Interphotoreceptor retinoid-binding protein (IRBP): Expression in the adult and developing Xenopus retina

Journal of Comparative Neurology

Volumn 367, Issue 3, 1996, Pages 329-341

  Hessler, Richard B ^a,c   Baer, Claxton A ^a   Bukelman, Amir ^a,b   Kittredge, Karen L ^a   Gonzalez Fernandez, Federico ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b KAPLAN HOSPITAL   (Israel)

^c GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

extracellular matrix; interphotoreceptor matrix; retinal development; Xenopus laevis

Indexed keywords

RETINOID BINDING PROTEIN;

ANIMAL TISSUE; ARTICLE; EXTRACELLULAR MATRIX; EYE DEVELOPMENT; NONHUMAN; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; XENOPUS LAEVIS;

ANIMALS; EYE PROTEINS; RETINA; RETINOL-BINDING PROTEINS; RNA, MESSENGER; XENOPUS LAEVIS;

EID: 0029931965     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960408)367:3<329::AID-CNE1>3.0.CO;2-7     Document Type: Article

References (74)

1. Adler, A., and M. Martin (1982) Retinol-binding proteins in the bovine interphotoreceptor matrix. Biochem. Biophys. Res. Commun. 108:1601-1608.
2. Adler, A., and S.A. Spencer (1991) Effect of light on endogenous ligands carried by interphotoreceptor retinoid-binding protein. Exp. Eye Res. 53:337-347.
3. Azuma, M., T. Seki, and S. Fujishita (1990) Changes of egg retinoids during the development of Xenopus laevis. Vis. Res. 30.1395-1400
4. Baer, C. A., K.L. Kittredge, A.L. Klinger, M. Briercheck, M.S. Braiman, and F. Gonzalez-Fernandez (1994) Expression and characterization of the fourth repeat of Xenopus interphotoreceptor retinoid-binding protein in E. coli. Curr. Eye Res. 13:391-400
5. Bazan, N G , T.S. Reddy, T.M. Redmond, B Wiggert, and G.J. Chader (1985) Endogenous fatty acids are convalently and noncovalently bound to interphotoreceptor retinoid-binding protein in the monkey retina. J. Biol. Chem. 260:13677-13680.
6. Borst, D.E , and J.M. Nickerson (1987) The isolation of a gene encoding interphotoreceptor retinoid-binding protein (IRBP). Exp. Eye Res. 47: 825-838.
7. Bridges, C.D.B , G.I. Liou, R.A. Alvarez, R A. Landers, A.M. Landry, and S.-L. Fong (1986) Distribution of interstitial retinol-binding protein (IRBP) in the vertebrates. J Exp. Zool. 239:335-346.
8. Bukelman, A., R.W. Hessler, and F. Gonzalez-Fernandez (1993) Synthesis and secretion of IRBP by the goldfish and Xenopus retina. Invest. Ophthalmol. Vis. Sci. 34(Suppl.):1198.
9. Bunt-Milam, A.H., J C. Saari, and D.L. Bredberg (1985) Characterization of the interstitial space - Immunohistochemical and biochemical studies. In C.D.B. Bridges and A.J. Adler (eds): The Interphotreceptor Matrix in Health and Disease. New York: Alan R. Liss, pp 151-170.
10. Carlson, A., and D. Bok (1992) Promotion of the release of 11-cis retinal from cultured retinal pigment epithelium by interphotoreceptor retinoid-binding protein Biochem. 31:9056-9062.
11. Carter-Dawson, L., and M. Burroughs (1992) Interphotoreceptor retinoid-binding protein in the golgi apparatus of monkey foveal cones Invest. Ophthalmol Vis Sci. 33:1589-1594
12. Carter-Dawson, L., R.A. Alvarez, S-L. Fong, H.G. Sperling, and C.D.B. Bridges (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.
13. Chen, Y., and N. Noy (1994) Retinoid specificity of interphotoreceptor retinoid-binding protein. Biochem. 33:10658-10665.
14. Chen, Y., J C. Saari, and N. Noy (1993) Interactions of all-trons retinol and long-chain fatty acids with interphotoreceptor retinoid-binding protein. Biochemistry 32 11311-11318.
15. Chomczynski, P., and N. Sacchi (1987) A rapid method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem 162 156-159.
16. Crouch, R.K., S. Hazard, T. Lind, B. Wiggert, G. Chader, and D.W. Corson (1992) Interphotoreceptor retinoid-binding protein and α-tocopherol preserve the isomeric and oxidation state of retinol. Photochem. Photobiol. 56:251-255.
