, T.; Ogawa, S.; Nishida, E. ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nat. Cell Biol. 2001, 3, 453–459. [Google Scholar] [CrossRef] [PubMed]
- Maisonpierre, P.C.; Belluscio, L.; Friedman, B.; Alderson, R.F.; Wiegand, S.J.; Furth, M.E.; Lindsay, R.M.; Yancopoulos, G.D. NT-3, BDNF, and NGF in the developing rat nervous system: Parallel as well as reciprocal patterns of expression. Neuron 1990, 5, 501–509. [Google Scholar] [CrossRef]
- Kuroda, M.; Muramatsu, R.; Maedera, N.; Koyama, Y.; Hamaguchi, M.; Fujimura, H.; Yoshida, M.; Konishi, M.; Itoh, N.; Mochizuki, H.; et al. Peripherally derived FGF21 promotes remyelination in the central nervous system. J. Clin. Investig. 2017, 127, 3496–3509. [Google Scholar] [CrossRef] [PubMed]
- Arsenijevic, Y.; Weiss, S. Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors: Distinct actions from those of brain-derived neurotrophic factor. J. Neurosci. 1998, 18, 2118–2128. [Google Scholar] [PubMed]
- Bani-Yaghoub, M.; Felker, J.M.; Sans, C.; Naus, C.C. The effects of bone morphogenetic protein 2 and 4 (BMP2 and BMP4) on gap junctions during neurodevelopment. Exp. Neurol. 2000, 162, 13–26. [Google Scholar] [CrossRef] [PubMed]
- Guirland, C.; Buck, K.B.; Gibney, J.A.; DiCicco-Bloom, E.; Zheng, J.Q. Direct cAMP signaling through G-protein-coupled receptors mediates growth cone attraction induced by pituitary adenylate cyclase-activating polypeptide. J. Neurosci. 2003, 23, 2274–2283. [Google Scholar] [PubMed]
- Falluel-Morel, A.; Vaudry, D.; Aubert, N.; Galas, L.; Benard, M.; Basille, M.; Fontaine, M.; Fournier, A.; Vaudry, H.; Gonzalez, B.J. Pituitary adenylate cyclase-activating polypeptide prevents the effects of ceramides on migration, neurite outgrowth, and cytoskeleton remodeling. Proc. Natl. Acad. Sci. USA 2005, 102, 2637–2642. [Google Scholar] [CrossRef] [PubMed]
- DiCicco-Bloom, E.; Lu, N.; Pintar, J.E.; Zhang, J. The PACAP ligand/receptor system regulates cerebral cortical neurogenesis. Ann. N. Y. Acad. Sci. 1998, 865, 274–289. [Google Scholar] [CrossRef] [PubMed]
- Waschek, J.A.; Casillas, R.A.; Nguyen, T.B.; DiCicco-Bloom, E.M.; Carpenter, E.M.; Rodriguez, W.I. Neural tube expression of pituitary adenylate cyclase-activating peptide (PACAP) and receptor: Potential role in patterning and neurogenesis. Proc. Natl. Acad. Sci. USA 1998, 95, 9602–9607. [Google Scholar] [CrossRef] [PubMed]
- Negishi, M.; Oinuma, I.; Katoh, H. Plexins: Axon guidance and signal transduction. Cell. Mol. Life Sci. 2005, 62, 1363–1371. [Google Scholar] [CrossRef] [PubMed]
- Rizo, J.; Südhof, T.C. Snares and Munc18 in synaptic vesicle fusion. Nat. Rev. Neurosci. 2002, 3, 641–653. [Google Scholar] [CrossRef] [PubMed]
- Yoshihara, M.; Adolfsen, B.; Galle, K.T.; Littleton, J.T. Retrograde signaling by Syt 4 induces presynaptic release and synapse-specific growth. Science 2005, 310, 858–863. [Google Scholar] [CrossRef] [PubMed]
- Flynn, K.C. The cytoskeleton and neurite initiation. Bioarchitecture 2013, 3, 86–109. [Google Scholar] [CrossRef] [PubMed]
- Plantier, M.; Fattoum, A.; Menn, B.; Ben-Ari, Y.; Der Terrossian, E.; Represa, A. Acidic calponin immunoreactivity in postnatal rat brain and cultures: Subcellular localization in growth cones, under the plasma membrane and along actin and glial filaments. Eur. J. Neurosci. 1999, 11, 2801–2812. [Google Scholar] [CrossRef] [PubMed]
- Giblin, S.P.; Midwood, K.S. Tenascin-C: Form versus function. Cell Adhes. Migr 2015, 9, 48–82. [Google Scholar] [CrossRef] [PubMed]
