Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration

Developmental Neuroscience

Volumn 24, Issue 1, 2002, Pages 14-23

  Waschek, James A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Astrocyte; Axotomy; External granule layer; Holoprosencephaly; Microglia; Mitogen activating protein kinase; Mitosis; Nerve crush; Neurite outgrowth; Neuroblast; Oligodendrocyte; Patterning; Proliferation; Splice variant; Transection injury

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; FIBROBLAST GROWTH FACTOR; FORSKOLIN; GREEN FLUORESCENT PROTEIN; HOMEODOMAIN PROTEIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR ANTIBODY; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN 3 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PHOSPHOLIPASE D; PITUITARY ADENYLATE CYCLASE 1; PROTEIN KINASE P60; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE;

APOPTOSIS; BRAIN DEVELOPMENT; CELL ISOLATION; CELL MATURATION; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOME 18P; DNA SYNTHESIS; EXPERIMENTAL MODEL; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HOLOPROSENCEPHALY; IN SITU HYBRIDIZATION; IN VIVO STUDY; MYELINATION; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NERVE INJURY; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; TISSUE CULTURE CELL; UPREGULATION;

ANIMALS; BRAIN; CELL DIVISION; CELLS, CULTURED; CYTOKINES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; NERVE GROWTH FACTORS; NERVE REGENERATION; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; NERVOUS SYSTEM MALFORMATIONS; NEURITES; NEUROGLIA; NEURONS; NEUROPEPTIDES; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; RATS; TRAUMA, NERVOUS SYSTEM;

EID: 0036971940     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000064942     Document Type: Review

References (76)

