Vax2 regulates retinoic acid distribution and cone opsin expression in the vertebrate eye

Development

Volumn 138, Issue 2, 2011, Pages 261-271

  Alfano, Giovanna ^a,e   Conte, Ivan ^a,b   Caramico, Tiziana ^a   Avellino, Raffaella ^a   Arnò, Benedetta ^a   Pizzo, Maria Teresa ^a   Tanimoto, Naoyuki ^c   Beck, Susanne C ^c   Huber, Gesine ^c   Dollé, Pascal ^d   Seeliger, Mathias W ^c   Banfi, Sandro ^a  

^a TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^b INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cone opsins; Mouse; Oryzias latipes (medaka); Retinoic acid; Vax2

Indexed keywords

CYTOCHROME P450 26A1; CYTOCHROME P450 26C1; DRUG METABOLIZING ENZYME; OPSIN; PROTEIN RALDH3; RETINOIC ACID; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAPHY; EYE DEVELOPMENT; GENE EXPRESSION; GENE INACTIVATION; HOMEOBOX; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; KNOCKOUT MOUSE; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; OPHTHALMOSCOPY; OPTICAL COHERENCE TOMOGRAPHY; ORYZIAS; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA CONE; VAX2 GENE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CYTOCHROME P-450 ENZYME SYSTEM; EYE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; OPSINS; ORYZIAS; PREGNANCY; RETINAL CONE PHOTORECEPTOR CELLS; ROD OPSINS; TRETINOIN;

MAMMALIA; MUS; ORYZIAS LATIPES; ORYZIINAE; VERTEBRATA;

EID: 78751506878     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.051037     Document Type: Article

References (69)