- Chung, C.Y.; Murphy-Ullrich, J.E.; Erickson, H.P. Mitogenesis, cell migration, andloss of focal adhesions induced by tenascin-C interacting with its cell surfacereceptor, annexin II. Mol. Biol. Cell 1996, 6, 883–892. [Google Scholar] [CrossRef]
- Galas, L.; Benard, M.; Lebon, A.; Komuro, Y.; Schapman, D.; Vaudry, H.; Vaudry, D.; Komuro, H. Postnatal migration of cerebellar interneurons. Brain Sci. 2017, 7, 62. [Google Scholar] [CrossRef] [PubMed]
- Raoult, E.; Benard, M.; Komuro, H.; Lebon, A.; Vivien, D.; Fournier, A.; Vaudry, H.; Vaudry, D.; Galas, L. Cortical-layer-specific effects of PACAP and tPA on interneuron migration during post-natal development of the cerebellum. J. Neurochem. 2014, 130, 241–254. [Google Scholar] [CrossRef] [PubMed]
- Aubert, N.; Basille, M.; Falluel-Morel, A.; Vaudry, D.; Bucharles, C.; Jolivel, V.; Fisch, C.; de Jouffrey, S.; le Bigot, J.F.; Fournier, A.; et al. Molecular, cellular, and functional characterizations of pituitary adenylate cyclase-activating polypeptide and its receptors in the cerebellum of new and old world monkeys. J. Comp. Neurol. 2007, 504, 427–439. [Google Scholar] [CrossRef] [PubMed]
- Liang, R.; Chen, X.Q.; Bai, Q.X.; Wang, Z.; Zhang, T.; Yang, L.; Dong, B.X.; Gao, G.X.; Gu, H.T.; Zhu, H.F. Increased 14-3-3ζ expression in the multidrug-resistant leukemia cell line HL-60/VCR as compared to the parental line mediates cell growth and apoptosis in part through modification of gene expression. Acta Haematol. 2014, 132, 177–186. [Google Scholar] [CrossRef] [PubMed]
- Allais, A.; Burel, D.; Roy, V.; Arthaud, S.; Galas, L.; Isaac, E.R.; Desfeux, A.; Parent, B.; Fournier, A.; Chapillon, P.; et al. Balanced effect of PACAP and FasL on granule cell death during cerebellar development: A morphological, functional and behavioural characterization. J. Neurochem. 2010, 113, 329–340. [Google Scholar] [CrossRef] [PubMed]
- Yamada, K.; Matsuzaki, S.; Hattori, T.; Kuwahara, R.; Taniguchi, M.; Hashimoto, H.; Shintani, N.; Baba, A.; Kumamoto, N.; Yamada, K. Increased stathmin1 expression in the dentate gyrus of mice causes abnormal axonal arborizations. PLoS ONE 2010, 5, e8596. [Google Scholar] [CrossRef] [PubMed]
- Allais, A.; Burel, D.; Isaac, E.R.; Gray, S.L.; Basille, M.; Ravni, A.; Sherwood, N.M.; Vaudry, H.; Gonzalez, B.J. Altered cerebellar development in mice lacking pituitary adenylate cyclase-activating polypeptide. Eur. J. Neurosci. 2007, 25, 2604–2618. [Google Scholar] [CrossRef] [PubMed]
- Sándor, B.; Fintor, K.; Reglodi, D.; Fulop, D.; Helyes, Z.; Szántó, I.; Nagy, P.; Hashimoto, H.; Tamás, A. Structural and morphometric comparison of lower incisors in PACAP-deficient and wild-type mice. J. Mol. Neurosci. 2016, 59, 300–308. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Farkas, J.; Sandor, B.; Tamas, A.; Kiss, P.; Hashimoto, H.; Nagy, A.D.; Fulop, B.D.; Juhasz, T.; Manavalan, S.; Reglodi, D. Early neurobehavioral development of mice lacking endogenous PACAP. J. Mol. Neurosci. 2017, 61, 468–478. [Google Scholar] [CrossRef] [PubMed]
- Lee, M.; Lelievre, V.; Zhao, P.; Torres, M.; Rodriguez, W.; Byun, J.Y.; Doshi, S.; Ioffe, Y.; Gupta, G.; de los Monteros, A.E.; et al. Pituitary adenylyl cyclase-activating polypeptide stimulates DNA synthesis but delays maturation of oligodendrocyte progenitors. J. Neurosci. 2001, 21, 3849–3859. [Google Scholar] [PubMed]
