Retinoic acid and nitric oxide promote cell proliferation and differentially induce neuronal differentiation in vitro in the cnidarian Renilla koellikeri

Developmental Neurobiology

Volumn 70, Issue 12, 2010, Pages 842-852

  Estephane, Djoyce ^a   Anctil, Michel ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Cnidarian; Neuronal differentiation; Nitric oxide; Retinoic acid

Indexed keywords

ALITRETINOIN; NITRIC OXIDE; NITRIC OXIDE DONOR; POLYLYSINE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ADHESION; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; COELENTERATE; CONTROLLED STUDY; EPITHELIUM CELL; IN VITRO STUDY; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; RENILLA KOELLIKERI; SENSORY NERVE CELL;

ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EPITHELIAL CELLS; NEURITES; NEURONS; NITRIC OXIDE; RENILLA; TRETINOIN;

EID: 77957675036     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20824     Document Type: Article

References (69)

1. Achan V, Tran CTL, Arrigoni F, Whitley GS, Leiper JM, Vallance P. 2002. All-trans-Retinoic acid increases nitric oxide synthesis by endothelial cells. A role for the induction of dimethylarginine dimethylaminohydrolase. Circ Res 90:764-769.
2. Allenby G, Bocquel MT, Saunders M, Kazmer S, Speck J, Rosenberger M, Lovey A, et al. 1993. Retinoic acid receptors and retinoid X receptors: Interactions with endogenous retinoic acids. Proc Natl Acad Sci USA 90:30-34. (Pubitemid 23010243)
3. Anctil M, Poulain I, Pelletier C. 2005. Nitric oxide modulates peristaltic muscle activity associated with fluid circulation in the sea pansy Renilla koellikeri. J Exp Biol 208:2005-2018.
4. Andrews PA. 1984. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 103:285-293.
5. Bicker G. 2005. STOP and GO witn NO: Nitric oxide as a regulator of cell motility in simple brains. Bio Essays 27:495-505. (Pubitemid 40780852)
6. Bode HR. 1996. The interstitial cell lineage of hydra: A stem cell system that arose early in evolution. J Cell Sci 109:1155-1164.
7. Bosch TCG, Fujisawa T. 2001. Polyp, peptides and patterning. Bio Essays 23:420-427.
8. Bouzaiene M, Angers A, Anctil M. 2007. Immunohistochemical localization of a retinoic acid-like receptor in nerve cells of two colonial anthozoans (Cnidaria). Tissue Cell 39:123-130.
9. Cheung B, Hocker JE, Smith SA, Reichert U, Norris MD, Haber M, Stewart BW, Marshall GM. 1996. Retinoic acid receptors β and γ distinguish retinoid signals for growth inhibition and neuritogenesis in human neuroblastema cells. Biochem Biophys Res Commun 229:349-354.
10. Day RM, Lenhoff HM. 1981. Hydra mesoglea: A model for investigating epithelial cell-basement membrane interactions. Science 211:291-294.
11. Dmetrichuk JM, Carlone RL, Jones TRB, Vesprini ND, Spencer GE. 2006. Detection of endogenous retinoids in the molluscan CNS and characterization of the trophic and tropic actions of 9-cis retinoic acid on isolated neurons. J Neurosci 28:13014-13024.
12. Dmetrichuk JM, Carlone RL, Spencer GE. 2006. Retinoic acid induces neurite outgrowth and growth cone turning in invertebrate neurons. Dev Biol 294:39-49.
13. Estrada C, Murillo-Carretero M. 2005. Nitric oxide and adult neurogenesis in health and disease. Neuroscientist 11:294-307. (Pubitemid 41040859)
14. Fautin DG, Mariscal RN. 1991. Cnidaria: Anthozoa. In: Harrison FW, Westfall JA, editors. Microscopic Anatomy of Invertebrates, Vol. 2: Placozoa, Porifera, Cnidaria and Ctenophora. New York: Wiley-Liss, pp 267-358.
15. Frank U, Rabinowitz C, Rinkevich B. 1994. In vitro establishment of continuous cell cultures and cell lines from ten colonial cnidarians. Mar Biol 120:491-499.
16. Fritzenwanker JH, Genikhovich G, Kraus Y, Technau U. 2007. Early development and axis specification in the sea anemone Nematostella vectensis. Dev Biol 310:264-279. (Pubitemid 47483673)
17. Galliot B, Miljkovic-Licina M, de Rosa R, Chera S. 2006. Hydra, a niche for cell and developmental plasticity. Semin Cell Dev Biol 17:492-502. (Pubitemid 44314101)
18. Gauchat D, Escriva H, Miljkovic-Licina M, Chera S, Langlois M-C, Begue A, Laudet V, et al. 2004. The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev Biol 275:104-123. (Pubitemid 39298179)
