Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal polypeptide promote the genesis of calcium currents in differentiating mouse embryonic stem cells

Neuroscience

Volumn 199, Issue , 2011, Pages 103-115

  Chafai, M ^a   Basille, M ^a   Galas, L ^a   Rostene, W ^b   Gressens, P ^c   Vaudry, H ^a,d   Gonzalez, B J ^a   Louiset, E ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b INSTITUT DE LA VISION   (France)

^c HÔPITAL ROBERT DEBRÉ   (France)

^d International Associated Laboratory Samuel de Champlain   (France)

Author keywords

C jun amino terminal kinase1; Extracellular signal regulated kinase 1 and 2; L type calcium channel; Neuronal differentiation; T type calcium channel

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL L TYPE ALPHA1C SUBUNIT; CALCIUM CHANNEL L TYPE ALPHA1D SUBUNIT; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL N TYPE ALPHA1B SUBUNIT; CALCIUM CHANNEL T TYPE; CALCIUM CHANNEL T TYPE ALPHA1G SUBUNIT; CALCIUM CHANNEL T TYPE ALPHA1I SUBUNIT; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE; HYPOPHYSIS ADENYLATE CYCLASE ACTIVATING POLYPEPTIDE RECEPTOR 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEURON SPECIFIC ENOLASE; STRESS ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 1; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CALCIUM CHANNELS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; MICE; NEURAL STEM CELLS; NEUROGENESIS; PITUITARY ADENYLATE CYCLASE-ACTIVATING POLYPEPTIDE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASOACTIVE INTESTINAL PEPTIDE;

EID: 83055184251     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.09.062     Document Type: Article

References (81)

