Role of PACAP in the physiology and pathology of the sympathoadrenal system

Frontiers in Neuroendocrinology

Volumn 29, Issue 1, 2008, Pages 128-141

  Ghzili, Hafida ^a   Grumolato, Luca ^a   Thouënnon, Erwan ^a   Tanguy, Yannick ^a   Turquier, Valérie ^a   Vaudry, Hubert ^a   Anouar, Youssef ^a  

^a UNIVERSITÉ DE ROUEN   (France)

Author keywords

Catecholamines; Chromaffin cells; Differentiation; Neuroblastoma; Neuropeptides; PACAP; Pheochromocytoma; Sympathetic neurons; Transcriptome

Indexed keywords

CATECHOLAMINE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE;

ADRENERGIC SYSTEM; CATECHOLAMINE SYNTHESIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MIGRATION; CELL PROLIFERATION; CHROMAFFIN CELL; ENVIRONMENTAL FACTOR; HUMAN; NEURAL CREST; NEUROBLAST; NEUROBLASTOMA; PATHOPHYSIOLOGY; PHENOTYPE; PHEOCHROMOCYTOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SYMPATHETIC NERVE CELL; TRANSCRIPTOMICS; TUMOR CELL LINE;

ADRENAL GLAND NEOPLASMS; ADRENAL GLANDS; ANIMALS; CELL DIFFERENTIATION; CHROMAFFIN CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEUROBLASTOMA; PHEOCHROMOCYTOMA; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; SYMPATHETIC NERVOUS SYSTEM;

EID: 37649009936     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2007.10.001     Document Type: Review

References (175)

1. Ait-Ali D., Turquier V., Grumolato L., Yon L., Jourdain M., Alexandre D., Eiden L.E., Vaudry H., and Anouar Y. The proinflammatory cytokines tumor necrosis factor-alpha and interleukin-1 stimulate neuropeptide gene transcription and secretion in adrenochromaffin cells via activation of extracellularly regulated kinase 1/2 and p38 protein kinases, and activator protein-1 transcription factors. Mol. Endocrinol. 18 (2004) 1721-1739
2. Anderson C.R., Bergner A., and Murphy S.M. How many types of cholinergic sympathetic neuron are there in the rat stellate ganglion?. Neuroscience 140 (2006) 567-576
3. Anderson D.J., Carnahan J.F., Michelsohn A., and Patterson P.H. Antibody markers identify a common progenitor to sympathetic neurons and chromaffin cells in vivo and reveal the timing of commitment to neuronal differentiation in the sympathoadrenal lineage. J. Neurosci. 11 (1991) 3507-3519
4. Anderson D.J. Molecular control of cell fate in the neural crest: the sympathoadrenal lineage. Annu. Rev. Neurosci. 16 (1993) 129-158
5. Anouar Y., and Eiden L.E. Rapid and long-lasting increase in galanin mRNA levels in rat adrenal medulla following insulin-induced reflex splanchnic nerve stimulation. Neuroendocrinology 62 (1995) 611-618
6. Anouar Y., Lee H.W., and Eiden L.E. Both inducible and constitutive activator protein-1-like transcription factors are used for transcriptional activation of the galanin gene by different first and second messenger pathways. Mol. Pharmacol. 56 (1999) 162-169
7. Babinski K., Bodart V., Roy M., De Lean A., and Ong H. Pituitary adenylate-cyclase activating polypeptide (PACAP) evokes long-lasting secretion and de novo biosynthesis of bovine adrenal medullary neuropeptides. Neuropeptides 30 (1996) 572-582
8. Beaudet M.M., Braas K.M., and May V. Pituitary adenylate cyclase activating polypeptide (PACAP) expression in sympathetic preganglionic projection neurons to the superior cervical ganglion. J. Neurobiol. 36 (1998) 325-336
9. Beaudet M.M., Parsons R.L., Braas K.M., and May V. Mechanisms mediating pituitary adenylate cyclase-activating polypeptide depolarization of rat sympathetic neurons. J. Neurosci. 20 (2000) 7353-7361
10. Bilodeau M.L., Boulineau T., Hullinger R.L., and Andrisani O.M. Cyclic AMP signaling functions as a bimodal switch in sympathoadrenal cell development in cultured primary neural crest cells. Mol. Cell. Biol. 20 (2000) 3004-3014
11. Birren S.J., Lo L., and Anderson D.J. Sympathetic neuroblasts undergo a developmental switch in trophic dependence. Development 119 (1993) 597-610
12. Boeshore K.L., Schreiber R.C., Vaccariello S.A., Sachs H.H., Salazar R., Lee J., Ratan R.R., Leahy P., and Zigmond R.E. Novel changes in gene expression following axotomy of a sympathetic ganglion: a microarray analysis. J. Neurobiol. 59 (2004) 216-235
13. Braas K.M., and May V. Pituitary adenylate cyclase-activating polypeptides directly stimulate sympathetic neuron neuropeptide Y release through PAC(1) receptor isoform activation of specific intracellular signaling pathways. J. Biol. Chem. 274 (1999) 27702-27710
14. Brandenburg C.A., May V., and Braas K.M. Identification of endogenous sympathetic neuron pituitary adenylate cyclase-activating polypeptide (PACAP): depolarization regulates production and secretion through induction of multiple propeptide transcripts. J. Neurosci. 17 (1997) 4045-4055
15. Carey R.G., Li B., and DiCicco-Bloom E. Pituitary adenylate cyclase activating polypeptide anti-mitogenic signaling in cerebral cortical progenitors is regulated by p57Kip2-dependent CDK2 activity. J. Neurosci. 22 (2002) 1583-1591
