The Drosophila ninaE gene encodes an opsin

The Drosophila ninaE gene was isolated by a multistep protocol on the basis of its homology to bovine opsin cDNA. The gene encodes the major visual pigment protein (opsin) contained in Drosophila photoreceptor cells R1-R6. The coding sequence is interrupted by four short introns. The positions of three introns are conserved with respect to positions in mammalian opsin genes. The nucleotide sequence has intermittent regions of homology to bovine opsin coding sequences. The deduced amino acid sequence reveals significant homology to vertebrate opsins; there is strong conservation of the retinal binding site and two other regions. The predicted protein secondary structure strikingly resembles that of mammalian opsins. We conclude the Drosophila and vertebrate opsin genes are derived from a common ancestor.

[1]  G. Wald.  The Molecular Basis of Visual Excitation , 1968, Nature.

[2]  K Kirschfeld,et al.  Fluorescence of photoreceptor cells observed in vivo. , 1981, Science.

[3]  C. Vandenberg,et al.  Light-regulated biochemical events in invertebrate photoreceptors. 2. Light-regulated phosphorylation of rhodopsin and phosphoinositides in squid photoreceptor membranes. , 1984, Biochemistry.

[4]  H. Boedtker,et al.  RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. , 1977, Biochemistry.

[5]  P. Hargrave,et al.  Light-induced binding of guanosinetriphosphatase to bovine photoreceptor membranes: effect of limited proteolysis of the membranes. , 1981, Biochemistry.

[6]  E. Dratz,et al.  The structure of rhodopsin and the rod outer segment disk membrane , 1983 .

[7]  M. Pardue,et al.  Telomere regions in drosophila share complex DNA sequences with pericentric heterochromatin , 1983, Cell.

[8]  W. Harris,et al.  Genetic dissection of the photoreceptor system in the compound eye of Drosophila melanogaster , 1976, The Journal of physiology.

[9]  D. Bownds.  Site of Attachment of Retinal in Rhodopsin , 1967, Nature.

[10]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[11]  H. Kühn.  Chapter 5 Interactions between photoexcited rhodopsin and light-activated enzymes in rods , 1984 .

[12]  T. Maniatis,et al.  Full length and discrete partial reverse transcripts of globin and chorion mRNAs , 1975, Cell.

[13]  Lubert Stryer,et al.  Transducin: an amplifier protein in vision , 1981 .

[14]  B Fristensky,et al.  Portable microcomputer software for nucleotide sequence analysis. , 1982, Nucleic acids research.

[15]  F. Blattner,et al.  Charon phages: safer derivatives of bacteriophage lambda for DNA cloning. , 1977, Science.

[16]  W. Pak,et al.  Drosophila locus with gene-dosage effects on rhodopsin. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[17]  C. Vandenberg,et al.  Light-regulated biochemical events in invertebrate photoreceptors. 1. Light-activated guanosinetriphosphatase, guanine nucleotide binding, and cholera toxin catalyzed labeling of squid photoreceptor membranes. , 1984, Biochemistry.

[18]  S. W. Hall,et al.  Light‐induced binding of 48‐kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin , 1984, FEBS letters.

[19]  J. Nathans,et al.  Isolation and nucleotide sequence of the gene encoding human rhodopsin. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[20]  T. Goldsmith.  The Natural History of Invertebrate Visual Pigments , 1972 .

[21]  D. Pappin,et al.  Primary structure of C-terminal functional sites in ovine rhodopsin , 1981, Nature.

[22]  P. Sharp,et al.  Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids , 1977, Cell.

[23]  K. Kirschfeld,et al.  Reversible events in the transduction process of photoreceptors , 1980, Nature.

[24]  H. Saibil,et al.  Squid rhodopsin and GTP-binding protein crossreact with vertebrate photoreceptor enzymes. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[25]  W. A. Hagins.  The visual process: Excitatory mechanisms in the primary receptor cells. , 1972, Annual review of biophysics and bioengineering.

[26]  D. Pappin,et al.  A structural model for ovine rhodopsin , 1984 .

[27]  C Benoist,et al.  The ovalbumin gene-sequence of putative control regions , 1980, Nucleic Acids Res..

[28]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[29]  R. Doolittle,et al.  A simple method for displaying the hydropathic character of a protein. , 1982, Journal of molecular biology.

[30]  D. Pappin,et al.  Sequence variability in the retinal-attachment domain of mammalian rhodopsins. , 1984, The Biochemical journal.

[31]  B. Schmidt-Nielsen,et al.  CHARACTERIZATION OF AN α‐BUNGAROTOXIN BINDING COMPONENT FROM DROSOPHILA MELANOGASTER , 1977 .

