Identification of a novel Drosophila opsin reveals specific patterning of the R7 and R8 photoreceptor cells

Neuron

Volumn 17, Issue 6, 1996, Pages 1101-1115

  Chou, Wen Hai ^a   Hall, Kristin J ^a   Wilson, D Bianca ^a   Wideman, Christi L ^a   Townson, Steven M ^a   Chadwell, Linda V ^a   Britt, Steven G ^a  

^a University of Texas Health Science Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; OPSIN; RHODOPSIN;

ARTICLE; COLOR DISCRIMINATION; DROSOPHILA; GENE EXPRESSION; GENE ISOLATION; MOLECULAR CLONING; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; VISUAL STIMULATION;

EID: 0030450107     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80243-3     Document Type: Article

References (97)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Ashburner, M. (1989). Biotinylated DNA in situ hybridization. In Drosophila: A Laboratory Manual (Plainview, New York: Cold Spring Harbor Laboratory Press), pp. 44-49.
3. Baldwin, J.M. (1993). The probable arrangement of the helices in G protein-coupled receptors. EMBO J. 12, 1693-1703.
4. Banerjee, U., and Zipursky, S.L. (1990). The role of cell-cell interaction in the development of the Drosophila visual system. Neuron 4, 177-187.
5. Banerjee, U., Renfranz, P.J., Pollock, J.A., and Benzer, S. (1987). Molecular characterization and expression of sevenless, a gene involved in neuronal pattern formation in the Drosophila eye. Cell 49, 281-291.
6. Basler, K., and Hafen, E. (1988). Control of photoreceptor cell fate by the sevenless protein requires a functional tyrosine kinase domain. Cell 54, 299-311.
7. Basler, K., and Hafen, E. (1989). Ubiquitous expression of sevenless: position-dependent specification of cell fate. Science 243, 931-934.
8. Bownds, D. (1967). Site of attachment of retinal in rhodopsin. Nature 216, 1178-1181.
9. Breathnach, R., and Chambon, P. (1981). Organization and expression of eucaryotic split genes coding for proteins. Annu. Rev. Biochem. 50, 349-383.
10. Britt, S.G., Feiler, R., Kirschfeld, K., and Zuker, C.S. (1993). Spectral tuning of rhodopsin and metarhodopsin in vivo. Neuron 11, 29-39.
11. Burkhardt, D. (1962). Spectral sensitivity and other response characteristics of single visual cells in the arthropod eye. Symp. Soc. Exp. Biol. 16, 86-109.
12. Carulli, J.P., and Hartl, D.L. (1992). Variable rates of evolution among Drosophila opsin genes. Genetics 132, 193-204.
13. Colley, N.J., Baker, E.K., Stamnes, M.A., and Zuker, C.S. (1991). The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67, 255-263.
14. Cowman, A., Zuker, C., and Rubin, G. (1986). An opsin gene expressed in only one photoreceptor cell type of the Drosophila eye. Cell 44, 705-710.
15. Dickson, B., and Hafen, E. (1993). Genetic dissection of eye development in Drosophila. In The Development of Drosophila Melanogaster, M. Bate and A. M. Arias, eds. (Plainview, New York: Cold Spring Harbor Laboratory Press), pp. 1327-1362.
16. Dohlman, H.G., Thorner, J., Caron, M.G., and Lefkowitz, R.J. (1991). Model systems for the study of seven-transmembrane-segment receptors. Annu. Rev. Biochem. 60, 653-688.
17. Feiler, R., Harris, W.A., Kirschfeld, K., Wehrhahn, C., and Zuker, C.S. (1988). Targeted misexpression of a Drosophila opsin gene leads to altered visual function. Nature 333, 737-741.
18. Feiler, R., Bjornson, R., Kirschfeld, K., Mismer, D., Rubin, G.M., Smith, D.P., Socolich, M., and Zuker, C.S. (1992). Ectopic expression of ultraviolet-rhodopsins in the blue photoreceptor cells of Drosophila: visual physiology and photochemistry of transgenic animals. J. Neurosci. 12, 3862-3868.
19. The Flybase Consortium. (1996). FlyBase: the Drosophila database. Nucl. Acids Res. 24, 53-56.
20. 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.
21. Franceschini, N., Kirschfeld, K., and Minke, B. (1981). Fluorescence of photoreceptor cells observed in vivo. Science 213, 1264-1267.
22. Fryxell, K.J., and Meyerowitz, E.M. (1987). An opsin gene that is expressed only in the R7 photoreceptor cell of Drosophila. EMBO J. 6, 443-451.