16. Chik C.L., Inukai T., Ogiwara T., Boyd H., Li B., Karpinski E., and Ho A.K. Characterization of pituitary adenylate cyclase-activating polypeptide 38 (PACAP38)-, PACAP27-, and vasoactive intestinal peptide-stimulated responses in N1E-115 neuroblastoma cells. J. Neurochem. 67 (1996) 1005-1013
17. Conconi M.T., Spinazzi R., and Nussdorfer G.G. Endogenous ligands of PACAP/VIP receptors in the autocrine-paracrine regulation of the adrenal gland. Int. Rev. Cytol. 249 (2006) 1-51
18. Corbitt J., Vivekananda J., Wang S.S., and Strong R. Transcriptional and posttranscriptional control of tyrosine hydroxylase gene expression during persistent stimulation of pituitary adenylate cyclase-activating polypeptide receptors on PC12 cells: regulation by protein kinase A-dependent and protein kinase A-independent pathways. J. Neurochem. 71 (1998) 478-486
19. Corbitt J., Hagerty T., Fernandez E., Morgan W.W., and Strong R. Transcriptional and post-transcriptional regulation of tyrosine hydroxylase messenger RNA in PC12 cells during persistent stimulation by VIP and PACAP38: differential regulation by protein kinase A and protein kinase C-dependent pathways. Neuropeptides 36 (2002) 34-45
20. Cowen T., and Gavazzi I. Plasticity in adult and ageing sympathetic neurons. Prog. Neurobiol. 54 (1998) 249-288
21. Deutsch P.J., and Sun Y. The 38-amino acid form of pituitary adenylate cyclase-activating polypeptide stimulates dual signaling cascades in PC12 cells and promotes neurite outgrowth. J. Biol. Chem. 267 (1992) 5108-5113
22. Deutsch P.J., Schadlow V.C., and Barzilai N. 38-Amino acid form of pituitary adenylate cyclase activating peptide induces process outgrowth in human neuroblastoma cells. J. Neurosci. Res. 35 (1993) 312-320
23. DiCicco-Bloom E., Deutsch P.J., Maltzman J., Zhang J., Pintar J.E., Zheng J., Friedman W.F., Zhou X., and Zaremba T. Autocrine expression and ontogenetic functions of the PACAP ligand/receptor system during sympathetic development. Dev. Biol. 219 (2000) 197-213
24. Doupe A.J., Landis S.C., and Patterson P.H. Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J. Neurosci. 5 (1985) 2119-2142
25. Drahushuk K., Connell T.D., and Higgins D. Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal peptide inhibit dendritic growth in cultured sympathetic neurons. J. Neurosci. 22 (2002) 6560-6569
26. Fahrenkrug J., Buhl T., and Hannibal J. PreproPACAP-derived peptides occur in VIP-producing tumours and co-exist with VIP. Regul. Pept. 58 (1995) 89-98
27. Falluel-Morel A., Aubert N., Vaudry D., Basille M., Fontaine M., Fournier A., Vaudry H., and Gonzalez B.J. Opposite regulation of the mitochondrial apoptotic pathway by C2-ceramide and PACAP through a MAP-kinase-dependent mechanism in cerebellar granule cells. J. Neurochem. 91 (2004) 1231-1243
28. Falluel-Morel A., Vaudry D., Aubert N., Galas L., Bernard M., Basille M., Fontaine M., Fournier A., Vaudry H., and Gonzales B.J. Effects of PACAP and C2-ceramide on motility of cerebellar granule neurons: the fastest is not the farthest. Med. Sci. 21 (2005) 696-698
29. Fann M.J., and Patterson P.H. Depolarization differentially regulates the effects of bone morphogenetic protein (BMP)-2, BMP-6, and activin A on sympathetic neuronal phenotype. J. Neurochem. 63 (1994) 2074-2079
30. Finotto S., Krieglstein K., Schober A., Deimling F., Lindner K., Bruhl B., Beier K., Metz J., Garcia-Arraras J.E., Roig-Lopez J.L., Monaghan P., Schmid W., Cole T.J., Kellendonk C., Tronche F., Schutz G., and Unsicker K. Analysis of mice carrying targeted mutations of the glucocorticoid receptor gene argues against an essential role of glucocorticoid signalling for generating adrenal chromaffin cells. Development 126 (1999) 2935-2944
31. Francis N.J., and Landis S.C. Cellular and molecular determinants of sympathetic neuron development. Annu. Rev. Neurosci. 22 (1999) 541-566
32. Frodin M., Hannibal J., Wulff B.S., Gammeltoft S., and Fahrenkrug J. Neuronal localization of pituitary adenylate cyclase-activating polypeptide 38 in the adrenal medulla and growth-inhibitory effect on chromaffin cells. Neuroscience 65 (1995) 599-608
33. Ganea D., and Delgado M. Vasoactive intestinal peptide (VIP) and pituitary adenylate cyclase-activating polypeptide (PACAP) as modulators of both innate and adaptive immunity. Crit. Rev. Oral Biol. Med. 13 (2002) 229-237
34. Garcia-Castro M., and Bronner-Fraser M. Induction and differentiation of the neural crest. Curr. Opin. Cell Biol. 11 (1999) 695-698
35. Ghzili H., Grumolato L., Thouennon E., Vaudry H., and Anouar Y. Possible implication of the transcriptional regulator Id3 in PACAP-induced pro-survival signaling during PC12 cell differentiation. Regul. Pept. 137 (2006) 89-94
36. Ginty D.D., Fanger G.R., Wagner J.A., and Maue R.A. The activity of cAMP-dependent protein kinase is required at a posttranslational level for induction of voltage-dependent sodium channels by peptide growth factors in PC12 cells. J. Cell Biol. 116 (1992) 1465-1473