17. De Leeuw, A.M., V.P Gaur, J C Saari, A.H. Milam (1990) Immunolocalization of cellular retinol-, retinaldehyde- and retinoic acid-binding proteins in rat retina during pre- and postnatal development. J Neurocytol. 19:253-264
18. DesJardin, L.E.. A.M. Timmers, W.W Hauswirth (1993) Transcription of photoreceptor genes during fetal retinal development. Evidence for positive and negative regulation. J. Biol. Chem 268:6953-6960
19. Edwards, R.B., and A J. Adler (1992) Comparison of retinol and retinal as substrates for retinoic acid synthesis by cultured rabbit Müller cells [Abstract]. Invest. Ophthalmol. Vis. Sci 33.695.
20. Edwards, R.B., and A.J. Adler (1994) Exchange of retinol between IRBP and CEBP. Exp. Eye Res. 59:161-170.
21. Eisenfeld, A.J., A.H. Bunt-Milan, and J.C. Saari (1985) Immunocytochemical localization of interphotoreceptor retinoid-binding protein in developing normal and RCS rat retinas Invest Ophthal. Vis. Sci. 26:775-778.
22. Feeney, L. (1973) The interphotoreceptor space I. Postnatal ontogeny in mice and rats. Dev. Biol. 32:101-114.
23. Flannery, J.B., W. O'Day, B.A. Pfeffer, J. Horwitz, and D. Bok (1990) Uptake, processing and release of retinoids by cultured human retinal pigment epithelium. Exp. Eye Res 51:717-728.
24. Gonzalez-Fernandez, F., and J.I. Healy (1990) Early expression of the gene for interstitial retinol-binding protein during photoreceptor differentiation suggests a critical role of the interphotoreceptor matrix during retinal development. J. Cell Biol. 111:2775-2784.
25. Gonzalez-Fernandez, F., and K.L. Kittredge (1992) Getting into the embryonic subretinal space. Invest. Ophthalmol. Vis. Sci. 33(Suppl ):816
26. Gonzalez-Fernandez, F., R.A. Landers, PA. Glazebrook, S.-L. Fong, G.I. Liou, D.M.K. Lam, and C.D.B. Bridges (1984) An extracellular retinol-binding glycoprotein in the eyes of mutant rats with retinal dystrophy: Development, localization and biosynthesis. J. Cell Biol. 99:2092-2098.
27. Gonzalez-Fernandez, F., R.A. Landers, S.-L. Fong, G.I. Liou, and C.D.B. Bridges (1985) IRBP in normal and dystrophic rats. In C.D.B. Bridges and A.J. Adler (eds): The Interphotoreceptor Matrix in Health and Disease. New York: Alan R. Liss, pp. 213-229.
28. Gonzalez-Fernandez, F., B.M.S. Lopes, J.M. Garcia-Fernandez, R.G. Foster, W.J. DeGrip, S. Rosemberg, S.A. Newman, and S.R. VandenBerg (1992) Expression of developmentally defined retinal phenotypes in the histogenesis of retinoblastomas. Am. J. Pathol. 141:363-375.
29. Gonzalez-Fernandez, F., K.L. Kittredge, M.E. Rayborn, J.G. Hollyfield, R.A. Landers, M. Saha, and R.E. Grainger (1993a) Interphotoreceptor retinoid-binding protein (IRBP), a major 124 kDa glycoprotein in the interphotoreceptor matrix of Xenopus laevis: characterization, molecular cloning and biosynthesis. J. Cell Sci. 105:7-21.
30. Gonzalez-Fernandez, F., E.E. Van Niel, C. Edmonds, H. Beaver, J M. Nickerson, J.M Garcia-Fernandez, P. Campochiaro, and R G. Foster (1993b) Differential expression of Interphotoreceptor retinoid-binding protein, opsin, cellular retinaldehyde-binding protein, and basic fibroblast growth factor. Exp. Eye Res. 56:411-427.
31. Hageman, G.S., M.A. Kirchoff-Rempe, G.P. Lewis, S.I. Fisher, D.H. Anderson (1991) Sequestration of basic fibroblast growth factor in the primate retinal interphotoreceptor matrix. Proc. Natl. Acad. Sci. U.S A. 88:6707-6710.
32. Harland, R.M. (1991) In situ hybridization: An improved whole-mount method for Xenopus embryos. In B.K. Kay and H.B. Peng (eds): Methods in Cell Biology, vol. 36. New York. Academic Press, pp. 685-695.
33. Hauswirth, W.W., A.V.D. Langerrjt, A.M. Timmers, G. Adamus, and R.J. Ulshafer (1992) Early expression and localization of rhodopsin and interphotoreceptor retinoid-binding protein (IRBP) in the developing fetal bovine retina. Exp. Eye Res. 54:661-670.
