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

Journal of Neuroscience

Volumn 33, Issue 9, 2013, Pages 3865-3878

  Yan, Yan ^a   Zhou, Xiaofeng ^a   Pan, Zui ^a   Ma, Jianjie ^a   Waschek, James A ^c   DiCicco Bloom, Emanuel ^a,b  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; DUAL SPECIFICITY PHOSPHATASE 2; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM CURRENT; CELL COUNT; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA SYNTHESIS; EMBRYO; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MITOGENESIS; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; BROMODEOXYURIDINE; CALCIUM; CELL CYCLE; CELL DIVISION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; CEREBRAL VENTRICLES; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, MAMMALIAN; ENZYME INHIBITORS; ESTRENES; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IN SITU NICK-END LABELING; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGENS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; PREGNANCY; PROTEIN KINASE C; PYRIDINES; PYRROLIDINONES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE, TYPE I; RNA ISOFORMS; RNA, SMALL INTERFERING; TRETINOIN;

EID: 84874588179     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1062-12.2013     Document Type: Article

References (69)

1. Arimura A (1992) Pituitary adenylate cyclase activating polypeptide (PACAP): discovery and current status of research. Regul Pept 37:287-303. Medline
2. Bani-Yaghoub M, Kubu CJ, Cowling R, Rochira J, Nikopoulos GN, Bellum S, Verdi JM (2007) A switch in numb isoforms is a critical step in cortical development. Dev Dyn 236:696-705. CrossRef Medline
3. Barrie AP, Clohessy AM, Buensuceso CS, Rogers MV, Allen JM (1997) Pituitary adenylyl cyclase-activating peptide stimulates extracellular signalregulated kinase 1 or 2 (ERK1/2) activity in a Ras-independent, mitogenactivated protein kinase/ERK kinase 1 or 2-dependent manner in PC12 cells. J Biol Chem 272:19666-19671. CrossRef Medline
4. Basille M, Vaudry D, Coulouarn Y, Jegou S, Lihrmann I, Fournier A, Vaudry H, Gonzalez B (2000) Comparative distribution of pituitary adenylate cyclase-activating polypeptide (PACAP) binding sites and PACAP receptorm RNA sin the rat brain during development. JCompNeurol 425:495-509. CrossRef Medline
5. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21. CrossRef Medline
6. Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517-529. CrossRef Medline
7. Carey RG, Li B, DiCicco-Bloom E (2002) Pituitary adenylate cyclase activating polypeptide anti-mitogenic signaling in cerebral cortical progenitors is regulated by p57Kip2-dependent CDK2 activity. J Neurosci 22:1583-1591. Medline
8. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelièvre V, Hu Z, Waschek JA (2004) Selective deficits in the circadian light response in mice lacking PACAP. Am J Physiol Regul Integr Comp Physiol 287:R1194-R1201. CrossRef Medline
9. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL (1990) Cortical radial glia: identification in tissue culture and evidence for their transformation to astrocytes. J Neurosci 10:684-692. Medline Di
10. Di Cicco-Bloom E, Deutsch PJ, Maltzman J, Zhang J, Pintar JE, Zheng J, Friedman WF, Zhou X, Zaremba T (2000) Autocrine expression and ontogenetic functions of the PACAP ligand/receptor system during sympathetic development. Dev Biol 219:197-213. CrossRef Medline
11. Fang KM, Chen JK, Hung SC, Chen MC, Wu YT, Wu TJ, Lin HI, Chen CH, Cheng H, Yang CS, Tzeng SF (2010) Effects of combinatorial treatment with pituitary adenylate cyclase activating peptide and human mesenchymal stem cells on spinal cord tissue repair. PLoS One 5:e15299. CrossRef Medline
12. Francone VP, Ifrim MF, Rajagopal C, Leddy CJ, Wang Y, Carson JH, Mains RE, Eipper BA (2010) Signaling from the secretory granule to the nucleus: Uhmk1 and PAM. Mol Endocrinol 24:1543-1558. CrossRef Medline
