Retinoic acid regulates the expression of dorsoventral topographic guidance molecules in the chick retina

Development

Volumn 132, Issue 23, 2005, Pages 5147-5159

  Sen, Jonaki ^a   Harpavat, Sanjiv ^a   Peters, Maureen A ^b   Cepko, Constance L ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b OBERLIN COLLEGE   (United States)

Author keywords

Dorsoventral; EphB; Ephrin B; Patterning; Retinoic acid; Retinotectal map

Indexed keywords

EPHRIN B2; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B3; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR VAX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHICKEN; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME SYNTHESIS; GENE EXPRESSION REGULATION; HOMEOSTASIS; IN SITU HYBRIDIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA DEVELOPMENT; RETINOTECTAL PROJECTION; SIGNAL TRANSDUCTION;

ANIMALS; AVIAN PROTEINS; BODY PATTERNING; CHICK EMBRYO; EPHRIN-B2; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HOMEOSTASIS; RECEPTOR, EPHB2; RECEPTOR, EPHB3; RECEPTORS, RETINOIC ACID; RETINA; TRETINOIN;

ANIMALIA;

EID: 29244433023     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02100     Document Type: Article

References (81)

1. Abu-Abed, S., MacLean, G., Fraulob, V., Chambon, P., Petkovich, M. and Dolle, P. (2002). Differential expression of the retinoic acid-metabolizing enzymes CYP26A1 and CYP26B1 during murine organogenesis. Mech. Dev. 110, 173-177.
2. Alexiades, M. R. and Cepko, C. (1996). Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev. Dyn. 205, 293-307.
3. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. (1998). Current Protocols in Molecular Biology. New York: Wiley Publishing.
4. Baniahmad, A., Tsai, S. Y., O'Malley, B. W. and Tsai, M. J. (1992). Kindred S thyroid hormone receptor is an active and constitutive silencer and a repressor for thyroid hormone and retinoic acid responses. Proc. Natl. Acad. Sci. USA 89, 10633-10637.
5. Barbieri, A. M., Broccoli, V., Bovolenta, P., Alfano, G., Marchitiello, A., Mocchetti, C., Crippa, L., Bulfone, A., Marigo, V., Ballabio, A. et al. (2002). Vax2 inactivation in mouse determines alteration of the eye dorsal-ventral axis, misrouting of the optic fibres and eye coloboma. Development 129, 805-813.
6. Birgbauer, E., Cowan, C. A., Sretavan, D. W. and Henkemeyer, M. (2000). Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127, 1231-1241.
7. Blackshaw, S., Harpavat, S., Trimarchi, J., Cai, L., Huang, H., Kuo, W. P., Weber, G., Lee, K., Fraioli, R. E., Cho, S. H. et al. (2004). Genomic analysis of mouse retinal development. PLoS Biol. 2, E247.
8. Blentic, A., Gale, E. and Maden, M. (2003). Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev. Dyn. 227, 114-127.
9. Braisted, J. E., McLaughlin, T., Wang, H. U., Friedman, G. C., Anderson, D. J. and O'Leary, D, D. (1997). Graded and lamina-specific distributions of ligands of EphB receptor tyrosine kinases in the developing retinotectal system. Dev. Biol. 191, 14-28.
10. Bruhn, S. L. and Cepko, C. L. (1996). Development of the pattern of photoreceptors in the chick retina. J. Neurosci. 16, 1430-1439.
11. Chen, C. M. and Cepko, C. L. (2002). The chicken RaxL gene plays a role in the initiation of photoreceptor differentiation. Development 129, 5363-5375.
12. Cheng, H. J., Nakamoto, M., Bergemann, A. D. and Flanagan, J. G. (1995). Complementary gradients in expression and binding of ELF-1 and Mek4 in development of the topographic retinotectal projection map. Cell 82, 371-381.
13. Connor, R. J., Menzel, P. and Pasquale, E. B. (1998). Expression and tyrosine phosphorylation of Eph receptors suggest multiple mechanisms in patterning of the visual system. Dev. Biol. 193, 21-35.
14. Crossland, W. J., Cowan, W. M., Rogers, L. A. and Kelly, J. P. (1974). The specification of the retino-tectal projection in the chick. J. Comp. Neurol. 155, 127-164.
15. Damm, K., Thompson, C. C. and Evans, R. M. (1989). Protein encoded by v-erbA functions as a thyroid-hormone receptor antagonist. Nature 339, 593-597.
16. Damm, K., Heyman, R. A., Umesono, K. and Evans, R. M. (1993). Functional inhibition of retinoic acid response by dominant negative retinoic acid receptor mutants. Proc. Natl. Acad. Sci. USA 90, 2989-2993.
