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Characterization and regulation of the protein binding to a cis-acting element, RET 1, in the rat opsin promoter

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Abstract

RET 1 is a binding site for retinal nuclear proteins located at −136 to −110 bp in the rat opsin promoter, as defined by DNase protection assays. A similar sequence is found in the upstream flanking regions of many other photoreceptor genes in mammals and other species, includingDrosophila. A 7-base consensus sequence, CAATTAG, is found in these genes and has the binding activity of the longer RET 1 element. A 40-kDa protein that binds to RET 1 has been purified over 2 × 105-fold to apparent homogeneity by affinity chromatography. The RET 1 binding activity is first detectable at E18 and increases during the first two postnatal weeks. At embryonic ages the retarded bands show an altered mobility and at early postnatal ages two bands are detected, with the adult band increasing and the embryonic band decreasing in intensity. Treatment of early postnatal retinas with bFGF increased the binding activity in nuclear extracts and caused a shift in migration of the retarded band to a position characteristic of the embryonic form of the complex. The results support the hypothesis that RET 1-like elements play an important role in rod photoreceptor development.

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References

  • Ahmad I., Yu X., and Barnstable C. J. (1994) Acis-acting element, Ta-1, in the upstream region of rod a-transducin gene that binds a developmentally regulated retina-specific nuclear factor.J. Neurochem. 62, 396–399.

    Article  PubMed  CAS  Google Scholar 

  • Altshuler D. M., Turner D. L., and Cepko C. K. (1991) Specification of cell type in the vertebrate retina, inDevelopment of the Visual System (Lam D. M. K. and Shatz C. J., eds.), MIT Press, Cambridge, MA, pp. 37–58.

    Google Scholar 

  • Altshuler D. and Cepko C. K. (1992) A temporally regulated, diffusible activity is required for rod photoreceptor development in vitro.Development 114, 947–957.

    PubMed  CAS  Google Scholar 

  • Altshuler D., Turco J. J. L., Rush J., and Cepko C. K. (1993) Taurine promotes the differentiation of a vertebrate retinal cell type in vitro.Development 119, 1317–1328.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Barnstable C. J. (1991) Molecular aspects of development of mammalian optic cup and formation of retinal cell types.Prog. Retina Res. 10, 45–67.

    Article  CAS  Google Scholar 

  • Barnstable C. J. and Morabito M. A. (1994) Isolation and coding sequence of the rat opsin gene.J. Mol. Neurosci. 5, 207–209.

    PubMed  CAS  Google Scholar 

  • Dignam J. D., Lebowitz R. M., and Roeder R. G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.Nucleic Acids Res. 11, 1475–1489.

    Article  PubMed  CAS  Google Scholar 

  • Fortini M. and Rubin M. G. (1990) Analysis of cis-acting requirements of the Rh3 and Rh4 genes reveals a bipartite organization to rhodopsin promoters in Drosophila melanogaster.Genes Develop. 4, 444–463.

    Article  PubMed  CAS  Google Scholar 

  • Hager D. A. and Gurgess R. R. (1980) Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes.Anal. Biochem. 109, 76–86.

    Article  PubMed  CAS  Google Scholar 

  • Hicks D. and Barnstable C. J. (1987) Different monoclonal antibodies reveal different binding patterns on developing and adult retina.J. Histochem. Cytochem. 35, 1317–1328.

    PubMed  CAS  Google Scholar 

  • Hicks D. and Courtois Y. (1988) Acidic fibroblast growth factor stimulates opsin levels in retinal photoreceptor cells in vitro.FEBS Lett. 234, 475–479.

    Article  PubMed  CAS  Google Scholar 

  • Hoppe-Seyler F., Butz K., Rittmuller C., and Doeberitz K. M. (1991) A rapid microscale nuclear procedure for the simultaneous preparation of cytoplasmic RNA, nuclear DNA binding proteins and enzymatically active luciferase extracts.Nucleic Acids Res. 19, 5080.