1. Vaudry D, Gonzalez BJ, 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.
2. Waschek JA: Vasoactive intestinal peptide: An important trophic factor and developmental regulator? Dev Neurosci 1995;17:1-7.
3. Ishihara T, Shigemoto R, Mori K, Takahashi K, Nagata S: Functional expression and tissue distribution of a novel receptor for vasoactive intestinal polypeptide. Neuron 1992;8:811-819.
4. 2 receptor: Molecular characterization of a cDNA encoding a novel receptor for vasoactive intestinal peptide. FEBS Lett 1993;334:3-8.
5. Pisegna JR, Wank SA: Molecular cloning and functional expression of the pituitary adenylate-activating polypeptide type I receptor. Proc Natl Acad Sci USA 1993;90:6345-6349.
6. Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg PH, Journot L: Differential signal transduction by five splice variants of the PACAP receptor. Nature 1993;365:170-175.
7. Journot L, Waeber C, Pantaloni C, Holsboer F, Seeburg PH, Bockaert J, Spengler D: Differential signal transduction by six splice variants of the pituitary adenylate cyclase-activating peptide (PACAP) receptor. Biochem Soc Trans 1995;23:133-137.
8. Pisegna JR, Wank SA: Cloning and characterization of the signal transduction of four splice variants of the human pituitary adenylate cyclase activating polypeptide receptor. J Biol Chem 1996;271:17267-17274.
9. Pantaloni C, Brabet P, Bilanges B, Dumuis A, Houssami S, Spengler D, Bockaert J, Journot L: Alternative splicing in the N-terminal extracellular domain of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor modulates receptor selectivity and relative potencies of PACAP-27 and PACAP-38 in phospholipase C activation. J Biol Chem 1996;271:22146-22151.
10. Chatterjee TK, Sharma RV, Fisher RA: Molecular cloning of a novel variant of the pituitary adenylate cyclase-activating polypeptide (PACAP) receptor that stimulates calcium influx by activation of L-type calcium channels. J Biol Chem 1996;271:32226-32232.
11. 2+ influx activates a constitutive NOS in dispersed gastric muscle cells. Am J Physiol 1993;265:G600-G671.
12. Morisset J, Douziech N, Rydzewska G, Buscail L, Rivard N: Cell signalling pathway involved in PACAP-induced AR4-2J cell proliferation. Cell Signal 1995;7:195-205.
13. Straub SG, Sharp GW: A wortmannin-sensitive signal transduction pathway involved in the stimulation of insulin release by vasoactive intestinal polypeptide and pituitary adenylate cyclase-activating polypeptide. J Biol Chem 1996;271:1660-1668.
14. Koh SW: Signal transduction through the vasoactive intestinal peptide receptor stimulates phosphorylation of the kinase pp60c-Src. Biochem Biophys Res Commun 1991;174:452-458.
15. Villalba M, Bockaert J, Journot L: Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 1997;17:83-90.
16. Barrie AF, Clohessy AM, Buensuceso CS, Rogers MV, Allen JM: Pituitary adenylyl cyclase-activating peptide stimulates extracellular signal-regulated kinase 1 or 2 (ERK1/2) activity in ras-independent, mitogen-activated protein kinase/ERK kinase 1- or 2-dependent manner in PC12 cells. J Biol Chem 1997;272:19666-19671.
17. Lelièvre V, Pineau N, Du J, Wen C-H, Nguyen TB, Janet J, Muller J-M, Waschek JA: Differential effects of peptide histidine isoleucine (PHI) and related peptides on stimulation and suppression on neuroblastoma cell proliferation: A novel VIP-independent action of PHI via MAPkinase. J Biol Chem 1998;273:19685-19690.
18. Tatsuno I, Somogyvari-Vigh A, Arimura A: Developmental changes of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptor in the rat brain. Peptides 1994;15:55-60.
19. Basille M, Gonzalez BJ, 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.
20. Waschek JA, Casillas RA, Nguyen TB, DiCicco-Bloom EM, Carpenter EM, Rodriguez WI: 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.
21. Sheward WJ, Lutz EM, Copp AJ, Harmar AJ: Expression of PACAP, and PACAP type 1 (PAC1) receptor mRNA during development of the mouse embryo. Dev Brain Res 1998;109:245-253.
22. Sheward WJ, Lutz EM, Harmar AJ: Expression of pituitary adenylate cyclase activating polypeptide receptors in the early mouse embryo as assessed by reverse transcription polymerase chain reaction and in situ hybridisation. Neurosci Lett 1996;216:45-48.
23. Shuto Y, Uchida D, Onda H, Arimura A: Ontogeny of pituitary adenylate cyclase activating polypeptide and its receptor mRNA in the mouse brain. Regul Pept 1996;67:79-83.
24. Zhou CJ, Shioda S, Shibanuma M, Nakajo S, Funahashi H, Nakai Y, Arimura A, Kikuyama S: Pituitary adenylate cyclase-activating polypeptide receptors during development: Expression in the rat embryo at primitive streak stage. Neuroscience 1999;93:375-391.
25. Zhou C, Kikuyama S, Nakajo S, Hirabayashi T, Mizushima H, Shioda S: Splice variants of PAC(1) receptor during early neural development of rats. Peptides 2000;21:1177-1183.
26. Zhou CJ, Yada T, Kohno D, Kikuyama S, Suzuki R, Mizushima H, Shioda S: PACAP activates PKA, PKC and Ca(2+) signaling cascades in rat neuroepithelial cells. Peptides 2001;22:1111-1117.
27. 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.