1. Allais A., Burel D., Isaac E.R., Gray S.L., Basille M., Ravni A., Sherwood N.M., Vaudry H., Gonzalez B.J. Altered cerebellar development in mice lacking pituitary adenylate cyclase-activating polypeptide. Eur J Neurosci 2007, 25:2604-2618.
2. Arnhold S., Andressen C., Angelov D.N., Vajna R., Volsen S.G., Hescheler J., Addicks K. Embryonic stem-cell derived neurones express a maturation dependent pattern of voltage-gated calcium channels and calcium-binding proteins. Int J Dev Neurosci 2000, 18:201-212.
3. Balster D.A., O'Dorisio M.S., Albers A.R., Park S.K., Qualman S.J. Suppression of tumorigenicity in neuroblastoma cells by upregulation of human vasoactive intestinal peptide receptor type 1. Regul Pept 2002, 109:155-165.
4. 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.
5. Bibel M., Richter J., Schrenk K., Tucker K.L., Staiger V., Korte M., Goetz M., Barde Y.A. Differentiation of mouse embryonic stem cells into a defined neuronal lineage. Nat Neurosci 2004, 7:1003-1009.
6. Carpenter M.K., Inokuma M.S., Denham J., Mujtaba T., Chiu C.P., Rao M.S. Enrichment of neurons and neural precursors from human embryonic stem cells. Exp Neurol 2001, 172:383-397.
7. Cazillis M., Gonzalez B.J., Billardon C., Lombet A., Fraichard A., Samarut J., Gressens P., Vaudry H., Rostène W. VIP and PACAP induce selective neuronal differentiation of mouse embryonic stem cells. Eur J Neurosci 2004, 19:798-808.
8. Chafai M., Louiset E., Basille M., Cazillis M., Vaudry D., Rostène W., Gressens P., Vaudry H., Gonzalez B.J. PACAP and VIP promote initiation of electrophysiological activity in differentiating embryonic stem cells. Ann N Y Acad Sci 2006, 1070:185-189.
9. Chambers I., Smith A. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 2004, 23:7150-7160.
10. Chatzi C., Scott R.H., Pu J., Lang B., Nakamoto C., McCaig C.D., Shen S. Derivation of homogeneous GABAergic neurons from mouse embryonic stem cells. Exp Neurol 2009, 217:407-416.
11. Chemin J., Nargeot J., Lory P. Neuronal T-type alpha 1H calcium channels induce neuritogenesis and expression of high-voltage-activated calcium channels in the NG108-15 cell line. J Neurosci 2002, 22:6856-6862.
12. Cui L., Jiang J., Wei L., Zhou X., Fraser J.L., Snider B.J., Yu S.P. Transplantation of embryonic stem cells improves nerve repair and functional recovery after severe sciatic nerve axotomy in rats. Stem Cells 2008, 26:1356-1365.
13. D'Ascenzo M., Piacentini R., Casalbore P., Budoni M., Pallini R., Azzena G.B., Grassi C. Role of L-type Ca2+ channels in neural stem/progenitor cell differentiation. Eur J Neurosci 2006, 23:935-944.
14. Desmadryl G., Hilaire C., Vigues S., Diochot S., Valmier J. Developmental regulation of T-, N- and L-type calcium currents in mouse embryonic sensory neurones. Eur J Neurosci 1998, 10:545-552.
15. Dolphin A.C. Calcium channel diversity: multiple roles of calcium channel subunits. Curr Opin Neurobiol 2009, 19:237-244.
16. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981, 292:154-156.
17. Falluel-Morel A., Tascau L.I., Sokolowski K., Brabet P., DiCicco-Bloom E. Granule cell survival is deficient in PAC1-/- mutant cerebellum. J Mol Neurosci 2008, 36:38-44.
18. Fukuda H., Takahashi J. Embryonic stem cells as a cell source for treating Parkinson's disease. Expert Opin Biol Ther 2005, 5:1273-1280.
19. Giladi E., Hill J.M., Dresner E., Stack C.M., Gozes I. Vasoactive intestinal peptide (VIP) regulates activity-dependent neuroprotective protein (ADNP) expression in vivo. J Mol Neurosci 2007, 33:278-283.
20. Ginty D.D., Bading H., Greenberg M.E. Trans-synaptic regulation of gene expression. Curr Opin Neurobiol 1992, 2:312-316.
21. Goncalves M.B., Agudo M., Connor S., McMahon S., Minger S.L., Maden M., Corcoran J.P. Sequential RARbeta and alpha signalling in vivo can induce adult forebrain neural progenitor cells to differentiate into neurons through Shh and FGF signalling pathways. Dev Biol 2009, 326:305-313.
22. Gonzalez B.J., 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.
23. Gonzalez B.J., Basille M., Vaudry D., Fournier A., Vaudry H. Pituitary adenylate cyclase-activating polypeptide. Ann Endocrinol 1998, 59:364-405.
24. Gressens P. Vasoactive intestinal peptide: a novel neurotrophic factor. Arch Pediatr 1998, 5:654-660.
25. Gressens P., Besse L., Robberecht P., Gozes I., Fridkin M., Evrard P. Neuroprotection of the developing brain by systemic administration of vasoactive intestinal peptide derivatives. J Pharmacol Exp Ther 1999, 288:1207-1213.
26. Grumolato L., Louiset E., Alexandre D., Aït-Ali D., Turquier V., Fournier A., Fasolo A., Vaudry H., 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 2003, 17:71-82.
27. Gu X., Spitzer N.C. Low-threshold Ca2+ current and its role in spontaneous elevations of intracellular Ca2+ in developing Xenopus neurons. J Neurosci 1993, 13:4936-4948.
