Functional dissection of the promoter of the interphotoreceptor retinoid-binding protein gene: The cone-rod-homeobox element is essential for photoreceptor-specific expression in vivo

Journal of Biochemistry

Volumn 125, Issue 6, 1999, Pages 1189-1199

  Fei, Yijian ^a   Matragoon, Suraporn ^a   Smith, Sylvia B ^a   Overbeek, Paul A ^b   Chen, Shiming ^c   Zack, Donald J ^d   Liou, Gregory I ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

CRXE; IRBP gene regulation; PCE; Photoreceptor specific

Indexed keywords

CHLORAMPHENICOL ACETYLTRANSFERASE; CYTOSINE; DEOXYRIBONUCLEASE I; GUANINE; HOMEODOMAIN PROTEIN; INTERPHOTORECEPTOR RETINOID BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA FOOTPRINTING; ENZYME ACTIVATION; ENZYME ACTIVITY; EXPRESSION VECTOR; GENE CONTROL; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HELA CELL; HOMEOBOX; HUMAN; HUMAN CELL; HYPERSENSITIVITY; IN VIVO STUDY; MOUSE; NONHUMAN; PHOTORECEPTOR; PROMOTER REGION; REPORTER GENE; RETINA CONE; RETINA ROD; RETINOBLASTOMA; SEQUENCE ANALYSIS; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

EID: 0032815363     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a022403     Document Type: Article

References (42)