37. Girard B.M., May V., Bora S.H., Fina F., and Braas K.M. Regulation of neurotrophic peptide expression in sympathetic neurons: quantitative analysis using radioimmunoassay and real-time quantitative polymerase chain reaction. Regul. Pept. 109 (2002) 89-101
38. Girard B.M., Keller E.T., Schutz K.C., May V., and Braas K.M. Pituitary adenylate cyclase activating polypeptide and PAC1 receptor signaling increase Homer 1a expression in central and peripheral neurons. Regul. Pept. 123 (2004) 107-116
39. Goldstein R.S., Avivi C., and Geffen R. In vivo NGF treatment increases proliferation in the primary sympathetic ganglia of chick embryos. Dev. Biol. 181 (1997) 116-120
40. Gonzalez B.J., Basille M., Vaudry D., Fournier A., and Vaudry H. Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Neuroscience 78 (1997) 419-430
41. Gray S.L., Yamaguchi N., Vencova P., and Sherwood N.M. Temperature-sensitive phenotype in mice lacking pituitary adenylate cyclase-activating polypeptide. Endocrinology 143 (2002) 3946-3954
42. Greene L.A., and Tischler A.S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. Natl. Acad. Sci. USA 73 (1976) 2424-2428
43. Grumolato L., Elkahloun A.G., Ghzili H., Alexandre D., Coulouarn C., Yon L., Salier J.P., Eiden L.E., Fournier A., Vaudry H., and Anouar Y. Microarray and suppression subtractive hybridization analyses of gene expression in pheochromocytoma cells reveal pleiotropic effects of pituitary adenylate cyclase-activating polypeptide on cell proliferation, survival, and adhesion. Endocrinology 144 (2003) 2368-2379
44. Grumolato L., Louiset E., Alexandre D., Ait-Ali D., Turquier V., Fournier A., Fasolo A., Vaudry H., and Anouar Y. PACAP and NGF regulate common and distinct traits of the sympathoadrenal lineage: effects on electrical properties, gene markers and transcription factors in differentiating PC12 cells. Eur. J. Neurosci. 17 (2003) 71-82
45. Guillemot F., Lo L.C., Johnson J.E., Auerbach A., Anderson D.J., and Joyner A.L. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75 (1993) 463-476
46. Guillemot J., Ait-Ali D., Turquier V., Montero-Hadjadje M., Fournier A., Vaudry H., Anouar Y., and Yon L. Involvement of multiple signaling pathways in PACAP-induced EM66 secretion from chromaffin cells. Regul. Pept. 137 (2006) 79-88
47. Hahm S.H., Hsu C.M., and Eiden L.E. PACAP activates calcium influx-dependent and -independent pathways to couple met-enkephalin secretion and biosynthesis in chromaffin cells. J. Mol. Neurosci. 11 (1998) 43-56
48. Hamelink C., Lee H.W., Chen Y., Grimaldi M., and Eiden L.E. Coincident elevation of cAMP and calcium influx by PACAP-27 synergistically regulates vasoactive intestinal polypeptide gene transcription through a novel PKA-independent signaling pathway. J. Neurosci. 22 (2002) 5310-5320
49. Hamelink C., Tjurmina O., Damadzic R., Young W.S., Weihe E., Lee H.W., and Eiden L.E. Pituitary adenylate cyclase-activating polypeptide is a sympathoadrenal neurotransmitter involved in catecholamine regulation and glucohomeostasis. Proc. Natl. Acad. Sci. USA 99 (2002) 461-466
50. Hoannibal J. Roles of PACAP-containing retinal ganglion cells in circadian timing. Int. Rev. Cytol. 251 (2006) 1-39
51. Hansel D.E., May V., Eipper B.A., and Ronnett G.V. Pituitary adenylyl cyclase-activating peptides and alpha-amidation in olfactory neurogenesis and neuronal survival in vitro. J. Neurosci. 21 (2001) 4625-4636
52. Harmar A.J. An essential role for peptidergic signalling in the control of circadian rhythms in the suprachiasmatic nuclei. J. Neuroendocrinol. 15 (2003) 335-338
53. Harmar A.J., Sheward W.J., Morrison C.F., Waser B., Gugger M., and Reubi J.C. Distribution of the VPAC2 receptor in peripheral tissues of the mouse. Endocrinology 145 (2004) 1203-1210
54. Hartfield P.J., Bilney A.J., and Murray A.W. Neurotrophic factors prevent ceramide-induced apoptosis downstream of c-Jun N-terminal kinase activation in PC12 cells. J. Neurochem. 71 (1998) 161-169
55. Heraud C., Hilairet S., Muller J.M., Leterrier J.F., and Chadeneau C. Neuritogenesis induced by vasoactive intestinal peptide, pituitary adenylate cyclase-activating polypeptide, and peptide histidine methionine in SH-SY5y cells is associated with regulated expression of cytoskeleton mRNAs and proteins. J. Neurosci. Res. 75 (2004) 320-329
56. Hernandez A., Kimball B., Romanchuk G., and Mulholland M.W. Pituitary adenylate cyclase-activating peptide stimulates neurite growth in PC12 cells. Peptides 16 (1995) 927-932
57. Holgert H., Holmberg K., Hannibal J., Fahrenkrug J., Brimijoin S., Hartman B.K., and Hokfelt T. PACAP in the adrenal gland-relationship with choline acetyltransferase, enkephalin and chromaffin cells and effects of immunological sympathectomy. Neuroreport 8 (1996) 297-301
58. Hoshino M., Li M., Zheng L.Q., Suzuki M., Mochizuki T., and Yanaihara N. Pituitary adenylate cyclase activating peptide and vasoactive intestinal polypeptide: differentiation effects on human neuroblastoma NB-OK-1 cells. Neurosci. Lett. 159 (1993) 35-38