17. Drescher, U., Kremoser, C., Handwerker, C., Loschinger, J., Noda, M. and Bonhoeffer, F. (1995). In vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82, 359-370.
18. Dupe, V., Matt, N., Garnier, J. M., Chambon, P., Mark, M. and Ghyselinck, N. B. (2003). A newborn lethal defect due to inactivation of retinaldehyde dehydrogenase type 3 is prevented by maternal retinoic acid treatment. Proc. Natl. Acad. Sci. USA 100, 14036-14041.
19. Fan, X., Molotkov, A., Manabe, S., Donmoyer, C. M., Deltour, L., Foglio, M. H., Cuenca, A. E., Blaner, W. S., Lipton, S. A. and Duester, G. (2003). Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol. Cell. Biol. 23, 4637-4648.
20. Feldheim, D. A., Kim, Y. I., Bergemann, A. D., Frisen, J., Barbacid, M. and Flanagan, J. G. (2000). Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563-574.
21. Fujii, H., Sato, T., Kaneko, S., Gotoh, O., Fujii-Kuriyama, Y., Osawa, K., Kato, S. and Hamada, H. (1997). Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J. 16, 4163-4173.
22. Grondona, J. M., Kastner, P., Gansmuller, A., Decimo, D., Chambon, P. and Mark, M. (1996). Retinal dysplasia and degeneration in RARbeta2/ RARgamma2 compound mutant mice. Development 122, 2173-2188.
23. Grun, F., Hirose, Y., Kawauchi, S., Ogura, T. and Umesono, K. (2000). Aldehyde dehydrogenase 6, a cytosolic retinaldehyde dehydrogenase prominently expressed in sensory neuroepithelia during development. J. Biol. Chem. 275, 41210-41218.
24. Hale, F. (1937). The relation of maternal vitamin A deficiency to micropthalmia in pigs. Tex. State J. Med. 33, 228-232.
25. Hamburger, V. and Hamilton, H. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 35-46.
26. Hindges, R., McLaughlin, T., Genoud, N., Henkemeyer, M. and O'Leary, D. D. (2002). EphB forward signaling controls directional branch extension and arborization required for dorsal-ventral retinotopic mapping. Neuron 35, 475-487.
27. Holash, J. A. and Pasquale, E. B. (1995). Polarized expression of the receptor protein tyrosine kinase Cek5 in the developing avian visual system. Dev. Biol. 172, 683-693.
28. Hyatt, G. A. and Dowling, J. E. (1997). Retinoic acid. A key molecule for eye and photoreceptor development. Invest. Ophthalmol. Vis. Sci. 38, 1471-1475.
29. Hyatt, G. A., Schmitt, E. A., Fadool, J. M. and Dowling, J. E. (1996a). Retinoic acid alters photoreceptor development in vivo. Proc. Natl. Acad. Sci. USA 93, 13298-13303.
30. Hyatt, G. A., Schmitt, E. A., Marsh-Armstrong, N., McCaffery, P., Drager, U. C. and Dowling, J. E. (1996b). Retinoic acid establishes ventral retinal characteristics. Development 122, 195-204.
31. Kalter, H. and Warkany, J. (1959). Experimental production of congenital maiformations in mammals by metabolic procedure. Physiol. Rev. 39, 69-115.
32. Kastner, P., Mark, M., Ghyselinck, N., Krezel, W., Dupe, V., Grondona, J. M. and Chambon, P. (1997). Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124, 313-326.
33. Kliewer, S. A., Umesono, K., Mangelsdorf, D. J. and Evans, R. M. (1992). Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 355, 446-449.
34. Koshiba-Takeuchi, K., Takeuchi, J. K., Matsumoto, K., Momose, T., Uno, K., Hoepker, V., Ogura, K., Takahashi, N., Nakamura, H., Yasuda, K. et al. (2000). Tbx5 and the retinotectum projection. Science 287, 134-137.
35. Labrecque, J., Dumas, F., Lacroix, A. and Bhat, P. V. (1995). A novel isoenzyme of aldehyde dehydrogenase specifically involved in the biosynthesis of 9-cis and all-trans retinoic acid. Biochem. J. 305, 681-684.
36. Lee, M. O., Manthey, C. L. and Sladek, N. E. (1991). Identification of mouse liver aldehyde dehydrogenases that catalyze the oxidation of retinaldehyde to retinoic acid. Biochem. Pharmacol. 42, 1279-1285.
37. Li, H., Wagner, E., McCaffery, P., Smith, D., Andreadis, A. and Drager, U. C. (2000). A retinoic acid synthesizing enzyme in ventral retina and telencephalon of the embryonic mouse. Mech. Dev. 95, 283-289.