13. Gerdin MJ, Eiden LE (2007) Regulation of PC12 cell differentiation by cAMP signaling to ERK independent of PKA: do all the connections add up? Sci STKE 2007:pe15. CrossRef Medline
14. Girard BA, Lelievre V, Braas KM, Razinia T, Vizzard MA, Ioffe Y, El Meskini R, Ronnett GV, Waschek JA, May V (2006) Noncompensation in peptide/ receptor gene expression and distinct behavioral phenotypes in VIPand PACAP-deficient mice. J Neurochem 99:499-513. CrossRef Medline
15. Greenberg ME, Xu B, Lu B, Hempstead BL (2009) New insights in the biology of BDNF synthesis and release: implications in CNS function. J Neurosci 29:12764-12767. CrossRef Medline
16. Harmar AJ, Arimura A, Gozes I, Journot L, Laburthe M, Pisegna JR, Rawlings SR, Robberecht P, Said SI, Sreedharan SP, Wank SA, Waschek JA (1998) International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol Rev 50:265-270. Medline
17. Hashimoto R, Hashimoto H, Shintani N, Chiba S, Hattori S, Okada T, Nakajima M, Tanaka K, Kawagishi N, Nemoto K, Mori T, Ohnishi T, Noguchi H, Hori H, Suzuki T, Iwata N, Ozaki N, Nakabayashi T, Saitoh O, Kosuga A, Tatsumi M, Kamijima K, Weinberger DR, Kunugi H, Baba A (2007) Pituitary adenylate cyclase-activating polypeptide is associated with schizophrenia. Mol Psychiatry 12:1026-1032. CrossRef Medline
18. Haskell GT, LaMantia AS (2005) Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain. J Neurosci 25:7636-7647. CrossRef Medline
19. Hegg CC, Au E, Roskams AJ, Lucero MT (2003) PACAP is present in the olfactory system and evokes calcium transients in olfactory receptor neurons. J Neurophysiol 90:2711-2719. CrossRef Medline
20. Hogan PG, Lewis RS, Rao A (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28:491-533. CrossRef Medline
21. Lee M, Lelievre V, Zhao P, Torres M, Rodriguez W, Byun JY, Doshi S, Ioffe Y, Gupta G, de los Monteros AE, de Vellis J, Waschek J (2001) Pituitary adenylyl cyclase-activating polypeptide stimulates DNA synthesis but delays maturation of oligodendrocyte progenitors. J Neurosci 21:3849-3859. Medline
22. Lewis RS (2003) Calcium oscillations in T-cells: mechanisms and consequences for gene expression. Biochem Soc Trans 31:925-929. CrossRef Medline
23. Li B, DiCicco-Bloom E (2004) Basic fibroblast growth factor exhibits dual and rapid regulation of cyclin D1 and p27 to stimulate proliferation of rat cerebral cortical precursors. Dev Neurosci 26:197-207. CrossRef Medline
24. Li Q, Lee JA, Black DL (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 8:819-831. CrossRef Medline
25. Lu N, DiCicco-Bloom E (1997) Pituitary adenylate cyclase-activating polypeptide is an autocrine inhibitor of mitosis in cultured cortical precursor cells. Proc Natl Acad Sci U S A 94:3357-3362. CrossRef Medline
26. Lu N, Zhou R, DiCicco-Bloom E (1998) Opposing mitogenic regulation by PACAP in sympathetic and cerebral cortical precursors correlates with differential expression of PACAP receptor (PAC1-R) isoforms. J Neurosci Res 53:651-662. CrossRef Medline
27. Mairet-Coello G, Tury A, DiCicco-Bloom E (2009) Insulin-like growth factor-1 promotes G(1)/S cell cycle progression through bidirectional regulation of cyclins and cyclin-dependent kinase inhibitors via the phosphatidylinositol 3-kinase/Akt pathway in developing rat cerebral cortex. J Neurosci 29:775-788. CrossRef Medline
28. Malagelada C, López-Toledano MA, Willett RT, Jin ZH, Shelanski ML, Greene LA (2011) RTP801/REDD1 regulates the timing of cortical neurogenesis and neuron migration. J Neurosci 31:3186-3196. CrossRef Medline
29. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Götz M (2003) Neuronal or glial progeny: regional differences in radial glia fate. Neuron 37:751-764. CrossRef Medline