59. Houchi H., Azuma M., Kitamura K., Okuno M., and Oka M. Pituitary adenylate cyclase-activating polypeptide stimulates the synthesis of dopamine in cultured bovine adrenal chromaffin cells. Hypertens. Res. 18 Suppl 1 (1995) S169-S171
60. Huber K., Karch N., Ernsberger U., Goridis C., and Unsicker K. The role of Phox2B in chromaffin cell development. Dev. Biol. 279 (2005) 501-508
61. Huber K. The sympathoadrenal cell lineage: specification, diversification, and new perspectives. Dev. Biol. 298 (2006) 335-343
62. Ip N.Y., Boulton T.G., Li Y., Verdi J.M., Birren S.J., Anderson D.J., and Yancopoulos G.D. CNTF, FGF, and NGF collaborate to drive the terminal differentiation of MAH cells into postmitotic neurons. Neuron 13 (1994) 443-455
63. Ishido M., and Masuo Y. Transcriptome of pituitary adenylate cyclase-activating polypeptide-differentiated PC12 cells. Regul. Pept. 123 (2004) 15-21
64. Isobe K., Yukimasa N., Nakai T., and Takuwa Y. Pituitary adenylate cyclase-activating polypeptide induces gene expression of the catecholamine synthesizing enzymes, tyrosine hydroxylase, and dopamine beta-hydroxylase in cultured porcine adrenal medullary chromaffin cells. Ann. N. Y. Acad. Sci. 805 (1996) 464-469
65. Isobe K., Tatsuno I., Yashiro T., Nanmoku T., Takekoshi K., Kawakami Y., and Nakai T. Expression of mRNA for PACAP and its receptors in intra- and extra-adrenal human pheochromocytomas and their relationship to catecholamine synthesis. Regul. Pept. 110 (2003) 213-217
66. Isobe K., Kaneko M., Kaneko S., Nissato S., Nanmoku T., Takekoshi K., Okuda Y., and Kawakami Y. Expression of mRNAs for PACAP and its receptor in human neuroblastomas and their relationship to catecholamine synthesis. Regul. Pept. 123 (2004) 29-32
67. Kee Y., and Bronner-Fraser M. To proliferate or to die: role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes Dev. 19 (2005) 744-755
68. Lamouche S., Martineau D., and Yamaguchi N. Modulation of adrenal catecholamine release by PACAP in vivo. Am. J. Physiol. 276 (1999) 162-170
69. Lamouche S., and Yamaguchi N. Role of PAC(1) receptor in adrenal catecholamine secretion induced by PACAP and VIP in vivo. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) 510-518
70. Lamouche S., and Yamaguchi N. PACAP release from the canine adrenal gland in vivo: its functional role in severe hypotension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 (2003) 588-597
71. Langley K., and Grant N.J. Molecular markers of sympathoadrenal cells. Cell Tissue Res. 298 (1999) 185-206
72. Laslop A., and Mahata S.K. Neuropeptides and chromogranins: session overview. Ann. N. Y. Acad. Sci. 971 (2002) 294-299
73. Lazarovici P., Jiang H., and Fink Jr. D. The 38-amino-acid form of pituitary adenylate cyclase-activating polypeptide induces neurite outgrowth in PC12 cells that is dependent on protein kinase C and extracellular signal-regulated kinase but not on protein kinase A, nerve growth factor receptor tyrosine kinase, p21(ras) G protein, and pp60(c-src) cytoplasmic tyrosine kinase. Mol. Pharmacol. 54 (1998) 547-558
74. Lee F.S., Rajagopal R., Kim A.H., Chang P.C., and Chao M.V. Activation of Trk neurotrophin receptor signaling by pituitary adenylate cyclase-activating polypeptides. J. Biol. Chem. 277 (2002) 9096-9102
75. Lee H.W., Hahm S.H., Hsu C.M., and Eiden L.E. Pituitary adenylate cyclase-activating polypeptide regulation of vasoactive intestinal polypeptide transcription requires Ca2+ influx and activation of the serine/threonine phosphatase calcineurin. J. Neurochem. 73 (1999) 1769-1772
76. Lelievre V., Becq-Giraudon L., Meunier A.C., and Muller J.M. Switches in the expression and function of PACAP and VIP receptors during phenotypic interconversion in human neuroblastoma cells. Neuropeptides 30 (1996) 313-322
77. Lelievre V., Pineau N., Du J., Wen C.H., Nguyen T., Janet T., Muller J.M., and Waschek J.A. Differential effects of peptide histidine isoleucine (PHI) and related peptides on stimulation and suppression of neuroblastoma cell proliferation. A novel VIP-independent action of PHI via MAP kinase. J. Biol. Chem. 273 (1998) 19685-19690
78. Lelievre V., Ghiani C.A., Seksenyan A., Gressens P., de Vellis J., and Waschek J.A. Growth factor-dependent actions of PACAP on oligodendrocyte progenitor proliferation. Regul. Pept. 137 (2006) 58-66
79. Lenders J.W., Eisenhofer G., Mannelli M., and Pacak K. Phaeochromocytoma. Lancet 366 (2005) 665-675
80. Li M., David C., Kikuta T., Somogyvari-Vigh A., and Arimura A. Signaling cascades involved in neuroprotection by subpicomolar pituitary adenylate cyclase-activating polypeptide 38. J. Mol. Neurosci. 27 (2005) 91-105
81. Light W., Vernon A.E., Lasorella A., Iavarone A., and LaBonne C. Xenopus Id3 is required downstream of Myc for the formation of multipotent neural crest progenitor cells. Development 132 (2005) 1831-1841
82. Lioudyno M., Skoglosa Y., Takei N., and 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. 51 (1998) 243-256