34. Henry, J.J., and R.M Grainger (1987) Inductive interactions in the spatial and temporal restriction of lens-forming potential in embryonic ectoderm of Xenopus laevis. Dev. Biol. 124:200-214.
35. Ho, M.T., J.B. Massey, H.J Pownall, R.E. Anderson, and J.G Hollyfield (1989) Mechanism of vitamin A movement between rod outer segments, interphotoreceptor retinol-binding protein, and liposomes. J Biol. Chem. 564:928-935.
36. Hollyfield, J.G., and P. Witkovsky, (1974) Pigmented retinal epithelium involvement in photoreceptor development and function J Exp. Zool. 189:357-377.
37. Hollyfield, J.G., S.J. Fhesler, M.E. Rayborn, S.-L. Fong, R.A. Landers, and C.D.B. Bridges (1985) Synthesis and secretion of interstitial retinol-binding protein by the human retina. Invest Ophthalmol. Vis. Sci. 26:58-67.
38. Holt, C.D., T.W. Bertsch, and H.M Elhs (1988) Cellular determination in the Xenopus retina is independent of lineage and birth date. Neuron 1:15-26.
39. Hunter, D.D., M.D Murphy, C V. Olsson, and W J. Brunken (1992) S-laminin expression in adult and developing retinae: A potential cue for photoreceptor morphogenesis. Neuron 8:399-413.
40. Johnson, A.T., F.L. Kretzer, H.M. Hittner, P.A. Glazebrook, C.D.B. Bridges, and D.M.K. Lam (1985). Development of the subretinal space in the preterin human eye: Ultrastructural and immunocytochemical studies. J. Comp Neurol. 233.497-505.
41. Jones, G.J , R.K. Crouch, B. Wiggert, M.C. Cornwall, and G.J. Chader (1989) Retinoid requirements for recovery of sensitivity after visual-pigment bleaching in isolated photorecpeotors. Proc. Natl. Acad. Sci. USA 86:9606-9610.
42. Kinney, M.S., and S.K. Fisher (1978) The photoreceptors and pigment epithelium of the larval Xenopus retina. Morphogenesis and outer segment renewal. Proc. R. Soc. Loud. B 201:149-167.
43. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
44. Lai, Y L., B. Wiggert, Y.P. Liu, and G J. Chader (1982). Interphotoreceptor retinol-binding proteins: Possible transport vehicles between compartments of the retina. Nature 298:848-849.
45. Lin, Z.S., S -L Fong, and C D.B. Bridges (1989) Retinoids bound to intersitial retinol-binding portein during light and dark-adaptation. Vis. Res. 29:1699-1709.
46. Liou, G.I., C.D.B. Bridges, R.A. Alvarez, and F. Gonzalez-Fernandez (1982) Vitamin A transport between retina and pigment epithelium - An interstitial protein carrying endogenous retinol (interstitial retinol-binding protein). Vis. Res. 22:457-1467.
47. Liou, G.I., M. Wang, and S. Matragoon (1994) Timing of interphotoreceptor retinoid-binding protein (IRBP) gene expression and hypomethylation in developing mouse retina. Dev. Biol. 161:345-356.
48. McCaffery, P., P. Tempst, G. Lara, and U.C. Drager (1991) Aldehyde dehydrogenase is a positional marker in the retina. Development 112:693-702.
49. Nieuwkoop, P.D., and J. Faber (1956) Normal Table of Xenopus laevis (Daudin). Amsterdam: North Holland.
50. Okajima, T -I.L , D.R. Pepperberg, R Harris, B. Wiggert, and G.J. Chader (1989) Interphotoreceptor retinoid-binding protein: Role in the delievery of retinol to the pigment epithelium. Exp. Eye Res. 49:629-644.
51. Okajima, T.-I.L., D.R. Pepperberg, R. Harris, B. Wiggert, and G.J. Chader (1990) Interphotoreceoptor retinoid-binding protein promotes rhodopsin regeneration in toad photoreceptors. Proc. Natl. Acad. Sci USA 87:6907-6911.
52. Okajima, T.-I L., B. Wiggert, G.J. Chader. and D.R. Pepperberg (1994) Retinoid processing in retinal pigment epithelium of toad (Bufo marinus). J. Biol. Chem. 269:21983-21989.
53. Payman, R., F. Gonzalez-Fernandez (1995) Turnover of IRBP in the Xenopus interphotoreceptor matrix Invest. Ophthal. Vis. Sci. 26(suppl.):25.