- Vincze, A.; Reglodi, D.; Helyes, Z.; Hashimoto, H.; Shintani, N.; Abraham, H. Role of endogenous pituitary adenylate cyclase activating polypeptide (PACAP) in myelination of the rodent brain: Lessons from PACAP-deficient mice. Int. J. Dev. Neurosci. 2011, 29, 923–935. [Google Scholar] [CrossRef] [PubMed]
- Vallejo, M. PACAP signaling to dream: A camp-dependent pathway that regulates cortical astrogliogenesis. Mol. Neurobiol. 2009, 39, 90–100. [Google Scholar] [CrossRef] [PubMed]
- Vertongen, P.; Camby, I.; Darro, F.; Kiss, R.; Robberecht, P. VIP and pituitary adenylate cyclase activating polypeptide (PACAP) have an antiproliferative effect on the T98G human glioblastoma cell line through interaction with VIP2 receptor. Neuropeptides 1996, 30, 491–496. [Google Scholar] [CrossRef]
- Waschek, J.A. VIP and PACAP: Neuropeptide modulators of CNS inflammation, injury, and repair. Br. J. Pharmacol. 2013, 169, 512–523. [Google Scholar] [CrossRef] [PubMed]
- Reglodi, D.; Cseh, S.; Somoskoi, B.; Fulop, B.D.; Szentleleky, E.; Szegeczki, V.; Kovacs, A.; Varga, A.; Kiss, P.; Hashimoto, H.; et al. Disturbed spermatogenic signaling in pituitary adenylate cyclase activating polypeptide-deficient mice. Reproduction 2018, 155, 129–139. [Google Scholar] [CrossRef] [PubMed]
- Hattori, S.; Takao, K.; Tanda, K.; Toyama, K.; Shintani, N.; Baba, A.; Hashimoto, H.; Miyakawa, T. Comprehensive behavioral analysis of pituitary adenylate cyclase-activating polypeptide (PACAP) knockout mice. Front. Behav. Neurosci. 2012, 6, 58. [Google Scholar] [CrossRef] [PubMed]
- Farkas, J.; Kovács, L.Á.; Gáspár, L.; Nafz, A.; Gaszner, T.; Ujvári, B.; Kormos, V.; Csernus, V.; Hashimoto, H.; Reglődi, D. Construct and face validity of a new model for the three-hit theory of depression using PACAP mutant mice on CD1 background. Neuroscience 2017, 354, 11–29. [Google Scholar] [CrossRef] [PubMed]
- Shibasaki, Y.; Hayata-Takano, A.; Hazama, K.; Nakazawa, T.; Shintani, N.; Kasai, A.; Nagayasu, K.; Hashimoto, R.; Tanida, M.; Katayama, T.; et al. Atomoxetine reverses locomotor hyperactivity, impaired novel object recognition, and prepulse inhibition impairment in mice lacking pituitary adenylate cyclase-activating polypeptide. Neuroscience 2015, 297, 95–104. [Google Scholar] [CrossRef] [PubMed]
- Kormos, V.; Gaspar, L.; Kovacs, L.A.; Farkas, J.; Gaszner, T.; Csernus, V.; Balogh, A.; Hashimoto, H.; Reglodi, D.; Helyes, Z. Reduced response to chronic mild stress in PACAP mutant mice is associated with blunted FosB expression in limbic forebrain and brainstem centers. Neuroscience 2016, 330, 335–358. [Google Scholar] [CrossRef] [PubMed]
- Hashimoto, H.; Shintani, N.; Tanaka, K.; Mori, W.; Hirose, M.; Matsuda, T.; Sakaue, M.; Miyazaki, J.-I.; Niwa, H.; Tashiro, F. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc. Natl. Acad. Sci. USA 2001, 98, 13355–13360. [Google Scholar] [CrossRef] [PubMed]
- Takuma, K.; Maeda, Y.; Ago, Y.; Ishihama, T.; Takemoto, K.; Nakagawa, A.; Shintani, N.; Hashimoto, H.; Baba, A.; Matsuda, T. An enriched environment ameliorates memory impairments in PACAP-deficient mice. Behav. Brain Res. 2014, 272, 269–278. [Google Scholar] [CrossRef] [PubMed]
- Vaudry, D.; Falluel-Morel, A.; Basille, M.; Pamantung, T.F.; Fontaine, M.; Fournier, A.; Vaudry, H.; Gonzalez, B.J. Pituitary adenylate cyclase-activating polypeptide prevents c2-ceramide-induced apoptosis of cerebellar granule cells. J. Neurosci. Res. 2003, 72, 303–316. [Google Scholar] [CrossRef] [PubMed]
- Takei, N.; Skoglösa, Y.; Lindholm, D. Neurotrophic and neuroprotective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on mesencephalic dopaminergic neurons. J. Neurosci. Res. 1998, 54, 698–706. [Google Scholar] [CrossRef]