30. Ménard C, Hein P, Paquin A, Savelson A, Yang XM, Lederfein D, Barnabé-Heider F, Mir AA, Sterneck E, Peterson AC, Johnson PF, Vinson C, Miller FD (2002) An essential role for a MEK-C/EBP pathway during growth factor-regulated cortical neurogenesis. Neuron 36:597-610. CrossRef Medline
31. Mercer A, Rönnholm H, Holmberg J, Lundh H, Heidrich J, Zachrisson O, Ossoinak A, Frisén J, Patrone C (2004) PACAP promotes neural stem cell proliferation in adult mouse brain. J Neurosci Res 76:205-215. CrossRef Medline
32. Nicot A, DiCicco-Bloom E (2001) Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc Natl Acad Sci U S A 98:4758-4763. CrossRef Medline
33. Nicot A, Lelièvre V, Tam J, Waschek JA, DiCicco-Bloom E (2002) Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J Neurosci 22: 9244-9254. Medline
34. Nijmeijer JS, Arias-Vásquez A, Rommelse NN, Altink ME, Anney RJ, Asherson P, Banaschewski T, Buschgens CJ, Fliers EA, Gill M, Minderaa RB, Poustka L, Sergeant JA, Buitelaar JK, Franke B, Ebstein RP, Miranda A, Mulas F, Oades RD, Roeyers H, Rothenberger A, Sonuga-Barke EJ, Steinhausen HC, Faraone SV, Hartman CA, Hoekstra PJ (2010) Identifying loci for the overlap between attention-deficit/hyperactivity disorder and autism spectrum disorder using a genome-wide QTL linkage approach. J Am Acad Child Adolesc Psychiatry 49:675-685. CrossRef Medline
35. Nishimoto M, Furuta A, Aoki S, Kudo Y, Miyakawa H, Wada K (2007) PACAP/PAC1 autocrine system promotes proliferation and astrogenesis in neural progenitor cells. Glia 55:317-327. CrossRef Medline
36. Nishizuka Y (1984) The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308:693-698. CrossRef Medline
37. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144. CrossRef Medline
38. Ohta S, Gregg C, Weiss S (2006) Pituitary adenylate cyclase-activating polypeptide regulates forebrain neural stem cells and neurogenesis in vitro and in vivo. J Neurosci Res 84:1177-1186. CrossRef Medline
39. 2+ by caffeine and ryanodine induces apoptosis of chinese hamster ovary cells transfected with ryanodine receptor. J Biol Chem 275:19978-19984. CrossRef Medline
40. Pearce LR, Komander D, Alessi DR (2010) The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11:9-22. CrossRef Medline
41. Picetti R, Saiardi A, Abdel Samad T, Bozzi Y, Baik JH, Borrelli E (1997) Dopamine D2 receptors in signal transduction and behavior. Crit Rev Neurobiol 11:121-142. CrossRef Medline
42. Qian X, Goderie SK, Shen Q, Stern JH, Temple S (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125:3143-3152. Medline
43. Ressler KJ, Mercer KB, Bradley B, Jovanovic T, Mahan A, Kerley K, Norrholm SD, Kilaru V, Smith AK, Myers AJ, Ramirez M, Engel A, Hammack SE, Toufexis D, Braas KM, Binder EB, May V (2011) Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature 470: 492-497. CrossRef Medline
44. Revil T, Gaffney D, Dias C, Majewski J, Jerome-Majewska LA (2010) Alternative splicing is frequent during early embryonic development in mouse. BMC Genomics 11:399. CrossRef Medline
45. Romito-DiGiacomo RR, Menegay H, Cicero SA, Herrup K (2007) Effects of Alzheimer's disease on different cortical layers: the role of intrinsic differences in Abeta susceptibility. J Neurosci 27:8496-8504. CrossRef Medline
46. Schaar BT, Kinoshita K, McConnell SK (2004) Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 41:203-213. CrossRef Medline
47. Scharf E, May V, Braas KM, Shutz KC, Mao-Draayer Y (2008) Pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) regulate murine neural progenitor cell survival, proliferation, and differentiation. J Mol Neurosci 36:79-88. CrossRef Medline
48. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340. CrossRef Medline
49. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743-751. CrossRef Medline
50. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, Napoli JL, Peterson AS, Pleasure SJ (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597-609. CrossRef Medline