83. Loring J.F., Barker D.L., and Erickson C.A. Migration and differentiation of neural crest and ventral neural tube cells in vitro: implications for in vitro and in vivo studies of the neural crest. J. Neurosci. 8 (1988) 1001-1015
84. Lu N., and DiCicco-Bloom E. Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc. Natl. Acad. Sci. USA 94 (1997) 3357-3362
85. Lutz E.M., Ronaldson E., Shaw P., Johnson M.S., Holland P.J., and Mitchell R. Characterization of novel splice variants of the PAC1 receptor in human neuroblastoma cells: consequences for signaling by VIP and PACAP. Mol. Cell. Neurosci. 31 (2006) 193-209
86. Mahapatra N.R., Mahata M., Datta A.K., Gerdes H.H., Huttner W.B., O'Connor D.T., and Mahata S.K. Neuroendocrine cell type-specific and inducible expression of the chromogranin B gene: crucial role of the proximal promoter. Endocrinology 141 (2000) 3668-3678
87. Manger W.M., and Eisenhofer G. Pheochromocytoma: diagnosis and management update. Curr. Hypertens. Rep. 6 (2004) 477-484
88. Maris J.M. The biologic basis for neuroblastoma heterogeneity and risk stratification. Curr. Opin. Pediatr. 17 (2005) 7-13
89. Marley P.D., Cheung C.Y., Thomson K.A., and Murphy R. Activation of tyrosine hydroxylase by pituitary adenylate cyclase-activating polypeptide (PACAP-27) in bovine adrenal chromaffin cells. J. Auton. Nerv. Syst. 60 (1996) 141-146
90. May V., and Braas K.M. Pituitary adenylate cyclase-activating polypeptide (PACAP) regulation of sympathetic neuron neuropeptide Y and catecholamine expression. J. Neurochem. 65 (1995) 978-987
91. McKenzie S., and Marley P.D. Caffeine stimulates Ca(2+) entry through store-operated channels to activate tyrosine hydroxylase in bovine chromaffin cells. Eur. J. Neurosci. 15 (2002) 1485-1492
92. McPherson C.E., Varley J.E., and Maxwell G.D. Expression and regulation of type I BMP receptors during early avian sympathetic ganglion development. Dev. Biol. 221 (2000) 220-232
93. Mercer A., Ronnholm H., Holmberg J., Lundh H., Heidrich J., Zachrisson O., Ossoinak A., Frisen J., and Patrone C. PACAP promotes neural stem cell proliferation in adult mouse brain. J. Neurosci. Res. 76 (2004) 205-215
94. Michael G.J., and Priestley J.V. Expression of trkA and p75 nerve growth factor receptors in the adrenal gland. Neuroreport 7 (1996) 1617-1622
95. Miyata A., Arimura A., Dahl R.R., Minamino N., Uehara A., Jiang L., Culler M.D., and Coy D.H. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem. Biophys. Res. Commun. 164 (1989) 567-574
96. Moller K., and Sundler F. Expression of pituitary adenylate cyclase activating peptide (PACAP) and PACAP type I receptors in the rat adrenal medulla. Regul. Pept. 63 (1996) 129-139
97. Moller K., Reimer M., Hannibal J., Fahrenkrug J., Sundler F., and Kanje M. Pituitary adenylate cyclase-activating peptide (PACAP) and PACAP type 1 receptor expression in regenerating adult mouse and rat superior cervical ganglia in vitro. Brain Res. 775 (1997) 156-165
98. Moriguchi T., Takako N., Hamada M., Maeda A., Fujioka Y., Kuroha T., Huber R.E., Hasegawa S.L., Rao A., Yamamoto M., Takahashi S., Lim K.C., and Engel J.D. Gata3 participates in a complex transcriptional feedback network to regulate sympathoadrenal differentiation. Development 133 (2006) 3871-3881
99. Morita K., Sakakibara A., Kitayama S., Kumagai K., Tanne K., and Dohi T. Pituitary adenylate cyclase-activating polypeptide induces a sustained increase in intracellular free Ca(2+) concentration and catechol amine release by activating Ca(2+) influx via receptor-stimulated Ca(2+) entry, independent of store-operated Ca(2+) channels, and voltage-dependent Ca(2+) channels in bovine adrenal medullary chromaffin cells. J. Pharmacol. Exp. Ther. 302 (2002) 972-982
100. Muroi M., Funahashi H., Zhou C.J., Ohtaki H., Arimura A., and Shioda S. PACAP receptor expression in the rat adrenal medulla by in situ hybridization and immunocytochemistry. Ann. N. Y. Acad. Sci. 921 (2000) 349-351
101. Nanmoku T., Isobe K., Sakurai T., Yamanaka A., Takekoshi K., Kawakami Y., Ishii K., Goto K., and Nakai T. Orexins suppress catecholamine synthesis and secretion in cultured PC12 cells. Biochem. Biophys. Res. Commun. 274 (2000) 310-315
102. Nicot A., and DiCicco-Bloom E. Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc. Natl. Acad. Sci. USA 98 (2001) 4758-4763
103. Nicot A., Lelievre V., Tam J., Waschek J.A., and DiCicco-Bloom E. Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J. Neurosci. 22 (2002) 9244-9254
104. Nielsen H.S., Hannibal J., and Fahrenkrug J. Prenatal expression of pituitary adenylate cyclase activating polypeptide (PACAP) in autonomic and sensory ganglia and spinal cord of rat embryos. Ann. N. Y. Acad. Sci. 865 (1998) 533-536
105. Nielsen K.M., Chaverra M., Hapner S.J., Nelson B.R., Todd V., Zigmond R.E., and Lefcort F. PACAP promotes sensory neuron differentiation: blockade by neurotrophic factors. Mol. Cell. Neurosci. 25 (2004) 629-641
106. Nishimoto M., Furuta A., Aoki S., Kudo Y., Miyakawa H., and Wada K. PACAP/PAC1 autocrine system promotes proliferation and astrogenesis in neural progenitor cells. Glia 55 (2007) 317-327