- Rozzi, S.J.; Borelli, G.; Ryan, K.; Steiner, J.P.; Reglodi, D.; Mocchetti, I.; Avdoshina, V. PACAP27 is protective against tat-induced neurotoxicity. J. Mol. Neurosci. 2014, 54, 485–493. [Google Scholar] [CrossRef] [PubMed]
- Aubert, N.; Vaudry, D.; Falluel-Morel, A.; Desfeux, A.; Fisch, C.; Ancian, P.; de Jouffrey, S.; Le Bigot, J.-F.; Couvineau, A.; Laburthe, M. PACAP prevents toxicity induced by cisplatin in rat and primate neurons but not in proliferating ovary cells: Involvement of the mitochondrial apoptotic pathway. Neurobiol. Dis. 2008, 32, 66–80. [Google Scholar] [CrossRef] [PubMed]
- Atlasz, T.; Szabadfi, K.; Kiss, P.; Babai, N.; Koszegi, Z.; Tamas, A.; Reglodi, D.; Gabriel, R. PACAP-mediated neuroprotection of neurochemically identified cell types in MSG-induced retinal degeneration. J. Mol. Neurosci. 2008, 36, 97–104. [Google Scholar] [CrossRef] [PubMed]
- Han, P.; Tang, Z.; Yin, J.; Maalouf, M.; Beach, T.G.; Reiman, E.M.; Shi, J. Pituitary adenylate cyclase-activating polypeptide protects against β-amyloid toxicity. Neurobiol. Aging 2014, 35, 2064–2071. [Google Scholar] [CrossRef] [PubMed]
- Ohtaki, H.; Nakamachi, T.; Dohi, K.; Shioda, S. Role of PACAP in ischemic neural death. J. Mol. Neurosci. 2008, 36, 16–25. [Google Scholar] [CrossRef] [PubMed]
- 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. Neuroscience 2008, 151, 63–73. [Google Scholar] [CrossRef] [PubMed]
- Watson, M.B.; Nobuta, H.; Abad, C.; Lee, S.K.; Bala, N.; Zhu, C.; Richter, F.; Chesselet, M.-F.; Waschek, J.A. PACAP deficiency sensitizes nigrostriatal dopaminergic neurons to paraquat-induced damage and modulates central and peripheral inflammatory activation in mice. Neuroscience 2013, 240, 277–286. [Google Scholar] [CrossRef] [PubMed]
- Uchida, D.; Arimura, A.; Somogyvari-Vigh, A.; Shioda, S.; Banks, W.A. Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide. Brain Res. 1996, 736, 280–286. [Google Scholar] [CrossRef]
- Reglodi, D.; Somogyvari-Vigh, A.; Vigh, S.; Kozicz, T.; Arimura, A. Delayed systemic administration of PACAP38 is neuroprotective in transient middle cerebral artery occlusion in the rat. Stroke 2000, 31, 1411–1417. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Reglodi, D.; Tamas, A.; Somogyvari-Vigh, A.; Szanto, Z.; Kertes, E.; Lenard, L.; Arimura, A.; Lengvari, I. Effects of pretreatment with PACAP on the infarct size and functional outcome in rat permanent focal cerebral ischemia. Peptides 2002, 23, 2227–2234. [Google Scholar] [CrossRef]
- Lamine, A.; Letourneau, M.; Doan, N.D.; Maucotel, J.; Couvineau, A.; Vaudry, H.; Chatenet, D.; Vaudry, D.; Fournier, A. Characterizations of a synthetic pituitary adenylate cyclase-activating polypeptide analog displaying potent neuroprotective activity and reduced in vivo cardiovascular side effects in a Parkinson’s disease model. Neuropharmacology 2016, 108, 440–450. [Google Scholar] [CrossRef] [PubMed]
- Tamas, A.; Lubics, A.; Lengvari, I.; Reglodi, D. Protective effects of PACAP in excitotoxic striatal lesion. Ann. N. Y. Acad. Sci. 2006, 1070, 570–574. [Google Scholar] [CrossRef] [PubMed]
- Polanco, M.J.; Parodi, S.; Piol, D.; Stack, C.; Chivet, M.; Contestabile, A.; Miranda, H.C.; Lievens, P.M.; Espinoza, S.; Jochum, T.; et al. Adenylyl cyclase activating polypeptide reduces phosphorylation and toxicity of the polyglutamine-expanded androgen receptor in spinobulbar muscular atrophy. Sci. Transl. Med. 2016, 8, 370ra181. [Google Scholar] [CrossRef] [PubMed]