    Article  PubMed  CAS  Google Scholar 

  • Kadonaga J. T. and Tjian R. (1986) Affinity purification of sequence-specific DNA binding proteins.Proc. Natl. Acad. Sci. USA 83, 5889–5893.

    Article  PubMed  CAS  Google Scholar 

  • Kelley M. W., Turner J. K., and Reh T. A. (1994) Retinoic acid promotes differentiation of photoreceptors in vitro.Development 120, 2091–2102.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  • Lem J., Applebury M. L., Falk J. D., Flannery J. G., and Simon M. I. (1991) Tissue-specific and developmental regulation of rod opsin chimeric genes in transgenic mice.Neuron 6, 201–210.

    Article  PubMed  CAS  Google Scholar 

  • Morabito M. A., Yu X., and Barnstable 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.

    PubMed  CAS  Google Scholar 

  • Nathans J. and Hogness D. S. (1983) Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin.Cell 34, 807–814.

    Article  PubMed  CAS  Google Scholar 

  • Nathans J. and Hogness D. S. (1984) Isolation and nucleotide sequence of the gene encoding human rhodopsin.Proc. Natl. Acad. Sci. USA 81, 4851–4855.

    Article  PubMed  CAS  Google Scholar 

  • Reh T. A. (1991) Determination of cell fate during retinal histogenesis: intrinsic and extrinsic mechanisms, inDevelopment of the Visual System (Lam D. M. K. and Shatz C. J., eds.), MIT Press, Cambridge, MA, pp. 79–94.

    Google Scholar 

  • Sambrook J., Fritsch E. F., and Maniatis T. (1989)Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Sparrow J. R., Hicks D., and Barnstable C. J. (1990) Cell commitment and differentiation in explants of embryonic rat retina. Comparison to the developmental potential of dissociated retina.Dev. Brain Res. 51, 69–84.

    Article  CAS  Google Scholar 

  • Tapscott S. J., Davis R. L., Thayer M. J., Cheng P. F., Weintraub H., and Lassar A. B. (1988) Myo-D: a nuclear phosphoprotein requiring a myc homology region to convert fibroblasts to myoblasts.Science 242, 405–411.

    Article  PubMed  CAS  Google Scholar 

  • Treisman J. E., Morabito M. A., and Barnstable C. J. (1988) Opsin expression in the rat retina is developmentally regulated by transcriptional activation.Mol. Cell. Biol. 8, 1570–1579.

    PubMed  CAS  Google Scholar 

  • Wang Y., Macke J. P., Merbs S. L., Zack D. J., Klaunberg B., Bennett J., Gearhart J., and Nathans J. (1992) A locus control region adjacent to the human red and green visual pigment genes.Neuron 9, 429–440.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T. and Raff M. (1990) Rod photoreceptor development in vitro: intrinsic properties of proliferating neuroepithelial cells change as development proceeds in the rat retina.Neuron 4, 461–467.

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T. and Raff M. C. (1992) Diffusible rod-promoting signals in the developing rat retina.Development 114, 899–906.

    PubMed  CAS  Google Scholar 

  • Yu X., Chung M., Morabito M. A., and Barnstable C. J. (1993) Shared nuclear protein binding sites in the upstream region of the rat opsin gene.Biochem. Biophys. Res. Comm. 191, 76–82.

    Article  PubMed  CAS  Google Scholar 

  • Zack D. J., Bennet J., Wang Y., Davenport C., Klaungerg B., Gearhart J., and Nathans J. (1991) Unusual topography of bovine rhodopsin promoter-lacZ fusion gene expression in transgenic mouse retinas.Neuron 6, 187–199.

    Article  PubMed  CAS  Google Scholar 

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  1. Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven, CT

    Xiu Yu & Colin J. Barnstable

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  1. Xiu Yu
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  2. Colin J. Barnstable
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Yu, X., Barnstable, C.J. Characterization and regulation of the protein binding to a cis-acting element, RET 1, in the rat opsin promoter. J Mol Neurosci 5, 259–271 (1994). https://doi.org/10.1007/BF02736726

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  • DOI: https://doi.org/10.1007/BF02736726

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