51. Spengler D, Waeber C, Pantaloni C, Holsboer F, Bockaert J, Seeburg PH, Journot L (1993) Differential signal transduction by five splice variants of the PACAP receptor. Nature 365:170-175. CrossRef Medline
52. Stevens HE, Smith KM, Rash BG, Vaccarino FM (2010) Neural stem cell regulation, fibroblast growth factors, and the developmental origins of neuropsychiatric disorders. Front Neurosci 4:59. CrossRef Medline
53. Studer M, Pöpperl H, Marshall H, Kuroiwa A, Krumlauf R (1994) Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 265:1728-1732. CrossRef Medline
54. Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E (2001) PACAP is an anti-mitogenic signal in developing cerebral cortex. Nat Neurosci 4:123-124. CrossRef Medline
55. Tomlinson DC, L'Hôte CG, Kennedy W, Pitt E, Knowles MA (2005) Alternative splicing of fibroblast growth factor receptor 3 produces a secreted isoform that inhibits fibroblast growth factor-induced proliferation and is repressed in urothelial carcinoma cell lines. Cancer Res 65:10441-10449. CrossRef Medline
56. Tury A, Mairet-Coello G, DiCicco-Bloom E (2011) The cyclindependent kinase inhibitor p57Kip2 regulates cell cycle exit, differentiation, and migration of embryonic cerebral cortical precursors. Cereb Cortex 21:1840-1856. CrossRef Medline
57. Usiello A, Baik JH, Rougé-Pont F, Picetti R, Dierich A, LeMeur M, Piazza PV, Borrelli E (2000) Distinct functions of the two isoforms of dopamine D2 receptors. Nature 408:199-203. CrossRef Medline
58. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT (1999) Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2:246-253. CrossRef Medline
59. Vaudry D, Stork PJ, Lazarovici P, Eiden LE (2002a) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296:1648-1649. CrossRef Medline
60. Vaudry D, Chen Y, Ravni A, Hamelink C, Elkahloun AG, Eiden LE (2002b) Analysis of the PC12 cell transcriptome after differentiation with pituitary adenylate cyclase-activating polypeptide (PACAP). J Neurochem 83: 1272-1284. CrossRef Medline
61. Vaudry D, Rousselle C, Basille M, Falluel-Morel A, Pamantung TF, Fontaine M, Fournier A, Vaudry H, Gonzalez BJ (2002c) Pituitary adenylate cyclase-activating polypeptide protects rat cerebellar granule neurons against ethanol-induced apoptotic cell death. Proc Natl Acad Sci U S A 99:6398-6403. CrossRef Medline
62. Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, Fournier A, Chow BK, Hashimoto H, Galas L, Vaudry H (2009) Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 61:283-357. CrossRef Medline
63. Verdi JM, Bashirullah A, Goldhawk DE, Kubu CJ, Jamali M, Meakin SO, Lipshitz HD (1999) Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc Natl Acad Sci U S A 96:10472-10476. CrossRef Medline
64. Waschek JA (2002) Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration. Dev Neurosci 24:14-23. CrossRef Medline
65. Waschek JA, Lelievre V, Bravo DT, Nguyen T, Muller JM (1997) Retinoic acid regulation of the VIP and PACAP autocrine ligand and receptor system in human neuroblastoma cell lines. Peptides 18:835-841. CrossRef Medline
66. Waschek JA, Casillas RA, Nguyen TB, DiCicco-Bloom EM, Carpenter EM, Rodriguez WI (1998) Neural tube expression of pituitary adenylate cyclase-activating peptide (PACAP) and receptor: potential role in patterning and neurogenesis. Proc Natl Acad Sci U S A 95:9602-9607. CrossRef Medline
67. Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, Mizuseki K, Sasai Y (2005) Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288-296. CrossRef Medline
68. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43:647-661. CrossRef Medline
69. Zhou C, Kikuyama S, Nakajo S, Hirabayashi T, Mizushima H, Shioda S (2000) Splice variants of PAC(1) receptor during early neural development of rats. Peptides 21:1177-1183. CrossRef Medline