28. Lee M, Lelièvre V, Zhao P, Torres M, Rodriguez W, Byun JY, Doshi S, Ioffe Y, Gupta G, de los Monteros AE, de Vellis J, Waschek J: Pituitary adenylyl cyclase-activating polypeptide stimulates DNA synthesis but delays maturation of oligodendrocyte progenitors. J Neurosci 2001;21:3849-3859.
29. Lelièvre V, Hu Z, Byun J-B, Ioffe Y, Waschek J: FGF-2 converts PACAP growth action on embryonic hindbrain precursors from stimulation to inhibition. J Neurosci Res 2002;67:566-573.
30. DiCicco-Bloom E, Deutsch PJ, Maltzman J, Zhang J, Pintar JE, Zheng J, Friedman WF, Zhou X, Zaremba T: Autocrine expression and ontogenetic functions of the PACAP ligand/receptor system during sympathetic development. Dev Biol 2000;219:197-213.
31. Lu N, DiCicco-Bloom E: Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc Natl Acad Sci USA 1997;94:3357-3362.
32. Frechilla D, Garcia-Osta A, Palacios S, Cenarruzabeitia E, Del Rio J: BDNF mediates the neuroprotective effects of PACAP-38 on rat cortical neurons. Neuroreport 2001;12:919-923.
33. Pellegri G, Magistretti PJ, Martin JL: VIP and PACAP potentiate the action of glutamate on BDNF expression in mouse cortical neurones. Eur J Neurosci 1998;10:272-280.
34. Gonzalez BJ, Basille M, Vaudry D, Fournier A, Vaudry H: Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Neuroscience 1997;78:419-430.
35. Villalba M, Bockaert J, Journot L: Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 1997;17:83-90.
36. Chang JY, Korolev VV, Wang JZ: Cyclic AMP and pituitary adenylate cyclase-activating polypeptide (PACAP) prevent programmed cell death of cultured rat cerebellar granule cells. Neurosci Lett 1996;206:181-184.
37. Cavallaro S, Copani A, D'Agata V, Musco S, Petralia S, Ventra C, Stivala F, Travali S, Canonico PL: Pituitary adenylate cyclase activating polypeptide prevents apoptosis in cultured cerebellar granule neurons. Mol Pharmacol 1996;50:60-66.
38. Campard PK, Crochemore C, Rene F, Monnier D, Koch B, Loeffler JP: PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. DNA Cell Biol 1997;16:323-333.
39. Hansel DE, May V, Eipper BA, Ronnett GV: Pituitary adenylyl cyclase-activating peptides and alpha-amidation in olfactory neurogenesis and neuronal survival in vitro. J Neurosci 2001;21:4625-4636.
40. Lioudyno M, Skoglosa Y, Takei N, Lindholm D: Pituitary adenylate cyclase-activating polypeptide (PACAP) protects dorsal root ganglion neurons from death and induces calcitonin gene-related peptide (CGRP) immunoreactivity in vitro. J Neurosci Res 1998;51:243-256.
41. Arimura A, Somogyvari-Vigh A, Weill C, Fiore RC, Tatsuno I, Bay V, Brenneman DE: PACAP functions as a neurotrophic factor. Ann NY Acad Sci 1994;739:228-243.
42. Takei N, Skoglosa Y, Lindholm D: Neurotrophic and neuroprotective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on mesencephalic dopaminergineurons. J Neurosci Res 1998;54:698-706.
43. Takei N, Torres E, Yuhara A, Jongsma H, Otto C, Korhonen L, Abiru Y, Skoglosa Y, Schutz G, Hatanaka H, Sofroniew MV, Lindholm D: Pituitary adenylate cyclase-activating polypeptide promotes the survival of basal forebrain cholinergic neurons in vitro and in vivo: Comparison with effects of nerve growth factor. Eur J Neurosci 2000;12:2273-2280.
44. Tatsuno I, Morio H, Tanaka T, Uchida D, Hirai A, Tamura Y, Saito Y: Pituitary adenylate cyclase-activating polypeptide (PACAP) is a regulator of astrocytes: PACAP stimulates proliferation and production of interleukin 6 (IL-6), but not nerve growth factor (NGF), in cultured rat astrocyte. Ann NY Acad Sci 1996;805:482-488.
45. Gottschall PE, Tatsuno I, Arimura A: Regulation of interleukin-6 (IL-6) secretion in primary cultured rat astrocytes: Synergism of interleukin-1 (IL-1) and pituitary adenylate cyclase activating polypeptide (PACAP). Brain Res 1994;637:197-203.
46. Kim WK, Kann Y, Ganea D, Hart RP, Gozes I, Jonakait GM: Vasoactive intestinal peptide and pituitary adenylyl cyclase-activating polypeptide inhibit tumor necrosis factor-alpha production in injured spinal cord and in activated microglia via a cAMP-dependent pathway. J Neurosci 2000;20:3622-3630.
47. Pincus DW, DiCicco-Bloom EM, Black IB: Vasoactive intestinal peptide regulates mitosis, differentiation and survival of cultured sympathetic neuroblasts. Nature 1990;343:564-567.
48. Pincus DW, DiCicco-Bloom EM, Black IB: Trophic mechanisms regulate mitotic neuronal precursors: Role of vasoactive intestinal peptide (VIP). Brain Res 1994;663:51-60.
49. Lu N, Zhou R, DiCicco-Bloom E: Opposing mitogenic regulation by PACAP in sympathetic and cerebral cortical precursors correlates with differential expression of PACAP receptor (PAC1-R) isoforms. J Neurosci Res 1998;53:651-662.
50. Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E: PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat Neurosci 2001;4:123-124.
51. Skoglosa Y, Takei N, Lindholm D: Distribution of pituitary adenylate cyclase activating polypeptide mRNA in the developing rat brain. Brain Res Mol Brain Res 1999;65:1-13.
52. Nielsen HS, Hannibal J, Fahrenkrug J: Expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the postnatal and adult rat cerebellar cortex. Neuroreport 1998;9:2639-2642.