23. Gish, W., and States, D.J. (1993). Identification of protein coding regions by database similarity search. Nature Genet. 3, 266-272.
24. Hafen, E., Basler, K., Edstroem, J.E., and Rubin, G.M. (1987). Sevenless, a cell-specific homeotic gene of Drosophila, encodes a putative transmembrane receptor with a tyrosine kinase domain. Science 236, 55-63.
25. Hardie, R.C. (1979). Electrophysiological analysis of fly retina. I: Comparative properties of R 1-6 and R 7 and 8. J. Comp. Physiol. 129, 19-33.
26. Hardie, R.C. (1983). Projection and connectivity of sex-specific photoreceptors in the compound eye of the male housefly (Musca domestica). Cell Tiss. Res. 233, 1-21.
27. Hardie, R.C. (1984). Properties of photoreceptors R7 and R8 in the dorsal marginal ommatidia in the compound eyes of Musca and Calliphora. J. Comp. Physiol. A. 154, 157-165.
28. Hardie, R.C. (1985). Functional organization of the fly retina. In Progress in Sensory Physiology, H. Autrum, D. Ottoson, E.R. Perl, R.F. Schmidt, H. Shimazu, and W. D. Willis, eds. (Berlin: Springer-Verlag), pp. 1-79.
29. Hardie, R.C., and Kirschfeld, K. (1983). Ultraviolet sensitivity of fly photoreceptors R7 and R8: evidence for a sensitising function. Biophys. Struct. Mech. 9, 171-180.
30. Hardie, R.C., Franceschini, N., and McIntyre, P.D. (1979). Electrophysiological analysis of fly retina. II: Spectral and polarisation sensitivity in R7 and R8. J. Comp. Physiol. 133, 23-39.
31. Hardie, R.C., Voss, D., Pongs, O., and Laughlin, S.B. (1991). Novel potassium channels encoded by the Shaker locus in Drosophila photoreceptors. Neuron 6, 477-486.
32. Harris, W.A., Stark, W.S., and Walker, J.A. (1976). Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster. J. Physiol. 256, 415-439.
33. Hart, A.C., Kramer, H., Van Vactor, D.L., Jr., Paidhungat, M., and Zipursky, S.L. (1990). Induction of cell fate in the Drosophila retina: the bride of sevenless protein is predicted to contain a large extracellular domain and seven transmembrane segments. Genes Dev. 4, 1835-1847.
34. Hart, A.C., Kramer, H., and Zipursky, S.L. (1993). Extracellular domain of the boss transmembrane ligand acts as an antagonist of the sev receptor. Nature 361, 732-736.
35. Heisenberg, M. (1971). Separation of receptor and lamina potentials in the electroretinogram of normal and mutant Drosophila. J. Exp. Biol. 55, 85-100.
36. Heisenberg, M., and Wolf, R. (1984). Vision in Drosophila (New York: Springer-Verlag).
37. Higgins, D.G., and Sharp, P.M. (1989). Fast and sensitive multiple sequence alignments on a microcomputer. Comput. Appl. Biosci. 5, 151-153.
38. Hu, K.G., Reichert, H., and Stark, W.S. (1978). Electrophysiological characterization of Drosophila ocelli. J. Comp. Physiol. A. 126, 15-24.
39. Huber, A., Smith, D.P., Zuker, C.S., and Paulsen, R. (1990). Opsin of Calliphora peripheral photoreceptors R1-6. Homology with Drosophila Rh1 and posttranslational processing. J. Biol. Chem. 265, 17906-17910.
40. Isono, K., Tanimura, T., Oda, Y., and Tsukahara, Y. (1988). Dependency on light and vitamin A derivatives of the biogenesis of 3-hydroxyretinal and visual pigment in the compound eyes of Drosophila melanogaster. J. Gen. Physiol. 92, 587-600.
41. Jacobs, G.H. (1981). Comparative color vision, E. C. Carterette and M. P. Friedman, eds. (New York: Academic Press).
42. Johnson, E.C., and Pak, W.L. (1986). Electrophysiological study of Drosophila rhodopsin mutants. J. Gen. Physiol. 88, 651-673.
43. Karess, R., and Rubin, G. (1984). Analysis of P transposable element functions in Drosophila. Cell 38, 135-146.
44. Karnik, S.S., and Khorana, H.G. (1990). Assembly of functional rhodopsin requires a disulfide bond between cysteine residues 110 and 187. J. Biol. Chem. 265, 17520-17524.
45. Karnik, S.S., Sakmar, T.P., Chen, H.B., and Khorana, H.G. (1988). Cysteine residues 110 and 187 are essential for the formation of correct structure in bovine rhodopsin. Proc. Natl. Acad. Sci. USA 85, 8459-8463.