107. Nogi H., Hashimoto H., Fujita T., Hagihara N., Matsuda T., and Baba A. Pituitary adenylate cyclase-activating polypeptide (PACAP) receptor mRNA in the rat adrenal gland: localization by in situ hybridization and identification of splice variants. Jpn. J. Pharmacol. 75 (1997) 203-207
108. Ogawa T., Nakamachi T., Ohtaki H., Hashimoto H., N S., Baba A., Watanabe J., Kikuyama S., and Shioda S. Monoaminergic neuronal development is not affected in PACAP-gene-deficient mice. Regul. Pept. 126 (2005) 103-108
109. Ohno F., Watanabe J., Sekihara H., Hirabayashi T., Arata S., Kikuyama S., Shioda S., Nakaya K., and Nakajo S. Pituitary adenylate cyclase-activating polypeptide promotes differentiation of mouse neural stem cells into astrocytes. Regul. Pept. 126 (2005) 115-122
110. Onoue S., Waki Y., Nagano Y., Satoh S., and Kashimoto K. The neuromodulatory effects of VIP/PACAP on PC-12 cells are associated with their N-terminal structures. Peptides 22 (2001) 867-872
111. Onoue S., Endo K., Ohshima K., Yajima T., and Kashimoto K. The neuropeptide PACAP attenuates beta-amyloid (1-42)-induced toxicity in PC12 cells. Peptides 23 (2002) 1471-1478
112. Onoue S., Ohshima K., Endo K., Yajima T., and Kashimoto K. PACAP protects neuronal PC12 cells from the cytotoxicity of human prion protein fragment 106-126. FEBS Lett. 522 (2002) 65-70
113. Pattyn A., Morin X., Cremer H., Goridis C., and Brunet J.F. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399 (1999) 366-370
114. Pavelock K.A., Girard B.M., Schutz K.C., Braas K.M., and May V. Bone morphogenetic protein down-regulation of neuronal pituitary adenylate cyclase-activating polypeptide and reciprocal effects on vasoactive intestinal peptide expression. J. Neurochem. 100 (2007) 603-616
115. Payet M.D., Bilodeau L., Breault L., Fournier A., Yon L., Vaudry H., and Gallo-Payet N. PAC1 receptor activation by PACAP-38 mediates Ca2+ release from a cAMP-dependent pool in human fetal adrenal gland chromaffin cells. J. Biol. Chem. 278 (2003) 1663-1670
116. Peterson S., and Bogenmann E. The RET and TRKA pathways collaborate to regulate neuroblastoma differentiation. Oncogene 23 (2004) 213-225
117. Powers J.F., Schelling K.H., Brachold J.M., and Tischler A.S. Plasticity of pheochromocytoma cell lines from neurofibromatosis knockout mice. Ann. N. Y. Acad. Sci. 971 (2002) 371-378
118. Przywara D.A., Guo X., Angelilli M.L., Wakade T.D., and Wakade A.R. A non-cholinergic transmitter, pituitary adenylate cyclase-activating polypeptide, utilizes a novel mechanism to evoke catecholamine secretion in rat adrenal chromaffin cells. J. Biol. Chem. 271 (1996) 10545-10550
119. Przywara D.A., Kulkarni J.S., Wakade T.D., Leontiev D.V., and Wakade A.R. 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. 71 (1998) 1889-1897
120. Raible D.W. Development of the neural crest: achieving specificity in regulatory pathways. Curr. Opin. Cell Biol. 18 (2006) 698-703
121. Ravni A., Bourgault S., Lebon A., Chan P., Galas L., Fournier A., Vaudry H., Gonzalez B., Eiden L.E., and Vaudry D. The neurotrophic effects of PACAP in PC12 cells: control by multiple transduction pathways. J. Neurochem. 98 (2006) 321-329
122. Ravni A., Eiden L.E., Vaudry H., Gonzalez B.J., and Vaudry D. Cycloheximide treatment to identify components of the transitional transcriptome in PACAP-induced PC12 cell differentiation. J. Neurochem. 98 (2006) 1229-1241
123. Reubi J.C., Laderach U., Waser B., Gebbers J.O., Robberecht P., and Laissue J.A. Vasoactive intestinal peptide/pituitary adenylate cyclase-activating peptide receptor subtypes in human tumors and their tissues of origin. Cancer Res. 60 (2000) 3105-3112
124. Rius R.A., Guidotti A., and Costa E. Pituitary adenylate cyclase activating polypeptide (PACAP) potently enhances tyrosine hydroxylase (TH) expression in adrenal chromaffin cells. Life Sci. 54 (1994) 1735-1743
125. Rouault J.P., Falette N., Guehenneux F., Guillot C., Rimokh R., Wang Q., Berthet C., Moyret-Lalle C., Savatier P., Pain B., Shaw P., Berger R., Samarut J., Magaud J.P., Ozturk M., Samarut C., and Puisieux A. Identification of BTG2, an antiproliferative p53-dependent component of the DNA damage cellular response pathway. Nat. Genet. 14 (1996) 482-486
126. Ruaro E.M., Collavin L., Del Sal G., Haffner R., Oren M., Levine A.J., and Schneider C. A proline-rich motif in p53 is required for transactivation-independent growth arrest as induced by Gas1. Proc. Natl. Acad. Sci. USA 94 (1997) 4675-4680
127. Rush R.A., Chie E., Liu D., Tafreshi A., Zettler C., and Zhou X.F. Neurotrophic factors are required by mature sympathetic neurons for survival, transmission and connectivity. Clin. Exp. Pharmacol. Physiol. 24 (1997) 549-555
128. Sakai Y., Hashimoto H., Shintani N., Tomimoto S., Tanaka K., Ichibori A., Hirose M., and Baba A. Involvement of p38 MAP kinase pathway in the synergistic activation of PACAP mRNA expression by NGF and PACAP in PC12h cells. Biochem. Biophys. Res. Commun. 285 (2001) 656-661