38. Lin, M., Zhang, M., Abraham, M., Smith, S. M. and Napoli, J. L. (2003). Mouse retinal dehydrogenase 4 (RALDH4), molecular cloning, cellular expression, and activity in 9-cis-retinoic acid biosynthesis in intact cells. J. Biol. Chem. 278, 9856-9861.
39. MacLean, G., Abu-Abed, S., Dolle, P., Tahayato, A., Chambon, P. and Petkovich, M. (2001). Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107, 195-201.
40. Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P. et al. (1995). The nuclear receptor superfamily: the second decade. Cell 83, 835-839.
41. Mann, F., Ray, S., Harris, W. and Holt, C. (2002). Topographic mapping in dorsoventral axis of the Xenopus retinotectal system depends on signaling through ephrin-B ligands. Neuron 35, 461-473.
42. Mark, M. and Chambon, P. (2003). Functions of RARs and RXRs in vivo: genetic dissection of the retinoid signaling pathway. Pure Appl. Chem. 75, 1709-1732.
43. Marsh-Armstrong, N., McCaffery, P., Gilbert, W., Dowling, J. E. and Drager, U. C. (1994). Retinoic acid is necessary for development of the ventral retina in zebrafish. Proc. Natl. Acad. Sci. USA 91, 7286-7290.
44. McCaffery, P., Tempst, P., Lara, G. and Drager, U. C. (1991). Aldehyde dehydrogenase is a positional marker in the retina. Development 112, 693-702.
45. McCaffery, P., Lee, M. O., Wagner, M. A., Sladek, N. E. and Drager, U. C. (1992). Asymmetrical retinoic acid synthesis in the dorsoventral axis of the retina. Development 115, 371-382.
46. McCaffery, P., Wagner, E., O'Neil, J., Petkovich, M. and Drager, U. C. (1999). Dorsal and ventral rentinoic territories defined by retinoic acid synthesis, break-down and nuclear receptor expression. Mech. Dev. 85, 203-214.
47. McLaughlin, T., Hindges, R. and O'Leary, D. D. (2003a). Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13, 57-69.
48. McLaughlin, T., Hindges, R., Yates, P. A. and O'Leary, D. D. (2003b). Bifunctional action of ephrin-B1 as a repellent and attractant to control bidirectional branch extension in dorsal-ventral retinotopic mapping. Development 130, 2407-2418.
49. Mey, J., McCaffery, P. and Drager, U. C. (1997). Retinoic acid synthesis in the developing chick retina. J. Neurosci. 17, 7441-7449.
50. Mey, J., McCaffery, P. and Klemeit, M. (2001). Sources and sink of retinoic acid in the embryonic chick retina: distribution of aldehyde dehydrogenase activities, CRABP-I, and sites of retinoic acid inactivation. Brain Res. Dev. Brain Res. 127, 135-148.
51. Mic, F. A., Molotkov, A., Fan, X., Cuenca, A. E. and Duester, G. (2000). RALDH3, a retinaldehyde dehydrogenase that generates retinoic acid, is expressed in the ventral retina, otic vesicle and olfactory pit during mouse development. Mech. Dev. 97, 227-230.
52. Morgan, B. A. and Fekete, D. M. (1996). Manipulating gene expression with replication-competent retroviruses. Methods Cell Biol. 51, 185-218.
53. Morrow, E. M., Belliveau, M. J. and Cepko, C. L. (1998). Two phases of rod photoreceptor differentiation during rat retinal development. J. Neurosci. 18, 3738-3748.
54. Mui, S. H., Hindges, R., O'Leary, D. D., Lemke, G. and Bertuzzi, S. (2002). The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129, 797-804.
55. Peters, M. A. and Cepko, C. L. (2002). The dorsal-ventral axis of the neural retina is divided into multiple domains of restricted gene expression which exhibit features of lineage compartments. Dev. Biol. 251, 59-73.
56. Petropoulos, C. J. and Hughes, S. H. (1991). Replication-competent retrovirus vectors for the transfer and expression of gene cassettes in avian cells. J. Virol. 65, 3728-3737.
57. Ray, W. J., Bain, G., Yao, M. and Gottlieb, D. I. (1997). CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. J. Biol. Chem. 272, 18702-18708.
58. Reijntjes, S., Gale, E. and Maden, M. (2003). Expression of the retinoic acid catabolising enzyme CYP26B1 in the chick embryo and its regulation by retinoic acid. Gene Expr. Patterns 3, 621-627.
59. Reijntjes, S., Gale, E. and Maden, M. (2004). Generating gradients of retinoic acid in the chick embryo: Cyp26C1 expression and a comparative analysis of the Cyp26 enzymes. Dev. Dyn. 230, 509-517.
60. Sakurai, T., Wong, E., Drescher, U., Tanaka, H. and Jay, D. G. (2002). Ephrin-A5 restricts topographically specific arborization in the chick retinotectal projection in vivo. Proc. Natl. Acad. Sci. USA 99, 10795-10800.