[32]  J. Findlay,et al.  Isolation and characterization of the CNBr peptides from the proteolytically derived N-terminal fragment of ovine opsin. , 1983, The Biochemical journal.

[33]  G. Rubin,et al.  Physical map of the white locus of Drosophila melanogaster. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[34]  N. Davidson,et al.  Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner , 1983, Cell.

[35]  G. Rubin,et al.  Isolation and structure of a rhodopsin gene from D. melanogaster , 1985, Cell.

[36]  S. Garen,et al.  Golgi and genetic mosaic analyses of visual system mutants in Drosophila melanogaster. , 1983, Developmental biology.

[37]  W. Gilbert,et al.  Sequencing end-labeled DNA with base-specific chemical cleavages. , 1980, Methods in enzymology.

[38]  N. Davidson,et al.  The actin genes of drosophila: Protein coding regions are highly conserved but intron positions are not , 1981, Cell.

[39]  W. Lennarz,et al.  The Function of Saccharide-Lipids in Synthesis of Glycoproteins , 1980 .

[40]  J. Schwemer,et al.  Proteins of invertebrate photoreceptor membranes. Characterization of visual-pigment preparations by gel electrophoresis. , 1973, European journal of biochemistry.

[41]  W. Pak,et al.  Drosophila rhodopsin: photochemistry, extraction and differences in the norp AP12 phototransduction mutant. , 1974, Biochemical and biophysical research communications.

[42]  T. Ebrey,et al.  A light-activated GTPase from octopus photoreceptors. , 1980, Biochemical and biophysical research communications.

[43]  S. Benzer,et al.  Neuronal development in the drosophila retina: Monoclonal antibodies as molecular probes , 1984, Cell.

[44]  J. Nathans,et al.  Isolation, sequence analysis, and intron-exon arrangement of the gene encoding bovine rhodopsin , 1983, Cell.

[45]  E. Southern.  Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[46]  F. M. Hagins.  Purification and partial characterization of the protein component of squid rhodopsin. , 1973, The Journal of biological chemistry.

[47]  W. D. Benton,et al.  Screening lambdagt recombinant clones by hybridization to single plaques in situ. , 1977, Science.

[48]  U Wilden,et al.  Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. , 1982, Biochemistry.

[49]  L. Kauvar,et al.  The engrailed locus of drosophila: Structural analysis of an embryonic transcript , 1985, Cell.

[50]  M. Sanders.  Handbook of Sensory Physiology , 1975 .

[51]  A. Oseroff,et al.  Resonance Raman spectroscopy of rhodopsin in retinal disk membranes. , 1974, Biochemistry.

[52]  R. Hardison,et al.  The isolation of structural genes from libraries of eucaryotic DNA , 1978, Cell.

[53]  W. Pak,et al.  Drosophila mutants with reduced rhodopsin content. , 1983, Symposia of the Society for Experimental Biology.

[54]  J. Lythgoe,et al.  List of Vertebrate Visual Pigments , 1972 .

[55]  R. Kretsinger,et al.  Structure and evolution of calcium-modulated proteins. , 1980, CRC critical reviews in biochemistry.

[56]  K. Hamdorf.  The Physiology of Invertebrate Visual Pigments , 1979 .

[57]  J. Hirsh,et al.  The cloned dopa decarboxylase gene is developmentally regulated when reintegrated into the drosophila genome , 1983, Cell.

[58]  D. Hogness,et al.  An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences , 1982, Cell.

[59]  R. Hubbard,et al.  THE RHODOPSIN SYSTEM OF THE SQUID , 1958, The Journal of general physiology.

[60]  E. N. Pugh,et al.  The control of phosphodiesterase in rod disk membranes: Kinetics, possible mechanisms and significance for vision , 1979, Vision Research.

[61]  G. Fain,et al.  Light-dependent calcium release from photoreceptors measured by laser micro-mass analysis , 1984, Nature.

[62]  P. Argos,et al.  Structural prediction of membrane-bound proteins. , 2005, European journal of biochemistry.

[63]  P Chambon,et al.  Organization and expression of eucaryotic split genes coding for proteins. , 1981, Annual review of biochemistry.

[64]  S. Ostroy.  Characteristics of Drosophila rhodopsin in wild-type and norpA vision transduction mutants , 1978, The Journal of general physiology.

[65]  J. West,et al.  Light activation of bovine rod phosphodiesterase by non‐physiological visual pigments , 1980, FEBS letters.

[66]  N. Proudfoot,et al.  3′ Non-coding region sequences in eukaryotic messenger RNA , 1976, Nature.