46. Kirschfeld, K., and Franceschini, N. (1977). Evidence for a sensitising pigment in fly photoreceptors. Nature 269, 386-390.
47. Kirschfeld, K., Feiler, R., and Franceschini, N. (1978). A photostable pigment within the rhabdomeres of fly photoreceptors no. 7. J. Comp. Physiol. 725, 275-284.
48. Kirschfeld, K., Hardie, R.C., Lenz, G., and Vogt, K. (1988a). The pigment system of the photoreceptor 7 yellow in the fly, a complex photoreceptor. J. Comp. Physiol. A. 162, 421-433.
49. Kirschfeld, K., Feiler, R., and Vogt, K. (1988b). Evidence for a sensitizing pigment in the ocellar photoreceptors of the fly (Musca, Calliphora). J. Comp. Physiol. A. 163, 421-423.
50. Kozak, M. (1991). Structural features in eukaryotic mRNAs that modulate the initiation of translation. J. Biol. Chem. 266, 19867-19870.
51. Kramer, H., Cagan, R.L., and Zipursky, S.L. (1991). Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor. Nature 352, 207-212.
52. Kurada, P., and O'Tousa, J.E. (1995). Retinal degeneration caused by dominant rhodopsin mutations in Drosophila. Neuron 14, 571-579.
53. Kyte, J., and Doolittle, R.F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
54. Lawrence, P.A., and Green, S.M. (1979). Cell lineage in the developing retina of Drosophila. Dev. Biol. 71, 142-152.
55. Lindsley, D.L., and Zimm, G.G. (1992). Genome of Drosophila melanogaster (Academic Press, San Diego).
56. Meffert, P., and Smola, U. (1976). Electrophysiological measurements of spectral sensitivity of central visual cells in eye of blowfly. Nature 260, 342-344.
57. Minke, B., and Kirschfeld, K. (1979). The contribution of a sensitizing pigment to the photosensitivity spectra of fly rhodopsin and metarhodopsin. J. Gen. Physiol. 73, 517-540.
58. Montell, C., Jones, K., Zuker, C., and Rubin, G. (1987). A second opsin gene expressed in the ultraviolet sensitive R7 photoreceptor cells of Drosophila melanogaster. J. Neurosci. 7, 1558-1566.
59. Nathans, J. (1990). Determinants of visual pigment absorbance: identification of the retinylidene Schiff's base counterion in bovine rhodopsin. Biochemistry 29, 9746-9752.
60. Nathans, J. (1992). Rhodopsin: structure, function, and genetics. Biochemistry 31, 4923-4931.
61. Nathans, J., Thomas, D., and Hogness, D.S. (1986a). Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232, 193-202.
62. Nathans, J., Piantanida, T.P., Eddy, R.L., Shows, T.B., and Hogness, D.S. (1986b). Molecular genetics of inherited variation in human color vision. Science 232, 203-210.
63. Nathans, J., Merbs, S.L., Sung, C.H., Weitz, C.J., and Wang, Y. (1992). Molecular genetics of human visual pigments. Annu. Rev. Genet. 26, 403-424.
64. O'Connell, P.O., and Rosbash, M. (1984). Sequence, structure, and codon preference of the Drosophila ribosomal protein 49 gene. Nucl. Acids Res. 12, 5495-5513.
65. Ohguro, H., Rudnicka-Nawrot, M., Buczylko, J., Zhao, X., Taylor, J.A., Walsh, K.A., and Palczewski, K. (1996). Structural and enzymatic aspects of rhodopsin phosphorylation. J. Biol. Chem. 271, 5215-5224.
66. Oprian, D.D. (1992). The ligand-binding domain of rhodopsin and other G protein-linked receptors. J. Bioenerg. Biomem. 24, 211-217.
67. O'Tousa, J.E., Baehr, W., Martin, R.L., Hirsh, J., Pak, W.L., and Applebury, M.L. (1985). The Drosophila ninaE gene encodes an opsin. Cell 40, 839-850.
68. Patton, J.S., Gomes, X.V., and Geyer, P.K. (1992). Position-independent germline transformation in Drosophila using a cuticle pigmentation gene as a selectable marker. Nucl. Acids Res. 20, 5859-5860.
69. Pollack, J.A., and Benzer, S. (1988). Transcript localization of four opsin genes in the three visual organs of Drosophila; RH2 is ocellus specific. Nature 333, 779-782.
70. Ranganathan, R., Harris, W.A., and Zuker, C.S. (1991). The molecular genetics of invertebrate phototransduction. Trends Neurosci. 14, 486-493.
71. Ready, D.F., Hanson, T.E., and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