61. Sakuta, H., Suzuki, R., Takahashi, H., Kato, A., Shintani, T., Iemura, S., Yamamoto, T. S., Ueno, N. and Noda, M. (2001). Ventroptin: a BMP-4 antagonist expressed in a double-gradient pattern in the retina. Science 293, 111-115.
62. Schulte, D., Furukawa, T., Peters, M. A., Kozak, C. A. and Cepko, C. L. (1999). Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24, 541-553.
63. Simon, D. K. and O'Leary, D. D. (1992a). Development of topographic order in the mammalian retinocollicular projection. J. Neurosci. 12, 1212-1232.
64. Simon, D. K. and O'Leary, D. D. (1992b). Influence of position along the medial-lateral axis of the superior colliculus on the topographic targeting and survival of retinal axons. Brain Res. Dev. Brain Res. 69, 167-172.
65. Simon, D. K. and O'Leary, D. D. (1992c). Responses of retinal axons in vivo and in vitro to position-encoding molecules in the embryonic superior colliculus. Neuron 9, 977-989.
66. Sjoberg, M., Vennstrom, B. and Forrest, D. (1992). Thyroid hormone receptors in chick retinal development: differential expression of mRNAs for alpha and N-terminal variant beta receptors. Development 114, 39-47.
67. Sperry, R. W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50, 703-710.
68. Suzuki, R., Shintani, T., Sakuta, H., Kato, A., Ohkawara, T., Osumi, N. and Noda, M. (2000). Identification of RALDH-3, a novel retinaldehyde dehydrogenase, expressed in the ventral region of the retina. Mech. Dev. 98, 37-50.
69. Swindell, E. C., Thaller, C., Sockanathan, S., Petkovich, M., Jessell, T. M. and Eichele, G. (1999). Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev. Biol. 216, 282-296.
70. Tahayato, A., Dolle, P. and Petkovich, M. (2003). Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr. Patterns 3, 449-454.
71. Taimi, M., Helvig, C., Wisniewski, J., Ramshaw, H., White, J., Amad, M., Korczak, B. and Petkovich, M. (2004). A novel human cytochrome P450, CYP26C1, involved in metabolism of 9-cis and all-trans isomers of retinoic acid. J. Biol. Chem. 279, 77-85.
72. Umesono, K., Murakami, K. K., Thompson, C. C. and Evans, R. M. (1991). Direct repeats as selective response elements for the thyroid hormone, retinoic acid, and vitamin D3 receptors. Cell 65, 1255-1266.
73. Usala, S. J., Menke, J. B., Watson, T. L., Wondisford, F. E., Weintraub, B. D., Berard, J., Bradley, W. E., Ono, S., Mueller, O. T. and Bercu, B. B. (1991). A homozygous deletion in the c-erbA beta thyroid hormone receptor gene in a patient with generalized thyroid hormone resistance: isolation and characterization of the mutant receptor. Mol. Endocrinol. 5, 327-335.
74. Wagner, M., Han, B. and Jessell, T. M. (1992). Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116, 55-66.
75. White, J. A., Ramshaw, H., Taimi, M., Stangle, W., Zhang, A., Everingham, S., Creighton, S., Tam, S. P., Jones, G. and Petkovich, M. (2000). Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-trans-retinoic acid metabolism. Proc. Natl. Acad. Sci. USA 97, 6403-6408.
76. Wilkinson, D. G. (2001). Multiple roles of EPH receptors and ephrins in neural development. Nat. Rev. Neurosci. 2, 155-164.
77. Wilson, J. G., Roth, C. B. and Warkany, J. (1953). An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am. J. Anat. 92, 189-217.
78. Yates, P. A., Roskies, A. L., McLaughlin, T. and O'Leary, D. D. (2001). Topographic-specific axon branching controlled by ephrin-As is the critical event in retinotectal map development. J. Neurosci. 21, 8548-8563.
79. Yoshida, A., Rzhetsky, A., Hsu, L. C. and Chang, C. (1998). Human aldehyde dehydrogenase gene family. Eur. J. Biochem. 251, 549-557.
80. Zenke, M., Munoz, A., Sap, J., Vennstrom, B. and Beug, H. (1990). v-erbA oncogene activation entails the loss of hormone-dependent regulator activity of c-erbA. Cell 61, 1035-1049.
81. Zhao, D., McCaffery, P., Ivins, K. J., Neve, R. L., Hogan, P., Chin, W. W. and Drager, U. C. (1996). Molecular identification of a major retinoic-acid-synthesizing enzyme, a retinaldehyde-specific dehydrogenase. Eur. J. Biochem. 240, 15-22.