Pituitary adenylate cyclase-activating polypeptide and Sonic Hedgehog interact to control cerebellar granule precursor cell proliferation

Journal of Neuroscience

Volumn 22, Issue 21, 2002, Pages 9244-9254

  Nicot, Arnaud ^a   Lelièvre, Vincent ^b   Tam, Jimmy ^c   Waschek, James A ^b   Dicicco Bloom, Emanuel ^a  

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

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Cerebellum; GPCR; Medulloblastoma; Neurogenesis; Neuronal precursors; Neuropeptide; Proliferation; Serpentine receptors

Indexed keywords

ADENYLATE CYCLASE ACTIVATOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR; MAXADILAN; POLYPEPTIDE; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; GENE MUTATION; GENETIC TRANSCRIPTION; GRANULE CELL; MEDULLOBLASTOMA; MITOGENESIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; STEM CELL;

EID: 0036848638     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-21-09244.2002     Document Type: Article

References (76)

1. Akimaru H, Chen Y, Dai P, Hou DX, Nonaka M, Smolik SM, Armstrong S, Goodman RH, Ishii S (1997) Drosophila CBP is a co-activator of cubitus interruptus in hedgehog signalling. Nature 386:735-738.
2. Alder J, Cho NK, Hatten ME (1996) Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 17:389-399.
3. Altman J, Bayer SA (1996) Development of the Cerebellar System in Relation to its Evolution, Structure and Functions. New York: CRC.
4. Arimura A (1998) Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Jpn J Physiol 48:301-331.
5. Barnes EA, Kong M, Ollendorff V, Donoghue DJ (2001) Patchedl interacts with cyclin B1 to regulate cell cycle progression. EMBO J 20:2214-2223.
6. Basille M, Gonzalez BJ, Desrues L, Demas M, Fournier A, Vaudry H (1995) Pituitary adenylate cyclase-activating polypeptide (PACAP) stimulates adenylyl cyclase and phospholipase C activity in rat cerebellar neuroblasts. J Neurochem 65:1318-1324.
7. 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 receptor mRNAs in the rat brain during development. J Comp Neurol 425:495-509.
8. Brewer G (1995) Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus. J Neurosci Res 42:674-683.
9. Campard PK, Crochemore C, Rene F, Monnier D, Koch B, Loeffler JP (1997) PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. DNA Cell Biol 16:323-333.
10. Kip2-dependent CDK2 activity. J Neurosci 22:1583-1591.
11. Cavallaro S, Copani A, D'Agata V, Musco S, Petralia S, Ventra C, Stivala F, Travali S, Canonico PL (1996) Pituitary adenylate cyclase activating polypeptide prevents apoptosis in cultured cerebellar granule neurons. Mol Pharmacol 50:60-66.
12. Chatterjee TK, Sharma RV, Fisher RA (1996) 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 271:32226-32232.
13. Cheng Y, Tao Y, Black IB, DiCicco-Bloom E (2001) A single peripheral injection of basic fibroblast growth factor (bFGF) stimulates granule cell production and increases cerebellar growth in newborn rats. J Neurobiol 46:220-229.
14. Cui H, Bulleit RF (1998) Potassium chloride inhibits proliferation of cerebellar granule neuron progenitors. Brain Res Dev Brain Res 106:129-135.
15. Cunningham JJ, Roussel MF (2001) Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12:387-396.
16. D'Agata V, Cavallaro S, Stivala F, Canonico PL (1996) Tissue-specific and developmental expression of pituitary adenylate cyclase-activating polypeptide (PACAP) receptors in rat brain. Eur J Neurosci 8:310-318.
17. Dahmane N, Ruiz-i-Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
18. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S (1999) Sonic Hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J Biol Chem 274:8143-8152.
19. DiCicco-Bloom E, Cohen RE, Black I (1989) Insulin growth factors regulate mitosis and survival in cultured cerebellar granule cells and precursors. Soc Neurosci Abstr 15:328.
20. DiCicco-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.
21. D'Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: Inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
22. Dong J, Gailani MR, Pomeroy SL, Reardon D, Bale AE (2000) Identification of PATCHED mutations in medulloblastomas by direct sequencing. Hum Mutat 16:89-90.
23. Echelard Y, Epstein DJ, St-Jacques B, Shen L, Mohler J, McMahon JA, McMahon AP (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75:1417-1430.