129. Salvi E.P., Vaccaro R., and Renda T.G. Ontogeny of PACAP immunoreactivity in extrinsic and intrinsic innervation of chicken gut. Peptides 21 (2000) 1703-1709
130. Schafer H., Trauzold A., Sebens T., Deppert W., Folsch U.R., and Schmidt W.E. The proliferation-associated early response gene p22/PRG1 is a novel p53 target gene. Oncogene 16 (1998) 2479-2487
131. Schober A., Krieglstein K., and Unsicker K. Molecular cues for the development of adrenal chromaffin cells and their preganglionic innervation. Eur. J. Clin. Invest. 30 Suppl 3 (2000) 87-90
132. Seematter G., Binnert C., Martin J.L., and Tappy L. Relationship between stress, inflammation and metabolism. Curr. Opin. Clin. Nutr. Metab. Care 7 (2004) 169-173
133. Shintani N., Suetake S., Hashimoto H., Koga K., Kasai A., Kawaguchi C., Morita Y., Hirose M., Sakai Y., Tomimoto S., Matsuda T., and Baba A. Neuroprotective action of endogenous PACAP in cultured rat cortical neurons. Regul. Pept. 126 (2005) 123-128
134. Shiotani Y., Kimura S., Ohshige Y., Yanaihara C., and Yanaihara N. Immunohistochemical localization of pituitary adenylate cyclase-activating polypeptide (PACAP) in the adrenal medulla of the rat. Peptides 16 (1995) 1045-1050
135. Skoglosa Y., Patrone C., and Lindholm D. Pituitary adenylate cyclase activating polypeptide is expressed by developing rat Purkinje cells and decreases the number of cerebellar gamma-amino butyric acid positive neurons in culture. Neurosci. Lett. 265 (1999) 207-210
136. Song Q., Mehler M.F., and Kessler J.A. Bone morphogenetic proteins induce apoptosis and growth factor dependence of cultured sympathoadrenal progenitor cells. Dev. Biol. 196 (1998) 119-127
137. Suh J., Lu N., Nicot A., Tatsuno I., and DiCicco-Bloom E. PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat. Neurosci. 4 (2001) 123-124
138. Tabarin A., Chen D., Hakanson R., and Sundler F. Pituitary adenylate cyclase-activating peptide in the adrenal gland of mammals: distribution, characterization and responses to drugs. Neuroendocrinology 59 (1994) 113-119
139. Tafreshi A.P., Zhou X.F., and Rush R.A. Endogenous nerve growth factor and neurotrophin-3 act simultaneously to ensure the survival of postnatal sympathetic neurons in vivo. Neuroscience 83 (1998) 373-380
140. Takahashi K., Totsune K., Murakami O., Sone M., Itoi K., Miura Y., and Mouri T. Pituitary adenylate cyclase activating polypeptide (PACAP)-like immunoreactivity in pheochromocytomas. Peptides 14 (1993) 365-369
141. Takei N., Skoglosa Y., and Lindholm D. Neurotrophic and neuroprotective effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on mesencephalic dopaminergic neurons. J. Neurosci. Res. 54 (1998) 698-706
142. Takei N., Torres E., Yuhara A., Jongsma H., Otto C., Korhonen L., Abiru Y., Skoglosa Y., Schutz G., Hatanaka H., Sofroniew M.V., and Lindholm D. Pituitary adenylate cyclase-activating polypeptide promotes the survival
143. Tanaka J., Koshimura K., Murakami Y., Sohmiya M., Yanaihara N., and Kato Y. Neuronal protection from apoptosis by pituitary adenylate cyclase-activating polypeptide. Regul. Pept. 72 (1997) 1-8
144. Taupenot L., Mahata S.K., Wu H., and O'Connor D.T. Peptidergic activation of transcription and secretion in chromaffin cells. Cis and trans signaling determinants of pituitary adenylyl cyclase-activating polypeptide (PACAP). J. Clin. Invest. 101 (1998) 863-876
145. Taupenot L., Mahata M., Mahata S.K., and O'Connor D.T. Time-dependent effects of the neuropeptide PACAP on catecholamine secretion: stimulation and desensitization. Hypertension 34 (1999) 1152-1162
146. Tischler A.S., Riseberg J.C., and Gray R. Mitogenic and antimitogenic effects of pituitary adenylate cyclase-activating polypeptide (PACAP) in adult rat chromaffin cell cultures. Neurosci. Lett. 189 (1995) 135-138
147. Tonshoff C., Hemmick L., and Evinger M.J. Pituitary adenylate cyclase activating polypeptide (PACAP) regulates expression of catecholamine biosynthetic enzyme genes in bovine adrenal chromaffin cells. J. Mol. Neurosci. 9 (1997) 127-140
148. Tornoe K., Hannibal J., Jensen T.B., Georg B., Rickelt L.F., Andreasen M.B., Fahrenkrug J., and Holst J.J. PACAP-(1-38) as neurotransmitter in the porcine adrenal glands. Am. J. Physiol. Endocrinol. Metab. 279 (2000) 1413-1425
149. Turquier V., Yon L., Grumolato L., Alexandre D., Fournier A., Vaudry H., and Anouar Y. Pituitary adenylate cyclase-activating polypeptide stimulates secretoneurin release and secretogranin II gene transcription in bovine adrenochromaffin cells through multiple signaling pathways and increased binding of pre-existing activator protein-1-like transcription factors. Mol. Pharmacol. 60 (2001) 42-52
150. Uchida D., Arimura A., Somogyvari-Vigh A., Shioda S., and Banks W.A. Prevention of ischemia-induced death of hippocampal neurons by pituitary adenylate cyclase activating polypeptide. Brain Res. 736 (1996) 280-286