- Kovesdi, E.; Tamas, A.; Reglodi, D.; Farkas, O.; Pal, J.; Toth, G.; Bukovics, P.; Doczi, T.; Buki, 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] [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. Neuroinflamm. 2012, 9, 256. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Samal, B.; Hamelink, C.R.; Xiang, C.C.; Chen, Y.; Chen, M.; Vaudry, D.; Brownstein, M.J.; Hallenbeck, J.M.; Eiden, L.E. Neuroprotection by endogenous and exogenous PACAP following stroke. Regul. Pept. 2006, 137, 4–19. [Google Scholar] [CrossRef][Green Version]
- Araki, T.; Milbrandt, J. Ninjurin, a novel adhesion molecule, is induced by nerve injury and promotes axonal growth. Neuron 1996, 17, 353–361. [Google Scholar] [CrossRef]
- Brifault, C.; Gras, M.; Liot, D.; May, V.; Vaudry, D.; Wurtz, O. Delayed pituitary adenylate cyclase–activating polypeptide delivery after brain stroke improves functional recovery by inducing m2 microglia/macrophage polarization. Stroke 2015, 46, 520–528. [Google Scholar] [CrossRef] [PubMed]
- Rogalla, T.; Ehrnsperger, M.; Preville, X.; Kotlyarov, A.; Lutsch, G.; Ducasse, C.; Paul, C.; Wieske, M.; Arrigo, A.P.; Buchner, J.; et al. Regulation of Hsp27 oligomerization, chaperone function, and protective activity against oxidative stress/tumor necrosis factor alpha by phosphorylation. J. Biol. Chem. 1999, 274, 18947–18956. [Google Scholar] [CrossRef] [PubMed]
- Rhee, S.G.; Kang, S.W.; Chang, T.S.; Jeong, W.; Kim, K. Peroxiredoxin, a novel family of peroxidases. IUBMB Life 2001, 52, 35–41. [Google Scholar] [CrossRef] [PubMed]
- Shendelman, S.; Jonason, A.; Martinat, C.; Leete, T.; Abeliovich, A. DJ-1 is a redox-dependent molecular chaperone that inhibits alpha-synuclein aggregate formation. PLoS Biol. 2004, 11, e362. [Google Scholar]
- Hayes, J.D.; Flanagan, J.U.; Jowsey, I.R. Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 2005, 45, 51–88. [Google Scholar] [CrossRef] [PubMed]
- Brifault, C.; Vaudry, D.; Wurtz, O. The neuropeptide PACAP, a potent disease modifier candidate for brain stroke treatment. In Pituitary Adenylate Cyclase Activating Polypeptide—PACAP; Springer: Cham, Switzerland, 2016; Volume 11, pp. 583–606. [Google Scholar]
- Reglodi, D.; Vaczy, A.; Rubio-Beltran, E.; MaassenVanDenBrink, A. Protective effects of PACAP in ischemia. J. Headache Pain 2018, 19, 19. [Google Scholar] [CrossRef] [PubMed]
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Rivnyak, A.; Kiss, P.; Tamas, A.; Balogh, D.; Reglodi, D. Review on PACAP-Induced Transcriptomic and Proteomic Changes in Neuronal Development and Repair. Int. J. Mol. Sci. 2018, 19, 1020. https://doi.org/10.3390/ijms19041020
Rivnyak A, Kiss P, Tamas A, Balogh D, Reglodi D. Review on PACAP-Induced Transcriptomic and Proteomic Changes in Neuronal Development and Repair. International Journal of Molecular Sciences. 2018; 19(4):1020. https://doi.org/10.3390/ijms19041020
Chicago/Turabian StyleRivnyak, Adam, Peter Kiss, Andrea Tamas, Dorottya Balogh, and Dora Reglodi. 2018. "Review on PACAP-Induced Transcriptomic and Proteomic Changes in Neuronal Development and Repair" International Journal of Molecular Sciences 19, no. 4: 1020. https://doi.org/10.3390/ijms19041020
APA StyleRivnyak, A., Kiss, P., Tamas, A., Balogh, D., & Reglodi, D. (2018). Review on PACAP-Induced Transcriptomic and Proteomic Changes in Neuronal Development and Repair. International Journal of Molecular Sciences, 19(4), 1020. https://doi.org/10.3390/ijms19041020