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. Applebury, M. L., Antoch, M. P., Baxter, L. C., Chun, L. L., Falk, J. D., Farhangfar, F., Kage, K., Krzystolik, M. G., Lyass, L. A. and Robbins, J. T. (2000). The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27, 513-523.
3. Applebury, M. L., Farhangfar, F., Glosmann, M., Hashimoto, K., Kage, K., Robbins, J. T., Shibusawa, N., Wondisford, F. E. and Zhang, H. (2007). Transient expression of thyroid hormone nuclear receptor TRbeta2 sets S opsin patterning during cone photoreceptor genesis. Dev. Dyn. 236, 1203-1212.
4. Barbieri, A. M., Lupo, G., Bulfone, A., Andreazzoli, M., Mariani, M., Fougerousse, F., Consalez, G. G., Borsani, G., Beckmann, J. S., Barsacchi, G. et al. (1999). A homeobox gene, vax2, controls the patterning of the eye dorsoventral axis. Proc. Natl. Acad. Sci. USA 96, 10729-10734.
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. Bulfone, A., Menguzzato, E., Broccoli, V., Marchitiello, A., Gattuso, C., Mariani, M., Consalez, G. G., Martinez, S., Ballabio, A. and Banfi, S. (2000). Barhl1, a gene belonging to a new subfamily of mammalian homeobox genes, is expressed in migrating neurons of the CNS. Hum. Mol. Genet. 9, 1443-1452.
7. Canestro, C., Catchen, J. M., Rodriguez-Mari, A., Yokoi, H. and Postlethwait, J. H. (2009). Consequences of lineage-specific gene loss on functional evolution of surviving paralogs: ALDH1A and retinoic acid signaling in vertebrate genomes. PLoS Genet. 5, e1000496.
8. Cepko, C. L., Austin, C. P., Yang, X., Alexiades, M. and Ezzeddine, D. (1996). Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589-595.
9. Conte, I. and Bovolenta, P. (2007). Comprehensive characterization of the cisregulatory code responsible for the spatio-temporal expression of olSix3.2 in the developing medaka forebrain. Genome Biol. 8, R137.
10. Conte, I., Lestingi, M., den Hollander, A., Miano, M. G., Alfano, G., Circolo, D., Pugliese, M., Testa, F., Simonelli, F., Rinaldi, E. et al. (2002). Characterization of MPP4, a gene highly expressed in photoreceptor cells, and mutation analysis in retinitis pigmentosa. Gene 297, 33-38.
11. Conte, I., Marco-Ferreres, R., Beccari, L., Cisneros, E., Ruiz, J. M., Tabanera, N. and Bovolenta, P. (2010). Proper differentiation of photoreceptors and amacrine cells depends on a regulatory loop between NeuroD and Six6. Development 137, 2307-2317.
12. Corbo, J. C., Myers, C. A., Lawrence, K. A., Jadhav, A. P. and Cepko, C. L. (2007). A typology of photoreceptor gene expression patterns in the mouse. Proc. Natl. Acad. Sci. USA 104, 12069-12074.
13. Dalton, D., Chadwick, R. and McGinnis, W. (1989). Expression and embryonic function of empty spiracles: a Drosophila homeo box gene with two patterning functions on the anterior-posterior axis of the embryo. Genes Dev. 3, 1940-1956.
14. Deeb, S. S., Liu, Y. and Hayashi, T. (2006). Mutually exclusive expression of the L and M pigment genes in the human retinoblastoma cell line WERI: resetting by cell division. Vis. Neurosci. 23, 371-378.
15. Duester, G. (2008). Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931.
16. Fei, Y. (2003). Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Mol. Vis. 9, 31-42.
17. Fischer, M. D., Huber, G., Beck, S. C., Tanimoto, N., Muehlfriedel, R., Fahl, E., Grimm, C., Wenzel, A., Reme, C. E., van de Pavert, S. A. et al. (2009). Noninvasive, in vivo assessment of mouse retinal structure using optical coherence tomography. PLoS ONE 4, e7507.
18. Fujieda, H., Bremner, R., Mears, A. J. and Sasaki, H. (2009). Retinoic acid receptor-related orphan receptor alpha regulates a subset of cone genes during mouse retinal development. J. Neurochem. 108, 91-101.
19. 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.
20. Gennarino, V. A., Sardiello, M., Avellino, R., Meola, N., Maselli, V., Anand, S., Cutillo, L., Ballabio, A. and Banfi, S. (2009). MicroRNA target prediction by expression analysis of host genes. Genome Res. 19, 481-490.
21. Golz, S., Muhleisen, T., Schulte, D. and Mey, J. (2008). Regulation of RALDH-1, RALDH-3 and CYP26A1 by transcription factors cVax/Vax2 and Tbx5 in the embryonic chick retina. Int. J. Dev. Neurosci. 26, 435-445.
22. Hallonet, M., Hollemann, T., Pieler, T. and Gruss, P. (1999). Vax1, a novel homeobox-containing gene, directs development of the basal forebrain and visual system. Genes Dev. 13, 3106-3114.
23. Huber, G., Beck, S. C., Grimm, C., Sahaboglu-Tekgoz, A., Paquet-Durand, F., Wenzel, A., Humphries, P., Redmond, T. M., Seeliger, M. W. and Fischer, M. D. (2009). Spectral domain optical coherence tomography in mouse models of retinal degeneration. Invest. Ophthalmol. Vis. Sci. 50, 5888-5895.
24. 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.
25. Hyatt, G. A., Schmitt, E. A., Marsh-Armstrong, N., McCaffery, P., Drager, U. C. and Dowling, J. E. (1996). Retinoic acid establishes ventral retinal characteristics. Development 122, 195-204.
26. Jean, D., Ewan, K. and Gruss, P. (1998). Molecular regulators involved in vertebrate eye development. Mech. Dev. 76, 3-18.
27. 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.
28. Li, Q., Timmers, A. M., Guy, J., Pang, J. and Hauswirth, W. W. (2008). Conespecific expression using a human red opsin promoter in recombinant AAV. Vision Res. 48, 332-338.
29. Liu, H., Etter, P., Hayes, S., Jones, I., Nelson, B., Hartman, B., Forrest, D. and Reh, T. A. (2008). NeuroD1 regulates expression of thyroid hormone receptor 2 and cone opsins in the developing mouse retina. J. Neurosci. 28, 749-756.
30. Loudig, O., Maclean, G. A., Dore, N. L., Luu, L. and Petkovich, M. (2005). Transcriptional co-operativity between distant retinoic acid response elements in regulation of Cyp26A1 inducibility. Biochem. J. 392, 241-248.
31. Luo, T., Sakai, Y., Wagner, E. and Drager, U. C. (2006). Retinoids, eye development, and maturation of visual function. J. Neurobiol. 66, 677-686.
32. 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.
33. 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.