28. Gutiérrez-Cañas I., Juarranz M.G., Collado B., Rodríguez-Henche N., Chiloeches A., Prieto J.C., Carmena M.J. Vasoactive intestinal peptide induces neuroendocrine differentiation in the LNCaP prostate cancer cell line through PKA, ERK, and PI3K. Prostate 2005, 63:44-55.
29. Hamelink C., Lee H.W., Hsu C.M., Eiden L.E. Role of protein kinases in neuropeptide gene regulation by PACAP in chromaffin cells: a pharmacological and bioinformatic analysis. Ann N Y Acad Sci 2002, 971:474-490.
30. Héraud C., Hilairet S., Muller J.M., Leterrier J.F., Chadéneau 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 2004, 75:320-329.
31. Hill J.M. Vasoactive intestinal peptide in neurodevelopmental disorders: therapeutic potential. Curr Pharm Des 2007, 13:1079-1089.
32. Hill J.M., Glazner G.W., Lee S.J., Gozes I., Gressens P., Brenneman D.E. Vasoactive intestinal peptide regulates embryonic growth through the action of activity-dependent neurotrophic factor. Ann N Y Acad Sci 1999, 897:92-100.
33. Hirooka K., Bertolesi G.E., Kelly M.E., Denovan-Wright E.M., Sun X., Hamid J., Zamponi G.W., Juhasz A.E., Haynes L.W., Barnes S. T-type calcium channel alpha1G and alpha1H subunits in human retinoblastoma cells and their loss after differentiation. J Neurophysiol 2002, 88:196-205.
34. Hirose M., Hashimoto H., Shintani N., Nakanishi M., Arakawa N., Iga J., Niwa H., Miyazaki J., Baba A. Differential expression of mRNAs for PACAP and its receptors during neural differentiation of embryonic stem cells. Regul Pept 2005, 126:109-113.
35. Iftinca M., Hamid J., Chen L., Varela D., Tadayonnejad R., Altier C., Turner R.W., Zamponi G.W. Regulation of T-type calcium channels by Rho-associated kinase. Nat Neurosci 2007, 10:854-860.
36. Jolivel V., Basille M., Aubert N., de Jouffrey S., Ancian P., Le Bigot J.F., Noack P., Massonneau M., Fournier A., Vaudry H., Gonzalez B.J., Vaudry D. Distribution and functional characterization of pituitary adenylate cyclase-activating polypeptide receptors in the brain of non-human primates. Neuroscience 2009, 160:434-451.
37. Laburthe M., Couvineau A., Marie J.C. VPAC receptors for VIP and PACAP. Receptors Channels 2002, 8:137-153.
38. Lelievre V., Hu Z., Byun J.Y., Ioffe Y., Waschek J.A. Fibroblast growth factor-2 converts PACAP growth action on embryonic hindbrain precursors from stimulation to inhibition. J Neurosci Res 2002, 67:566-573.
39. Lelièvre V., Meunier A.C., Caigneaux E., Falcon J., Muller J.M. Differential expression and function of PACAP and VIP receptors in four human colonic adenocarcinoma cell lines. Cell Signal 1998, 10:13-26.
40. Li W., Chang L., Rong Z., Zhang Q., Wang H., Wang H., Liu C., Liu W. Mechanism of retinoic acid and mitogen-activated protein kinases regulating hyperoxia lung injury. J Huazhong Univ Sci Technolog Med Sci 2006, 26:178-181.
41. Li Z., Theus M.H., Wei L. Role of ERK 1/2 signaling in neuronal differentiation of cultured embryonic stem cells. Dev Growth Differ 2006, 48:513-523.
42. 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 U S A 1997, 94:3357-3362.
43. 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.
44. Matsuda R., Yoshikawa M., Kimura H., Ouji Y., Nakase H., Nishimura F., Nonaka J., Toriumi H., Yamada S., Nishiofuku M., Moriya K., Ishizaka S., Nakamura M., Sakaki T. Cotransplantation of mouse embryonic stem cells and bone marrow stromal cells following spinal cord injury suppresses tumor development. Cell Transplant 2009, 18:39-54.
45. McCobb D.P., Best P.M., Beam K.G. Development alters the expression of calcium currents in chick limb motoneurons. Neuron 1989, 2:1633-1643.
46. Mercer A., Rönnholm H., Holmberg J., Lundh H., Heidrich J., Zachrisson O., Ossoinak A., Frisén J., Patrone C. PACAP promotes neural stem cell proliferation in adult mouse brain. J Neurosci Res 2004, 76:205-215.
47. Meyer J.S., Katz M.L., Maruniak J.A., Kirk M.D. Embryonic stem cell-derived neural progenitors incorporate into degenerating retina and enhance survival of host photoreceptors. Stem Cells 2006, 24:274-283.
48. Milligan G. G protein-coupled receptor hetero-dimerization: contribution to pharmacology and function. Br J Pharmacol 2009, 158:5-14.
49. Miyata A., Arimura A., Dahl R.R., Minamino N., Uehara A., Jiang L., Culler M.D., Coy D.H. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 1989, 164:567-574.
50. Monaghan T.K., Pou C., MacKenzie C.J., Plevin R., Lutz E.M. Neurotrophic actions of PACAP-38 and LIF on human neuroblastoma SH-SY5Y cells. J Mol Neurosci 2008, 36:45-56.
51. Muñoz-Sanjuán I., Brivanlou A.H. Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 2002, 3:271-280.
52. Nam C., Case A.J., Hostager B.S., O'Dorisio M.S. The role of vasoactive intestinal peptide (VIP) in megakaryocyte proliferation. J Mol Neurosci 2009, 37:160-167.