54. Pepperberg, D.R., T -L. Okajima, B. Wiggert, H. Ripps, R K. Crouch, and G.J. Chader (1993) Interphotoreceptor retinoid-binding protein (IRBP): Molecular biology and physiological role in the visual cycle of rhodopsin. Molec. Neurobiol. 7:61-85.
55. Perlman, J.I., B.R. Nodes, and D.R. Pepperberg (1982) Utilization of retinoids in the bullfrog retina. J. Gen. Physiol. 80:885-913
56. Porrello, K , S.P Bhat, and D. Bok (1991) Detection of interphotoreceptor retinoid-binding portein (IRBP) mRNA in human and cone-dominant squirrel retinas by in situ hybridization. J. Histochem. Cyotochem 39:171-176.
57. Rodrigues, M.M., J. Hackett, R. Gaskins, B. Wiggert, L. Lee, M. Redmond, and G.J Chader (1986) Interphotoreceptor retinoid-binding protein in retinal rod cells and pineal gland. Invest. Ophthal. Vis. Sci. 27:844-850.
58. Rugh, R. (1962) Experimental Embryology. Minneapolis: Burgess.
59. Saari, J.C (1994) Retinoids in photosensitive systems. In M.B. Sporn, A.B. Roberts, and D.S. Goodman (eds): The Retinoids. New York: Raven Press, pp 351-385.
60. Saari, JC , D C Teller, J.W. Crabb, and L. Bredberg (1985) Properties of an interphotoreceptor retinoid-binding protein from bovine retina. J. Biol. Chem. 260:195-201.
61. Saari, J.C., GG. Garwin, J. Haung, and J.W. Crabb (1992) Purification and properties of an aldehyde dehydrogenase from bovine retina that oxidizes retinaldehyde to retinoic acid. Invest. Ophthalmol. Vis. Sci. 33(Suppl.):1182
62. Schubert, D., M LaCorbiere, and F. Esch (1986) A chick neural retina adhesion and survival molecule is a retinal-binding protein. J. Cell Biol. 102:2295-2301.
63. Scott, B.L., and N.G. Bazan (1989) Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc. Natl Acad. Sci. USA 86.2903-2907.
64. Tautz, D., and C. Pfiefle (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translation control of the segmentation gene hunchack. Chromosoma 98:81-85.
65. Tombran-Tink, J., S.M Shivaram, G.J. Chader, L.V. Johnson, D. Bok (1995) Expression, secretion, and age-related downregulation of pigment epithelium-derived factor serpin with neurotrophic activity J. Neurosci. 15.4992-5003.
66. Uehara, F., M T. Matthes, D. Yasumura, and M.M. LaVail (1990) Light-evoked changes in the interphotoreceptor matrix. Science 248:1633-1636.
67. Ying, S.-Y , S. Li, M. Ishikawa, L V. Johnson (1995) Immunohistochemical localization of inhibin in the retinal interphotoreceptor matrix. Exp. Eye Res. 60:585-590.
68. van Veen, T.H., A. Katial, T. Shinohara, D.J. Banett, B. Wiggert, G.J. Chader, and J.M. Nickerson (1986) Retinal photoreceptor neurons and pinealocytes accumulate mRNA for interphotoreceptor retinoid-binding protein (IRBP). FEBS Lett. 208:133-137.
69. Vollmer, G , and P.G. Layer (1986) An in vitro moldel of proliferation and differentiation of the chick retina: Coaggregates of retinal and pigment epithelial cells J. Neurosci. 6:1885-1896
70. Wagenhorst, B.B, R.R. Rajendran, E.E Van Niel, R.B. Hessler, A. Bukelman, and F. Gonzalez-Fernandez (1995) Goldfish cones secrete a two repeat interphotoreceptor retinoid-binding protein. J. Mol. Evol., 41:646-656.
71. Yokoyama, T., G.I. Liou, R.B. Caldwell, and P.A. Overbeek (1992) Photoreceptor-specific activity of the human interphotoreceptor retinoid-binding protein (IRBP) promoter in transgenic mice. Exp. Eye Res. 55.225-238.
72. Xiao-Ying, Y., G.S. Hageman, and M F. Marmor (1992) Recovery of retinal adhesion after enzymatic perturbation of the interphotoreceptor matrix. Invest. Ophthalmol. Vis. Sci. 33:498-503.
73. Zauberman, H. (1979) Adhesive forces between the retinal pigment epithelium and sensory retina. In K.M. Zinn and M.F. Marmor (eds): The Retinal Pigment Epithelium. Cambridge, MA: Harvard Universiy Press, pp. 192-204.
74. Zimmerman, L.E., and A.B. Eastham (1959). Acid mucopolysaccharide in the retinal pigment epithelium and visual cell layer of the developing mouse eye. Am. J Ophthalmol 47:488-498.