24. Fan CM, Porter JA, Chiang C, Chang DT, Beachy PA, Tessier-Lavigne M (1995) Long-range sclerotome induction by sonic hedgehog: Direct role of the amino-terminal cleavage product and modulation by the cyclic AMP signaling pathway. Cell 81:457-465.
25. Gao WO, Heintz N, Hatten ME (1991) Cerebellar granule cell neurogenesis is regulated by cell-cell interactions in vitro. Neuron 6:705-715.
26. Gonzalez BJ, Basille M, Vaudry D, Fournier A, Vaudry H (1997) Pituitary adenylate cyclase-activating polypeptide promotes cell survival and neurite outgrowth in rat cerebellar neuroblasts. Neuroscience 78:419-430.
27. Grewal SS, York RD, Stork PJ (1999) Extracellular-signal-regulated kinase signalling in neurons. Curr Opin Neurobiol 9:544-553.
28. Hammerschmidt M, Bitgood MJ, McMahon AP (1996) Protein kinase A is a common negative regulator of Hedgehog signaling in the vertebrate embryo. Genes Dev 10:647-658.
29. 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.
30. Hatten ME (1985) Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol 100:384-396.
31. Jaworski DM (2000) Expression of pituitary adenylate cyclase-activating polypeptide (PACAP) and the PACAP-selective receptor in cultured rat astrocytes, human brain tumors, and in response to acute intracranial injury. Cell Tissue Res 300:219-230.
32. Jaworski DM, Proctor MD (2000) Developmental regulation of pituitary adenylate cyclase-activating polypeptide and PAC(1) receptor mRNA expression in the rat central nervous system. Brain Res Dev Brain Res 120:27-39.
33. Jensen AM, Wallace VA (1997) Expression of Sonic hedgehog and its putative role as a precursor cell mitogen in the developing mouse retina. Development 124:363-371.
34. Kenney AM, Rowitch DH (2000) Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055-9067.
35. Kingsbury AE, Gallo V, Woodhams PL, Balazs R (1985) Survival, morphology and adhesion properties of cerebellar interneurones cultured in chemically defined and serum-supplemented medium. Brain Res 349:17-25.
36. Klein RS, Rubin JB, Gibson HD, DeHaan EN, Alvarez-Hernandez X, Segal RA, Luster AD (2001) SDF-1 alpha induces chemotaxis and enhances Sonic hedgehog-induced proliferation of cerebellar granule cells. Development 128:1971-1981.
37. Lelievre V, Hu Z, Byun JY, Ioffe Y, Wachek JA (2002) FGF-2 converts PACAP growth action on embryonic hindbrain precursors from stimulation to inhibition. J Neurosci Res 67:566-573.
38. Lezoualc'h F, Seugnet I, Monnier AL, Ghysdael J, Behr JP, Demeneix BA (1995) Inhibition of neurogenic precursor proliferation by antisense alpha thyroid hormone receptor oligonucleotides. J Biol Chem 270:12100-12108.
39. Lin X, Bulleit RF (1997) Insulin-like growth factor I (IGF-I) is a critical trophic factor for developing cerebellar granule cells. Brain Res Dev Brain Res 99:234-242.
40. Lindholm D, Skoglosa Y, Takei N (1998) Developmental regulation of pituitary adenylate cyclase activating polypeptide (PACAP) and its receptor 1 in rat brain: Function of PACAP as a neurotrophic factor. Ann NY Acad Sci 865:189-196.
41. 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 USA 94:3357-3362.
42. Lu N, Black IB, DiCicco-Bloom E (1996) A paradigm for distinguishing the roles of mitogenesis and trophism in neuronal precursor proliferation. Brain Res Dev Brain Res 94:31-36.
43. 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.
44. Lundblad JR, Kwok RP, Laurance ME, Harter ML, Goodman RH (1995) Adenoviral E1A-associated protein p300 as a functional homologue of the transcriptional co-activator CBP. Nature 374:85-88.
45. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ (1996) Biochemical evidence that patched is the Hedgehog receptor. Nature 384:176-179.
46. Moro O, Lerner EA (1997) Maxadilan, the vasodilator from sand flies, is a specific pituitary adenylate cyclase activating peptide type I receptor agonist. J Biol Chem 272:966-970.
47. Morrione A, Romano G, Navarro M, Reiss K, Valentinis B, Dews M, Eves E, Rosner MR, Baserga R (2000) Insulin-like growth factor I receptor signaling in differentiation of neuronal H19-7 cells. Cancer Res 60:2263-2272.
48. Niblock MM, Brunso-Bechtold JK, Riddle DR (2000) Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J Neurosci 20:4165-4176.