34. Matsumoto, Y., Fukamachi, S., Mitani, H. and Kawamura, S. (2006). Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371, 268-278.
35. Matt, N., Dupe, V., Garnier, J. M., Dennefeld, C., Chambon, P., Mark, M. and Ghyselinck, N. B. (2005). Retinoic acid-dependent eye morphogenesis is orchestrated by neural crest cells. Development 132, 4789-4800.
36. 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.
37. McCaffery, P., Wagner, E., O'Neil, J., Petkovich, M. and Drager, U. C. (1999). Dorsal and ventral rentinoic territories defined by retinoic acid synthesis, breakdown and nuclear receptor expression. Mech. Dev. 85, 203-214.
38. Mey, J., McCaffery, P. and Drager, U. C. (1997). Retinoic acid synthesis in the developing chick retina. J. Neurosci. 17, 7441-7449.
39. 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.
40. Molotkov, A., Molotkova, N. and Duester, G. (2006). Retinoic acid guides eye morphogenetic movements via paracrine signaling but is unnecessary for retinal dorsoventral patterning. Development 133, 1901-1910.
41. Muhleisen, T. W., Agoston, Z. and Schulte, D. (2006). Retroviral misexpression of cVax disturbs retinal ganglion cell axon fasciculation and intraretinal pathfinding in vivo and guidance of nasal ganglion cell axons in vivo. Dev. Biol. 297, 59-73.
42. 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.
43. Mui, S. H., Kim, J. W., Lemke, G. and Bertuzzi, S. (2005). Vax genes ventralize the embryonic eye. Genes Dev. 19, 1249-1259.
44. Ng, L., Hurley, J. B., Dierks, B., Srinivas, M., Salto, C., Vennstrom, B., Reh, T. A. and Forrest, D. (2001). A thyroid hormone receptor that is required for the development of green cone photoreceptors. Nat. Genet. 27, 94-98.
45. Niederreither, K., Fraulob, V., Garnier, J. M., Chambon, P. and Dolle, P. (2002). Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech. Dev. 110, 165-171.
46. Oh, E. C., Khan, N., Novelli, E., Khanna, H., Strettoi, E. and Swaroop, A. (2007). Transformation of cone precursors to functional rod photoreceptors by bZIP transcription factor NRL. Proc. Natl. Acad. Sci. USA 104, 1679-1684.
47. Ohsaki, K., Morimitsu, T., Ishida, Y., Kominami, R. and Takahashi, N. (1999). Expression of the Vax family homeobox genes suggests multiple roles in eye development. Genes Cells 4, 267-276.
48. Osakada, F., Ikeda, H., Mandai, M., Wataya, T., Watanabe, K., Yoshimura, N., Akaike, A., Sasai, Y. and Takahashi, M. (2008). Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat. Biotechnol. 26, 215-224.
49. Prabhudesai, S. N., Cameron, D. A. and Stenkamp, D. L. (2005). Targeted effects of retinoic acid signaling upon photoreceptor development in zebrafish. Dev. Biol. 287, 157-167.
50. Raine, J. C. and Hawryshyn, C. W. (2009). Changes in thyroid hormone reception precede SWS1 opsin downregulation in trout retina. J. Exp. Biol. 212, 2781-2788.
51. 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.
52. 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.
53. Roberts, M. R., Hendrickson, A., McGuire, C. R. and Reh, T. A. (2005). Retinoid X receptor (gamma) is necessary to establish the S-opsin gradient in cone photoreceptors of the developing mouse retina. Invest. Ophthalmol. Vis. Sci. 46, 2897-2904.
54. Roberts, M. R., Srinivas, M., Forrest, D., Morreale de Escobar, G. and Reh, T. A. (2006). Making the gradient: thyroid hormone regulates cone opsin expression in the developing mouse retina. Proc. Natl. Acad. Sci. USA 103, 6218-6223.
55. Rossant, J., Zirngibl, R., Cado, D., Shago, M. and Giguere, V. (1991). Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, 1333-1344.
56. Sakai, Y., Meno, C., Fujii, H., Nishino, J., Shiratori, H., Saijoh, Y., Rossant, J. and Hamada, H. (2001). The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 15, 213-225.
57. Sakai, Y., Luo, T., McCaffery, P., Hamada, H. and Drager, U. C. (2004). CYP26A1 and CYP26C1 cooperate in degrading retinoic acid within the equatorial retina during later eye development. Dev. Biol. 276, 143-157.
58. Saszik, S. M., Robson, J. G. and Frishman, L. J. (2002). The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J. Physiol. 543, 899-916.
59. 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.
60. Schulte, D., Peters, M. A., Sen, J. and Cepko, C. L. (2005). The rod photoreceptor pattern is set at the optic vesicle stage and requires spatially restricted cVax expression. J. Neurosci. 25, 2823-2831.
61. Seeliger, M. W., Grimm, C., Stahlberg, F., Friedburg, C., Jaissle, G., Zrenner, E., Guo, H., Reme, C. E., Humphries, P., Hofmann, F. et al. (2001). New views on RPE65 deficiency: the rod system is the source of vision in a mouse model of Leber congenital amaurosis. Nat. Genet. 29, 70-74.
62. Seeliger, M. W., Beck, S. C., Pereyra-Munoz, N., Dangel, S., Tsai, J. Y., Luhmann, U. F., van de Pavert, S. A., Wijnholds, J., Samardzija, M., Wenzel, A. et al. (2005). In vivo confocal imaging of the retina in animal models using scanning laser ophthalmoscopy. Vision Res. 45, 3512-3519.
63. Sen, J., Harpavat, S., Peters, M. A. and Cepko, C. L. (2005). Retinoic acid regulates the expression of dorsoventral topographic guidance molecules in the chick retina. Development 132, 5147-5159.
64. Simeone, A., Gulisano, M., Acampora, D., Stornaiuolo, A., Rambaldi, M. and Boncinelli, E. (1992). Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J. 11, 2541-2550.
65. Srinivas, M., Ng, L., Liu, H., Jia, L. and Forrest, D. (2006). Activation of the blue opsin gene in cone photoreceptor development by retinoid-related orphan receptor beta. Mol. Endocrinol. 20, 1728-1741.
66. 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.
67. 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.
68. Veldhoen, K., Allison, W. T., Veldhoen, N., Anholt, B. R., Helbing, C. C. and Hawryshyn, C. W. (2006). Spatio-temporal characterization of retinal opsin gene expression during thyroid hormone-induced and natural development of rainbow trout. Vis. Neurosci. 23, 169-179.
69. Wang, T. and Montell, C. (2005). Rhodopsin formation in Drosophila is dependent on the PINTA retinoid-binding protein. J. Neurosci. 25, 5187-5194.