72. Reinke, R., and Zipursky, S.L. (1988). Cell-cell interaction in the Drosophila retina: the bride of sevenless gene is required in photoreceptor cell R8 for R7 cell development. Cell 55, 321-330.
73. Renfranz, P.J., and Benzer, S. (1989). Monoclonal antibody probes discriminate early and late mutant defects in development of the Drosophila retina. Dev. Biol. 136, 411-429.
74. Ressler, K.J., Sullivan, S.L., and Buck, L.B. (1994). A molecular dissection of spatial patterning in the olfactory system. Curr. Opin. Neurobiol. 4, 588-596.
75. Robertson, H.M., and Engels, W.R. (1989). Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics 123, 815-824.
76. Sakmar, T.P., Franke, R.R., and Khorana, H.G. (1989). Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc. Natl. Acad. Sci. USA 86, 8309-8313.
77. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (Plainview, New York: Cold Spring Harbor Laboratory Press).
78. Scavarda, N.J., O'Tousa, J., and Pak, W.L. (1983). Drosophila locus with gene-dosage effects on rhodopsin. Proc. Natl. Acad. Sci. USA 80, 4441-4445.
79. Schertler, G.F., Villa, C., and Henderson, R. (1993). Projection structure of rhodopsin. Nature 362, 770-772.
80. Sengupta, P., Chou, J.H., and Bargmann, C.I. (1996). odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899-909.
81. Smola, U., and Meffert, P. (1979). The spectral sensitivity of the visual cells R7 and R8 in the eye of the blowfly Calliphora erythrocephala. J. Comp. Physiol. 133, 41-52.
82. Stark, W.S. (1977). Sensitivity and adaptation in R7, an ultraviolet photoreceptorin the Drosophila retina. J. Comp. Physiol. 115, 47-59.
83. Stark, W.S., Ivanyshyn, A.M., and Greenberg, R.M. (1977). Sensitivity and photopigments of R1-6; a two-peaked photoreceptor in Drosophila, Calliphora and Musca. J. Comp. Physiol. 121, 289-305.
84. Stryer, L. (1986). Cyclic GMP Cascade of Vision. Annu. Rev. Neurosci. 9, 87-119.
85. Sved, J. (1986). Eyes absent. Dros. Inf. Serv. 63, 169.
86. Swimmer, C., and Shenk, T. (1985). Selection of sequence elements that substitute for the standard AATAAA motif which signals 3′ processing and polyadenylation of late simian virus 40 mRNAs. Nucl. Acids Res. 13, 8053-8063.
87. Tomlinson, A., Bowtell, D.D., Hafen, E., and Rubin, G.M. (1987). Localization of the sevenless protein, a putative receptor for positional information, in the eye imaginal disc of Drosophila. Cell 51, 143-150.
88. Van Vactor, D.L., Jr., Cagan, R.L., Kramer, H., and Zipursky, S.L. (1991). Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell. Cell 67, 1145-1155.
89. Vogt, K. (1984). The chromophore of the visual pigment in some insect orders. Z. Naturforsch. 39c, 196-197.
90. Vogt, K., and Kirschfeld, K. (1984). Chemical identity of the chromophores of fly visual pigment. Naturwissenschaften 71, 211-213.
91. Wolff, T., and Ready, D.F. (1993). Pattern formation in the Drosophila retina. In The Development of Drosophila melanogaster, M. Bate and A. M. Arias, eds. (Plainview, New York: Cold Spring Harbor Laboratory Press), pp. 1277-1325.
92. Zhukovsky, E.A., and Oprian, D.D. (1989). Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246, 928-930.
93. Zipursky, S.L., and Rubin, G.M. (1994). Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. Annu. Rev. Neurosci. 17, 373-397.
94. Zuker, C.S. (1996). The biology of vision of Drosophila. Proc. Natl. Acad. Sci. USA 93, 571-576.
95. Zuker, C.S., Cowman, A.F., and Rubin, G.M. (1985). Isolation and structure of a rhodopsin gene from D. melanogaster. Cell 40, 851-858.
96. Zuker, C., Montell, C., Jones, K., Laverty, T., and Rubin, G. (1987). A rhodopsin gene expressed in photoreceptor cell R7 of the Drosophila eye: homologies with other signal-transducing molecules. J. Neurosci. 7, 1550-1557.
97. Zuker, C.S., Mismer, D., Hardy, R., and Rubin, G.M. (1988). Ectopic expression of a minor Drosophila opsin in the major photoreceptor cell class: distinguishing the role of primary receptor and cellular context. Cell 53, 475-482.