19. Germain G, Anctil M. 1988. Luminescent activity and ultrastructural characterization of photocytes dissociated from the coelenterate Renilla köllikeri. Tissue Cell 20:701-720.
20. Ghigo D, Priotto C, Migliorino D, Geromin D, Franchino C, Todde R, Costamagna C, et al. 1998. Retinoic acid-induced differentiation in a human neuroblastoma cell line is associated with an increase in nitric oxide synthesis. J Cell Physiol 174:99-106. (Pubitemid 128492437)
21. Giannini G, Dawson MI, Zhang X-K, Thiele CJ. 1997. Activation of three distinct RXR/RAR heterodimers induces growth arrest and differentiation of neuroblastoma cells. J Biol Chem 272:26693-26701. (Pubitemid 27458895)
22. Gibbs SM. 2003. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol Neurobiol 27:107-120.
23. Haase A, Bicker G. 2003. Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development 130:3977-3987.
24. Hager G, David CN. 1997. Pattern of differentiated nerve cells in hydra is determined by precursor migration. Development 124:569-576. (Pubitemid 27101690)
25. Henion PD, Weston JA. 1994. Retinoic acid selectively promotes the survival and proliferation of neurogenic precursors in cultured neural crest cell populations. Dev Biol 161:243-250.
26. Knack BA, Iguchi A, Shinzato C, Hayward DC, Ball EE, Miller DJ. 2008. Unexpected diversity of cnidarian integrins: Expression during coral integration. BMC Evol Biol 8:136. (Pubitemid 351749362)
27. Kostrouch Z, Kostrouchova M, Love W, Jannini E, Piatigorsky J, Rall JE. 1998. Retinoic acid X receptor in the diploblast, Tripedalia cystophora. Proc Natl Acad Sci USA 95:13442-13447.
28. Krumenacker JS, Murad F. 2006. NO-cGMP signaling in development and stem cells. Mol Genet Metab 87:311-314.
29. Kurz E, Schmid V. 1991. Effects of tumor promoters and diacylglycerol on the transdifferentiation of striated muscle cells of the medusa Podocoryne carnea to RFamide positive nerve cells. In: Williams RB, Cornelius PFS, Hughes RG, Robson EA, editors. Coelenterate Biology: Recent Research on Cnidaria and Ctenophora. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp 11-17.
30. Kuzin B, Roberts I, Peunova N, Enikolopov G. 1996. Nitric oxide regulates cell proliferation during Drosophila development. Cell 87:639-649.
31. Lefebvre PP, Malgrange B, Staecker H, Moonen G, Van De Water TR. 1993. Retinoic acid stimulates regeneration of mammalian auditory hair cell. Science 260:692-695. (Pubitemid 23167595)
32. Liu J-P, Laufer E, Jessell TM. 2001. Assigning the positional identity of spinal motor neurons: Rostrocaudal patterning of Hox-c expression by Fgfs. Gdf11, and retinoids Neuron 32:997-1012.
33. Maden M. 2007. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nature Rev Neurosci 8:755-765.
34. Maden M, Gale E, Kostetskii I, Zile M. 1996. Vitamin A-deficient quail embryos have half a midbrain and other neural defects. Curr Biol 6:417-426. (Pubitemid 126656289)
35. Magie CR, Martindale MQ. 2008. Cell-cell adhesion in the Cnidaria: Insights into the evolution of tissue morphogenesis. Biol Bull 214:218-232.
36. Matus DQ, Thomsen GH, Martindale MQ. 2007. FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian. Dev Genes Evol 217:137-148.
37. Mejia-Garcia TA, Paes-de-Carvalho R. 2007. Nitric oxide regulates cell survival in purified cultures of avian retinal neurons: Involvement of multiple transduction pathways. J Neurochem 100:382-394.
38. Minobe S, Koizumi O, Sugiyama T. 1995. Nerve cell differentiation in nerve-free tissue of epithelial hydra from precursor cells introduced by grafting. I. Tentacles and hypostome. Dev Biol 172:170-181.
39. Moroz LL. 2001. Gaseous transmission across time and species. Am Zool 41:304-320. (Pubitemid 33770229)
40. Moroz LL, Meech RW, Sweedler JV, Mackie GO. 2004. Nitric oxide regulates swimming in the jellyfish Aglantha digitale. J Comp Neurol 471:26-36.
41. Müller WA. 1984. Retinoids and pattern formation in a hydroid. J Embryol Exp Morph 81:253-271.
42. Nabeyrat E, Besnard V, Corroyer S, Cazals V, Clément A. 1998. Retinoic acid-induced proliferation of lung alveolar epithelial cells: Relation with the IGF system. Am J Physiol 275:L71-L79. (Pubitemid 28376227)
43. Neuman K, Soosaar A, Nornes HO, Neuman T. 1995. Orphan receptor COUP-TF I antagonizes retinoic acid-induced neuronal differentiation. J Neurosci Res 41: 39-48.
44. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, et al. 2003. Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566-9571. (Pubitemid 37033968)
45. Pani AK, Anctil M, Umbriaco D. 1994. Neuronal localization and evoked release of norepinephrine in the cnidarian Renilla koellikeri. J Exp Zool 272:1-12.
46. Pernet V, Anctil M, Grimmelikhuijzen CJP. 2004. Antho-RFamide-containing neurons in the primitive nervous system of the anthozoan Renilla koellikeri. J Comp Neurol 472:208-220. (Pubitemid 38429021)
47. Peunova N, Enikolopov G. 1995. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375:68-73.
48. Przysiezniak J, Spencer AN. 1989. Primary culture of identified neurones from a cnidarian. J Exp Biol 142:97-113.
49. Raz Y, Kelley MW. 1999. Retinoic acid signaling is necessary for the development of the organ of Corti. Dev Biol 213:180-193. (Pubitemid 29409955)
50. Schaller HC, Hoffmeister SA, Dubel S. 1989. Role of the neuropeptide head activator for growth and development in hydra and mammals. Development 107:99-107. (Pubitemid 20055060)
51. Schetz JA, Anderson PAV. 1993. Investigations of lipid components of neurone-enriched membranes of the jellyfish Cyanea capillata. J Exp Biol 177:23-39.
52. Schmid V, Ono S-I, Reber-Müller S. 1999. Cell-substrate interactions in Cnidaria. Microsc Res Tech 44:254-268.
53. Schmid V, Reber-Müller S. 1995. Transdifferentiation of isolated striated muscle of jellyfish in vitro: The initiation process. Sem Cell Biol 6:109-116.
54. Seidel C, Bicker G. 2000. Nitric oxide and cGMP influence axogenesis of antennal pioneer neurons. Development 127:4541-4549.
55. Seipel K, Eberhardt M, Müller P, Pescia E, Yanze N, Schmid V. 2004. Homologs of vascular endothelial growth factor and receptor, VEGF and VEGFR, in the jellyfish Podocoryne camea. Dev Dynamics 231:303-312.
56. Shapiro SS. 1986. Retinoids and epithelial differentiation. In: Sherman MI, editor. Retinoids and Cell Differentiation. Boca Raton: CRC Press, pp 29-60.
57. Sidell N. 1981. Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst 68:589-596.
58. Sidell N, Altman A, Haussler MR. 1983. Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp Cell Res 148:21-30. (Pubitemid 14231413)
59. Steele RE, Lieu P, Mai NH, Shenk MA, Sarras MP Jr. 1996. Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggest a role for an insulin-like molecule in regulating growth and patterning in Hydra. Dev Genes Evol 206:247-259. (Pubitemid 126774742)
60. Takahashi T, Koizumi O, Ariura Y, Romanovitch A, Bosch TCG, Kobayakawa Y, Mohri S, et al. 2000. A novel neuropeptide. Hym-355, positively regulates neuron differentiation in hydra. Development 127:997-1005.
61. Takahashi T, Muneoka Y, Lohmann J, Lopez deHaro MS, Solleder G, Bosch TCG, David CN, et al. 1997. Systematic isolation of peptide signal molecules regulating development in hydra: Lwamide and PW families. Proc Natl Acad Sci USA 94:1241-1246.
62. Tota B, Trimmer B, editors. Nitric Oxide. Amsterdam: Elsevier B.V.390 p.
63. Trimm KR, Rehder V. 2004. Nitric oxide acts as a slow-down and search signal in developing neurites. Eur J Neurosci 19:809-818.
64. Ulibarri JA, Mozdziak PE, Schultz E, Cook C, Best TM. 1999. Nitric oxide donors, sodium nitroprusside and S-Nitroso-N-acetylpenicillamine, stimulate myoblast prolifereation in vitro. In Vitro Cell Dev Biol Anim 35:215-218. (Pubitemid 29181357)
65. Urano A, Sugawara A, Kanatsuka H, Kagechika H, Saito A, Sato K, Kudo M, Takeuchi K, Ito S. 2005. Upregulation of nitric oxide production in vascular endothelial cells by all-trans retinoic acid through the phosphoinositide 3-kinase/Akt pathway. Circulation 112:727-736. (Pubitemid 41099053)
66. Varon S. 1979. The culture of chick embryo dorsal root ganglionic cells on polylysine-coated plastic. Neurochem Res 4:155-173. (Pubitemid 9244361)
67. Wiens M, Batel R, Korzhev M, Müller WEG. 2003. Retinoic X receptor and retinoic acid response in the marine sponge Suberites domuncula. J Exp Biol 206:3261-3271. (Pubitemid 37181424)
68. Wilson L, Gale E, Chambers D, Maden M. 2004. The role of retinoic acid in the dorsoventral patterning of the spinal cord. Dev Biol 269:433-446. (Pubitemid 38521109)
69. 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. (Pubitemid 28478250)