1. Adler, R. and Hatlee, M. (1988) Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 243, 391-393
2. Cepko, C.L., Austin, C.P., Yang, S., Alexiades, M., and Ezzeddine, D. (1996) Cell fate determination in the vertebrate retina. Proc. Natl. Acad. Sci. USA 93, 589-595
3. Chen, S., Wang, Q.-L., Nie, Z., Sun, H., Lennon, G., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., and Zack, D.J. (1997) Crx, a novel otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19, 1017-1030
4. Furukawa, T., Morrow, E.M., and Cepko, C.L. (1997) Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 521-541
5. Mathers, P.H., Grinberg, A., Mahon, K.A., and Jamrich, M. (1997) The rx homeobox gene is essential for vertebrate eye development. Nature 387, 603-607
6. Freund, C.L., Gregory-Evans, C.Y., Furukawa, T., Papaioannou, M., Looser, J., Ploder, L., Bellingham, J., Ng, D., Herbrick, J.S., Duncan, A., Scherer, S.W., Tsui, L-C., Loutradis-Anagnostou, A., Jacobson, S.G., Cepko, C.L., Bhattacharya, S.S., and McInnes, R.R. (1997) Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 91, 543-553
7. Swain, P.K., Chen, S., Wang, Q-L., Affatigato, L.M., Coats, C.L., Brady, K.D., Fishman, G.A., Jacobson, S.G., Swaroop, A., Stone, E., Sieving, P.A., and Zack, D.J. (1997) Mutations in the cone-rod homebox gene are associated with the cone-rod dystrophy photoreceptor degeneration. Neuron 19, 1329-1336
8. Carter-Dawson, L., Alvarez, R.A., Fong, S.-L., Liou, G.I., Sperling, H.G., and Bridges, C.D.B. (1986) Rhodopsin, 11-cis vitamin A, and interstitial retinol-binding protein (IRBP) during retinal development in normal and rd mutant mice. Dev. Biol. 116, 431-438
9. Hauswirth, W.W., Langerijt, A.V.D., Timmers, A.M., Adamus, G., and Ulshafer, R.J. (1992) Early expression and localization of rhodopsin and IRBP in the developing fetal bovine retina. Exp. Eye Res. 54, 661-670
10. Timmers, A.M., Newton, R.B., and Hauswirth, W.W. (1993) Synthesis and stability of retinal photoreceptor mRNAs are coordinately regulated during bovine fetal development. Exp. Eye Res. 56, 257-265
11. Pepperberg, D.R., Okajima, T.-I.L., Wiggert, B., Ripps, H., Crouch, R.K., and Chader, G.J. (1993) IRBP - Molecular biology and physiological role in the visual cycle of rhodopsin. Mol. Neurobiol. 7, 61-84
12. Adler, A.J., Evans, C.D., and Stafford, W.F. (1985) Molecular properties of bovine interphotoreceptor retinoid-binding protein. J. Biol. Chem. 260, 4850-4855
13. Duffy, M., Sun, Y., Wiggert, B., Duncan, T., Chader, G.J., and Ripps, H. (1993) IRBP enhances rhodopsin regeneration in the experimentally detached retina. Exp. Eye Res. 57, 771-782
14. Liou, G.I., Bridges, C.D.B., Fong, S.-L., Alvarez, R.A., and Gonzalez-Fernandez, F. (1982) Vitamin A transport between retina and pigment epithelium-An interstitial protein carrying endogenous retinol (IRBP). Vis. Res. 22, 1457-1467
15. Okajima, T.-I.L., Pepperberg, D.R., Ripps, H., Wiggert, B., and Chader, G.J. (1990) Interphotoreceptor retinoid-binding protein promotes rhodopsin regeneration in toad photoreceptors. Proc. Natl. Acad. Sci. USA 87, 6907-6911
16. Saari, J.C., Teller, D.C., Crabb, J.W., and Bredberg, L. (1985) Properties of an interphotoreceptor retinoid-binding protein from bovine retina. J. Biol. Chem. 260, 195-201
17. Ho, M.T.P., Massey, J.B., Pownall, H.J., Anderson, R.E., and Hollyfield, J.G. (1989) Mechanisms of vitamin A movement between rod outer segments, IRBP, and liposomes. J. Biol. Chem. 264, 928-935
18. Liou, G.I., Fei, Y., Peachey, N.S., Matragoon, S., Wei, S., Blaner, W.S., Wang, Y., Liu, C., Gottesman, M.E., and Ripps, H. (1998) Early onset photoreceptor abnormalities induced by targeted disruption of the interphotoreceptor retinoid-binding protein gene. J. Neurosci. 18, 4511-4520
19. Liou, G.I., Matragoon, S., Yang, J., Geng, L., Overbeek, P.A., and Ma, D.-P. (1991) Retina-specific expression from the IRBP promoter in transgenic mice is conferred by 212 bp of the 5′-flanking region. Biochem. Biophys. Res. Commun. 181, 159-165
20. Bobola, N., Hirsch, E., Albini, A., Altruda, F., Noonan, D., and Ravazzolo, R. (1995) A single cis-acting element in a short promoter segment of the gene encoding the interphotoreceptor retinoid-binding protein confers tissue-specific expression. J. Biol. Chem. 270, 1289-1294