151. Unsicker K., Krisch B., Otten U., and Thoenen H. Nerve growth factor-induced fiber outgrowth from isolated rat adrenal chromaffin cells: impairment by glucocorticoids. Proc. Natl. Acad. Sci. USA 75 (1978) 3498-3502
152. Unsicker K., Finotto S., and Krieglstein K. Generation of cell diversity in the peripheral autonomic nervous system: the sympathoadrenal cell lineage revisited. Ann. Anat. 179 (1997) 495-500
153. Unsicker K., Huber K., Schutz G., and Kalcheim C. The chromaffin cell and its development. Neurochem. Res. 30 (2005) 921-925
154. Usdin T.B., Bonner T.I., and Mezey E. Two receptors for vasoactive intestinal polypeptide with similar specificity and complementary distributions. Endocrinology 135 (1994) 2662-2680
155. Vallejo I., and Vallejo M. Pituitary adenylate cyclase-activating polypeptide induces astrocyte differentiation of precursor cells from developing cerebral cortex. Mol. Cell. Neurosci. 21 (2002) 671-683
156. Vaudry D., Gonzalez B.J., Basille M., Yon L., Fournier A., and Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol. Rev. 52 (2000) 269-324
157. Vaudry D., Chen Y., Ravni A., Hamelink C., Elkahloun A.G., and Eiden L.E. Analysis of the PC12 cell transcriptome after differentiation with pituitary adenylate cyclase-activating polypeptide (PACAP). J. Neurochem. 83 (2002) 1272-1284
158. Vaudry D., Stork P.J., Lazarovici P., and Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296 (2002) 1648-1649
159. Vaudry D., Falluel-Morel A., Basille M., Pamantung T.F., Fontaine M., Fournier A., Vaudry H., and Gonzalez B.J. Pituitary adenylate cyclase-activating polypeptide prevents C2-ceramide-induced apoptosis of cerebellar granule cells. J. Neurosci. Res. 72 (2003) 303-316
160. Venihaki M., Ain K., Dermitzaki E., Gravanis A., and Margioris A.N. KAT45, a noradrenergic human pheochromocytoma cell line producing corticotropin-releasing hormone. Endocrinology 139 (1998) 713-722
161. Verdi J.M., Ip N., Yancopoulos G.D., and Anderson D.J. Expression of trk in MAH cells lacking the p75 low-affinity nerve growth factor receptor is sufficient to permit nerve growth factor-induced differentiation to postmitotic neurons. Proc. Natl. Acad. Sci. USA 91 (1994) 3949-3953
162. Vertongen P., Devalck C., Sariban E., De Laet M.H., Martelli H., Paraf F., Helardot P., and Robberecht P. Pituitary adenylate cyclase activating peptide and its receptors are expressed in human neuroblastomas. J. Cell. Physiol. 167 (1996) 36-46
163. Vertongen P., De Clerck P., Fournet J.C., Martelli H., Helardot P., Devalck C., Peeters T., Sariban E., and Robberecht P. Comparison between vasoactive intestinal polypeptide and pituitary adenylate cyclase activating polypeptide levels in neuroblastoma tumour tissues. Neuropeptides 31 (1997) 409-413
164. Waschek J.A., Casillas R.A., Nguyen T.B., DiCicco-Bloom E.M., Carpenter E.M., and 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 95 (1998) 9602-9607
165. Waschek J.A. Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration. Dev. Neurosci. 24 (2002) 14-23
166. Weihe E., and Eiden L.E. Chemical neuroanatomy of the vesicular amine transporters. FASEB J. 14 (2000) 2435-2449
167. Weihe E., Schutz B., Hartschuh W., Anlauf M., Schafer M.K., and Eiden L.E. Coexpression of cholinergic and noradrenergic phenotypes in human and nonhuman autonomic nervous system. J. Comp. Neurol. 492 (2005) 370-379
168. Whalen E.J., Johnson A.K., and Lewis S.J. Hemodynamic actions of systemically injected pituitary adenylate cyclase activating polypeptide-27 in the rat. Eur. J. Pharmacol. 365 (1999) 205-215
169. Williams Z., Tse V., Hou L., Xu L., and Silverberg G.D. Sonic hedgehog promotes proliferation and tyrosine hydroxylase induction of postnatal sympathetic cells in vitro. Neuroreport 11 (2000) 3315-3319
170. Wong D.L., Anderson L.J., and Tai T.C. Cholinergic and peptidergic regulation of phenylethanolamine N-methyltransferase gene expression. Ann. N. Y. Acad. Sci. 971 (2002) 19-26
171. Yamaguchi N., and Lamouche S. Enhanced reactivity of the adrenal medulla in response to pituitary adenylate cyclase activating polypeptide1-27 (PACAP) during insulin-induced hypoglycemia in anesthetized dogs. Can. J. Physiol. Pharmacol. 77 (1999) 819-826
172. Yamaguchi N. Pituitary adenylate cyclase activating polypeptide enhances glucose-evoked insulin secretion in the canine pancreas in vivo. Jop 2 (2001) 306-316
173. Yuhara A., Nishio C., Abiru Y., Hatanaka H., and Takei N. PACAP has a neurotrophic effect on cultured basal forebrain cholinergic neurons from adult rats. Brain Res. Dev. Brain Res. 131 (2001) 41-45
174. Zheng J., Zhou G., and Hexum T.D. Neuropeptide Y secretion from bovine chromaffin cells inhibits cyclic AMP accumulation. Life Sci. 67 (2000) 617-625
175. Zhou C.J., Shioda S., Shibanuma M., Nakajo S., Funahashi H., Nakai Y., Arimura A., and Kikuyama S. Pituitary adenylate cyclase-activating polypeptide receptors during development: expression in the rat embryo at primitive streak stage. Neuroscience 93 (1999) 375-391