53. Vaudry D, Gonzalez BJ, Basille M, Anouar Y, Fournier A, Vaudry H: Pituitary adenylate cyclase-activating polypeptide stimulates both c-fos gene expression and cell survival in rat cerebellar granule neurons through activation of the protein kinase A pathway. Neuroscience 1998;84:801-812.
54. Vaudry D, Gonzalez BJ, Basille M, Pamantung TF, Fontaine M, Fournier A, Vaudry H: The neuroprotective effect of pituitary adenylate cyclase-activating polypeptide on cerebellar granule cells is mediated through inhibition of the CED3-related cysteine protease caspase-3/CPP32. Proc Natl Acad Sci USA 2000;97:13390-13395.
55. DiCicco-Bloom E, Emsb K, Black IB: VIP regulates development of multiple neuronal populations: Sensory and cerebellar granule cells. Soc Neurosci 1992;18:418.
56. Vaudry D, Gonzalez BJ, Basille M, Fournier A, Vaudry H: Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development. Proc Natl Acad Sci USA 1999;96:9415-9420.
57. Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E: PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat Neurosci 2001;4:123-124.
58. Chang E, Welch S, Luna J, Giacalone J, Francke U: Generation of a human chromosome 18-specific YAC clone collection and mapping of 55 unique YACs by FISH and fingerprinting. Genomics 1993;17:393-402.
59. Overhauser J, Mitchell HF, Zackai EH, Tick DB, Rojas K, Muenke M: Physical mapping of the holoprosencephaly critical region in 18p11.3. Am J Hum Genet 1995;57:1080-1085.
60. Mackay M, Fantes J, Scherer S, Boyle S, West K, Tsui LC, Belloni E, Lutz E, Van Heyningen V, Harmar AJ: Chromosomal localization in mouse and human of the vasoactive intestinal peptide receptor type 2 gene: A possible contributor to the holoprosencephaly 3 phenotype. Genomics 1996;37:345-353.
61. Przywara DA, Kulkarni JS, Wakade TD, Leontiev DV, Wakade AR: Pituitary adenylyl cyclase-activating polypeptide and nerve growth factor use the proteasome to rescue nerve growth factor-deprived sympathetic neurons cultured from chick embryos. J Neurochem 1998;71:1889-1897.
62. Zhou X, Rodriguez WI, Casillas RA, Ma V, Tam J, Hu Z, Lelièvre V, Chao A, Waschek JA: Axotomy-induced changes in pituitary adenylate cyclase activating polypeptide (PACAP) and PACAP receptor gene expression in the adult rat facial motor nucleus. J Neurosci Res 1999;57:953-961.
63. Moller K, Reimer M, Ekblad E, Hannibal J, Fahrenkrug J, Kanje M, Sundler F: The effects of axotomy and preganglionic denervation on the expression of pituitary adenylate cyclase activating peptide (PACAP), galanin and PACAP type 1 receptors in the rat superior cervical ganglion. Brain Res 1997;775:166-182.
64. Zhang YZ, Hannibal J, Zhao Q, Moller K, Danielsen N, Fahrenkrug J, Sundler F: Pituitary adenylate cyclase activating peptide expression in the rat dorsal root ganglia: Up-regulation after peripheral nerve injury. Neuroscience 1996;74:1099-1110.
65. Skoglosa Y, Lewen A, Takei N, Hillered L, Lindholm D: Regulation of pituitary adenylate cyclase activating polypeptide and its receptor type 1 after traumatic brain injury: Comparison with brain-derived neurotrophic factor and the induction of neuronal cell death. Neuroscience 1997;90:235-247.
66. Shin CM, Chung YH, Kim MJ, Cha CI: Spatial and temporal distribution of pituitary adenylate cyclase activating polypeptide in gerbil global cerebral ischemia. Neurosci Lett 2001;309:53-56.
67. Gillardon F, Hata R, Hossmann KA: Delayed up-regulation of Zac1 and PACAP type I receptor after transient focal cerebral ischemia in mice. Brain Res Mol Brain Res 1998;61:207-210.
68. Uchida D, Arimura A, Somogyvari-Vigh A, Shioda S, Banks WA: Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide. Brain Res 1996;736:280-286.
69. 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.
70. Takei N, Torres E, Yuhara A, Jongsma H, Otto C, Korhonen L, Abiru Y, Skoglosa Y, Schutz G, Hatanaka H, Sofroniew MV, Lindholm D: Pituitary adenylate cyclase-activating polypeptide promotes the survival of basal forebrain cholinergic neurons in vitro and in vivo comparison with effects of nerve growth factor. Eur J Neurosci 2000;12:2273-2280.
71. Morio H, Tatsuno I, Hirai A, Tamura Y, Saito Y: Pituitary adenylate cyclase-activating polypeptide protects rat-cultured cortical neurons from glutamate-induced cytotoxicity. Brain Res 1996;741:82-88.
72. Ito Y, Arakawa M, Ishige K, Fukuda H: Comparative study of survival signal withdrawal- and 4-hydroxynonenal-induced cell death in cerebellar granule cells. Neurosci Res 1999;35:321-327.
73. Bellinger DL, Lorton D, Brouxhon S, Felten S, Felten DL: The significance of vasoactive intestinal polypeptide (VIP) in immunomodulation. Adv Neuroimmunol 1996;6:5-27.
74. Ganea D: Regulatory effects of vasoactive intestinal peptide on cytokine production in central and peripheral lymphoid organs. Adv Neuroimmunol 1996;6:61-74.
75. De la Fuente M, Delgado M, Gomariz RP: VIP modulation of immune cell functions. Adv Neuroimmunol 1996;6:75-91.
76. Goetzl EJ, Pankhaniya RR, Gaufo GO, Mu Y, Xia M, Sreedharan SP: Selectivity of effects of vasoactive intestinal peptide on macrophages and lymphocytes in compartmental immune responses. Ann NY Acad Sci 1998;840:540-550.