49. Nicot A, DiCicco-Bloom E (2001) Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc Natl Acad Sci USA 98:4758-4763.
50. Nielsen HS, Hannibal J, Fahrenkrug J (1998) Expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the postnatal and adult rat cerebellar cortex. NeuroReport 9:2639-2642.
51. Pisegna JR, Wank SA (1993) Molecular cloning and functional expression of the pituitary adenylate cyclase-activating polypeptide type I receptor. Proc Natl Acad Sci USA 90:6345-6349.
52. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, et al (2002) Prediction of central nervous system embryonal tumor outcome based on gene expression. Nature 415:436-442.
53. Pons S, Trejo JL, Martinez-Morales JR, Marti E (2001) Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128:1481-1492.
54. Ruiz i Altaba A (1999) Gli proteins and Hedgehog signaling: Development and cancer. Trends Genet 15:418-425.
55. Skoglosa Y, Patrone C, Lindholm D (1999) 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 265:207-210.
56. Smeyne RJ, Chu T, Lewin A, Bian F, S-Crisman S, Kunsch C, Lira SA, Oberdick J (1995) Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 6:230-251.
57. Solecki DJ, Liu XL, Tomoda T, Fang Y, Hatten ME (2001) Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 31:557-568.
58. 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.
59. Stone DM, Hynes M, Armanini M, Swanson TA, Gu Q, Johnson RL, Scott MP, Pennica D, Goddard A, Phillips H, Noll M, Hooper JE, Sauvage FD, Rosenthal A (1996) The tumor-suppressor gene patched encodes a candidate receptor for Sonic hedgehog. Nature 384:129-134.
60. 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.
61. Tabuchi A, Koizumi M, Nakatsubo J, Yaguchi T, Tsuda M (2001) Involvement of endogenous PACAP expression in the activity-dependent survival of mouse cerebellar granule cells. Neurosci Res 39:85-93.
62. Tao Y, Black IB, DiCicco-Bloom E (1996) Neurogenesis in neonatal rat brain is regulated by peripheral injection of basic fibroblast growth factor (bFGF). J Comp Neurol 376:653-663.
63. Testaz S, Jarov A, Williams KP, Ling LE, Koteliansky VE, Fournier-Thibault C, Duband JL (2001) Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the Patched-Smoothened-Gli signaling pathway. Proc Natl Acad Sci USA 98:12521-12526.
64. Toftgard R (2000) Hedgehog signalling in cancer. Cell Mol Life Sci 57:1720-1731.
65. Traiffort E, Charytoniuk D, Watroba L, Faure H, Sales N, Ruat M (1999) Discrete localizations of hedgehog signalling components in the developing and adult rat nervous system. Eur J Neurosci 11:3199-3214.
66. Vaudry D, Gonzalez BJ, Basille M, Fournier A, Vaudry H (1999) Neurotrophic activity of pituitary adenylate cyclase-activating polypeptide on rat cerebellar cortex during development. Proc Natl Acad Sci USA 96:9415-9420.
67. Villalba M, Bockaert J, Journot L (1997) 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 17:83-90.
68. Vogel MW, Sunter K, Herrup K (1989) Numerical matching between granule and Purkinje cells in lurcher chimeric mice: A hypothesis for the trophic rescue of granule cells from target-related cell death. J Neurosci 9:3454-3462.
69. Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curt Biol 9:445-448.
70. Waschek JA (2002) Multiple actions of pituitary adenylyl cyclase activating peptide in nervous system development and regeneration. Dev Neurosci 24:14-23.
71. Waschek JA, Casillas RA, Nguyen TB, DiCicco-Bloom EM, Carpenter EM, Rodriguez WI (1998) Neural tube expression of pituitary adenylate cyclase-activating polypeptide (PACAP) and receptor: Potential role in patterning and neurogenesis. Proc Natl Acad Sci USA 95:9602-9607.
72. Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22:103-114.
73. Wechsler-Reya RJ, Scott MP (2001) The developmental biology of brain tumors. Annu Rev Neurosci 24:385-428.
74. Wohl CA, Weiss S (1998) Retinoic acid enhances neuronal proliferation and astroglial differentiation in cultures of CNS stem cell-derived precursors. J Neurobiol 37:281-290.
75. Ye P, Xing Y, Dai Z, D'Ercole AJ (1996) In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: Evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 95:44-54.
76. Zurawel RH, Allen C, Wechsler-Reya R, Scott MP, Raffel C (2000) Evidence that haploinsufficiency of Patch leads to medulloblastoma in mice. Genes Chromosomes Cancer 28:77-81.