21. Kikuchi, T., Raju, K., Breitman, M.L., and Shinohara, T. (1993) The proximal promoter of the mouse arrestin gene directs gene expression in photoreceptor cells and contains an evolutionarily conserved retinal factor-binding site. Mol. Cell. Biol. 13, 4400-4408
22. Morabito, M.A., Yu, X., and Bamstable, C.J. (1991) Characterization of developmentally regulated and retina-specific nuclear protein binding to a site in the upstream region of the rat opsin gene. J. Biol. Chem. 266, 9667-9672
23. Fong, S.-L., Morris, T.A., Lee, C.-H., Donoso, L.A., and Fong, W.-B. (1993) Transfection of retinoblastoma cells: Localization of cis-acting elements for human IRBP gene in Methods in Neurosciences (Hargrave, P., ed.) Vol. 15, pp. 322-329, Academic Press, Orlando, FL
24. Liou, G.I., Geng, L., Al-Ubaidi, M.R., Matragoon, S., Hanten, G., Baehr, W., and Overbeek, P.A. (1990)Tissue-specific expression in transgenic mice directed by the 5′-flanking sequences of the human gene encoding interphotoreceptor retinoid-binding protein. J. Biol. Chem. 265, 8373-8376
25. Fei, Y., Matragoon, S., and Liou, G.I. (1995) Simple and efficient method for the preparation of nuclear extracts. BioTechniques 18, 984-986
26. Higuchi, R.B. (1990) PCR Protocols: A Guide to Methods and Applications (Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J., eds.) pp. 177-183, Academic Press, San Diego, CA
27. Liou, G.I., Wang, M., and Matragoon, S. (1994) Timing of interphotoreceptor retinoid-binding protein (IRBP) gene expression and hypomethylation in developing mouse retina. Dev. Biol. 161, 345-356
28. Baehr, W., Falk, J.D., Bugra, K., Triantafyllos, J.T., and McGinnis, J.F. (1988) Isolation and analysis of the mouse opsin gene. FEBS Lett. 238, 253-256
29. Zack, D.J., Bennett, J., Wang, Y., Davenport, C., Klaunberg, B., Gearhart, J., and Nathans, J. (1991) Unsual topography of bovine rhodopsin promoter-lacZ fusion gene expression in transgenic mouse retinas. Neuron 6, 187-199
30. Liou, G.I., Matragoon, S., Overbeek, P.A., and Fei, Y. (1994) Identification of a retina-specific footprint within the retina-specific regulatory region of the human interphotoreceptor retinoid-binding protein gene. Biochem. Biophys. Res. Commun. 203, 1875-1881
31. Fortini, M.E. and Rubin, G.M. (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster. Genes Dev. 4, 444-463
32. Droba, M. (1988) Properties of acid beta-galactosidase from fowl spermatozoa. Br. Poult. Sci. 29, 555-562
33. Fassina, G., Paglialunga, G., Noonan, D.M., Chader, G.J., and Albini, A. (1993) Modulation of Y-79 retinoblastoma cell differentiation and IRBP expression by dibutyryl cyclic AMP and laminin. Int. J. Oncol. 2, 745-751
34. Boatright, J.H., Borst, D.E., Peoples, J.W., Bruno, J., Edwards, C.L., Si, J.-S., and Nickerson, J.M. (1997) A major cis activator of the IRBP gene contains CRX-binding and Ret-1/PCE-1 elements. Mol. Vis. 3, 15-28
35. Catron, K.M., Iler, N., and Abate, C. (1993) Nucleotides flanking a conserved TAAT core dictate the DNA binding specificity of three murine homeodomain proteins. Mol. Cell. Biol. 13, 2354-2365
36. Furukawa, T., Kozak, C.A., and Cepko, C.L. (1997) Rax, a novel paired-type homeobox gene, shows expression in the anterior neural fold and developing retina. Proc. Natl. Acad. Sci. USA 94, 3088-3093
37. Martinez, J.A. and Barnstable, C.J. (1998) Erx, a novel retina-specific homeodomain transcription factor, can interact with Ret 1/PCE 1 sites. Biochem. Biophys. Res. Commun. 250, 175-180
38. Hanes, S.D. and Brent, R. (1991) A genetic model for interaction of the homeodomain recognition helix with DNA. Science 251, 426-430
39. Takahashi, K., Vigneron, M., Matthes, H., Wildeman, A., Zenke, M., and Chambon, P. (1986) Requirement of stereospecific alignments for initiation from the simian virus 40 early promoter. Nature 319, 121-126
40. Chen, S. and Zack, D.J. (1996) Ret 4, a positive acting rhodopsin regulatory element identified using a bovine retina in vitro transcription system. J. Biol. Chem. 271, 28549-28557
41. DiPolo, A., Rickman, C.B., and Farber, D.B. (1996) Isolation and initial characterization of the 5′ flanking region of the human and murine cyclic guanosine monophosphate-phosphodiesterase β-subunit genes. Invest. Ophthal. Vis. Sci. 37, 551-560
42. Ahmad, I., Yu, X., and Barnstable, C.J. (1994) A cis-acting element, Tα-1, in the upstream region of rod α-transducin gene that binds a developmentally regulated retina-specific nuclear factor. J. Neurochem. 62, 396-399