53. Nicot A., DiCicco-Bloom E. Regulation of neuroblast mitosis is determined by PACAP receptor isoform expression. Proc Natl Acad Sci U S A 2001, 98:4758-4763.
54. Nicot A., Lelièvre V., Tam J., Waschek J.A., DiCicco-Bloom E. Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J Neurosci 2002, 22:9244-9254.
55. Nowycky M.C., Fox A.P., Tsien R.W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 1985, 316:440-443.
56. Ohta S., Gregg C., Weiss S. Pituitary adenylate cyclase-activating polypeptide regulates forebrain neural stem cells and neurogenesis in vitro and in vivo. J Neurosci Res 2006, 84:1177-1186.
57. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 2003, 83:117-161.
58. Piacentini R., Ripoli C., Mezzogori D., Azzena G.B., Grassi C. Extremely low-frequency electromagnetic fields promote in vitro neurogenesis via upregulation of Ca(v)1-channel activity. J Cell Physiol 2008, 215:129-139.
59. Pincus D.W., DiCicco-Bloom E.M., Black I.B. Vasoactive intestinal peptide regulates mitosis, differentiation and survival of cultured sympathetic neuroblasts. Nature 1990, 343:564-567.
60. Ravni A., Vaudry D., Gerdin M.J., Eiden M.V., Falluel-Morel A., Gonzalez B.J., Vaudry H., Eiden L.E. A cAMP-dependent, protein kinase A-independent signaling pathway mediating neuritogenesis through Egr1 in PC12 cells. Mol Pharmacol 2008, 73:1688-1708.
61. Said S.I., Mutt V. Polypeptide with broad biological activity: isolation from small intestine. Science 1970, 169:1217-1218.
62. Scharf E., May V., Braas K.M., Shutz K.C., Mao-Draayer Y. Pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) regulate murine neural progenitor cell survival, proliferation, and differentiation. J Mol Neurosci 2008, 36:79-88.
63. Sexton P.M., Poyner D.R., Simms J., Christopoulos A., Hay D.L. Modulating receptor function through RAMPs: can they represent drug targets in themselves?. Drug Discov Today 2009, 14:413-419.
64. Sheward W.J., Lutz E.M., Harmar A.J. 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.
65. Shuto Y., Uchida D., Onda H. Ontogeny of pituitary adenylate cyclase activating polypeptide and its receptor mRNA in the mouse brain. Regul Pept 1996, 67:79-83.
66. Sokolowska P., Nowak J.Z. Effects of PACAP and VIP on cAMP-generating system and proliferation of C6 glioma cells. J Mol Neurosci 2008, 36:286-291.
67. Soundararajan P., Miles G.B., Rubin L.L., Brownstone R.M., Rafuse V.F. Motoneurons derived from embryonic stem cells express transcription factors and develop phenotypes characteristic of medial motor column neurons. J Neurosci 2006, 26:3256-3268.
68. Ster J., De Bock F., Guérineau N.C., Janossy A., Barrère-Lemaire S., Bos J.L., Bockaert J., Fagni L. Exchange protein activated by cAMP (Epac) mediates cAMP activation of p38 MAPK and modulation of Ca2+-dependent K+ channels in cerebellar neurons. Proc Natl Acad Sci U S A 2007, 104:2519-2524.
69. Suh J, Lu N, Nicot A, Tatsuno I, DiCicco-Bloom E (2001) PACAP is an anti-mitogenic signal in developing cerebral cortex 4:123-124.
70. Thomson J.A., Marshall V.S., Trojanowski J.Q. Neural differentiation of rhesus embryonic stem cells. APMIS 1998, 106:149-157.
71. Trimmer J.S., Rhodes K.J. Localization of voltage-gated ion channels in mammalian brain. Annu Rev Physiol 2004, 66:477-519.
72. Vaudry D., Chen Y., Ravni A., Hamelink C., Elkahloun A.G., Eiden L.E. Analysis of PC12 cell transcriptome after differentiation with pituitary adnylate cyclase-activating polypeptide (PACAP). J Neurochem 2002, 83:1272-1284.
73. Vaudry D., Falluel-Morel A., Bourgault S., Basille M., Burel D., Wurtz O., Fournier A., Chow B.K., Hashimoto H., Galas L., Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 2009, 61:283-357.
74. Vaudry D., Gonzalez B.J., Basille M., Pamantung T.F., 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 U S A 2000, 97:13390-13395.
75. Vaudry D., Gonzalez B.J., Basille M., Yon L., Fournier A., Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from a structure to functions. Pharmacol Rev 2000, 52:269-324.
76. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649.
77. 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.
78. Waschek J.A., Casillas R.A., Nguyen T.B., DiCicco-Bloom E.M., Carpenter E.M., Rodriguez W.I. Neural tube expression of pituitary adenylate cyclase-activating peptide (PACAP) and receptor: potential role in patterning and neurogenesis. Proc Natl Acad Sci U S A 1998, 95:9602-9607.
79. Wichterle H., Peljto M. Differentiation of mouse embryonic stem cells to spinal motor neurons. Curr Protoc Stem Cell Biol 2008, Chapter 1:Unit 1H.1.1-1H.1.9.
80. Ying Q.L., Wray J., Nichols J., Batlle-Morera L., Doble B., Woodgett J., Cohen P., Smith A. The ground state of embryonic stem cell self-renewal. Nature 2008, 453:519-523.
81. Yunker A.M., McEnery M.W. Low-voltage-activated ("T-Type") calcium channels in review. J Bioenerg Biomembr 2003, 35:533-575.