Abstract
The function of conserved novel human genes can be efficiently addressed in genetic model organisms. From a collection of genes expressed in the Drosophila visual system, cDNAs expressed in vertebrates were identified and one similar to a novel human gene was chosen for further investigation. The results reported here characterize the Drosophila retinophilin gene and demonstrate that a similar gene is expressed in the human retina. The Drosophila and human retinophilin sequences are 50% identical, and they share an additional 16% conserved substitutions. Examination of the cDNA and genomic sequence indicates that it corresponds to the gene CG10233 of the annotated genome and predicts a 22.7 kDa protein. Polyclonal antibodies generated to a predicted retinophilin peptide recognize an antigen in Drosophila photoreceptor cells. The retinophilins encode 4 copies of a repeat associated with a Membrane Occupation and Recognition Nexus (MORN) function first discovered in junctophilins, which may interact with the plasma membrane. These results therefore show that Drosophila retinophilin is expressed in fly photoreceptor cells, demonstrate that a conserved human gene is expressed in human retina, and suggest that a mutational analysis of the Drosophila gene would be valuable.
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References
Adams MD et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195
Arbeitman MN, Furlong EEM, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270–2275
Benzer S (1991) The 1990 Helmerich lecture: the fly and eye. In: Lam DM, Shatz CJ (eds) Development of the visual system. MIT, Cambridge, MA, pp 9–34
Berridge MJ (1998) Neuronal calcium signaling. Neuron 21:13–26
Boutros M, Kiger AA, Armknecht S, Kerr K, Hild M, Koch B, Haas SA, Consortium HF, Paro R, Perrimon N (2004) Genome-wide RNAi analysis of growth and viability in Drosophila cells. Science 303:832–835
Chowers I, Gunatilaka TL, Farkas RH, Qian J, Hackam AS, Duh E, Kageyama M, Wang C, Vora A, Campochiaro PA, Zack DJ (2003) Identification of novel genes preferentially expressed in the retina using a custom human retina cDNA microarray. Invest Ophthalmol Vis Sci 44:3732–3741
Hardie RC, Raghu P (2001) Visual transduction in Drosophila. Nature 413:186–193
Hyde DR, Mecklenburg KL, Pollock JA, Vihtelic TS, Benzer S (1990) Twenty Drosophila visual system cDNA clones: one is a homolog of human arrestin. Proc Natl Acad Sci USA 87:1008–1012
Koundakjian EJ, Cowan DM, Hardy RW, Becker AH (2004) The Zuker collection: a resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167:203–206
Lee YJ, Dobbs MB, Verardi ML, Hyde DR (1990) dgq: a Drosophila gene encoding a visual system-specific Gα molecule. Neuron 5:889–898
Lee YJ, Shah S, Suzuki E, Zars T, O’Day PM, Hyde DR (1994) The Drosophila dgq gene encodes a Gα protein that mediates phototransduction. Neuron 13:1143–1157
Lein ES, et al (2006) Genome-wide atlas of gene expression in the adult mouse brain. DOI:10.1038/Nature05453
Lennon G, Auffray C, Polymeropoulos M, Soares MB (1996) The I.M.A.G.E consortium: an integrated molecular analysis of genomes and their expression. Genomics 33:151–152
Li C, Geng C, Leung HT, Hong YS, Strong LRR, Schneuwly S, Pak WL (1999) INAF, a protein required for transient receptor potential Ca2+ channel function. Proc Natl Acad Sci USA 96:13474–13479
Montell C (1999) Visual transduction in Drosophila. Annu Rev Cell Dev Biol 15:231–268
Montell C (2005) TRP channels in Drosophila photoreceptor cells. J Physiol 567:45–51
Nishi M, Mizushima A, Nakagawara K, Takeshima H (2000) Characterization of human junctophilin subtype genes. Biochem Biophys Res Commun 273:920–927
Palazzolo MJ, Hyde DR, VijayRaghavan K, Mecklenburg K, Benzer S, Meyerowitz E (1989) Use of a new strategy to isolate and characterize 436 Drosophila cDNA clones corresponding to RNAs detected in adult heads but not in early embryos. Neuron 3:527–539
Schwarz EM, Benzer S (1997) Calx, a Na-Ca exchanger gene of Drosophila melanogaster. Proc Natl Acad Sci USA 94:10249–10254
Shah S, Hyde DR (1995) Two Drosophila genes that encode the α and β subunits of the brain soluble guanylyl cyclase. J Biol Chem 270:15368–15376
Sharon D, Blackshaw S, Cepko CL, Dryja TP (2002) Profile of the genes expressed in the human peripheral retina, macula, and retinal pigment epithelium determined through serial analysis of gene expression (SAGE). Proc Natl Acad Sci USA 99:315–320
Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6:11–22
Venter JC, et al (2001) The sequence of the human genome. Science 291:1304–1351
Wang T, Xu H, Oberwinkler J, Gu Y, Hardie RC, Montell C (2005) Light activation, adaptation, and cell survival functions of the Na+/Ca2+ exchanger CalX. Neuron 45:367–378
Xu H, Lee SJ, Suzuki E, Dugan KD, Stoddard A, Li HS, Chodosh LA, Montell C (2004) A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. EMBO J 23:811–822
Yang Z, Edenberg HJ, Davis RL (2005) Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nuc Acids Res 33:e148
Yoshida M, Sugimoto A, Ohshima Y, Takeshima H (2001) Important role of junctophilin in nematode motor function. Biochem Biophys Res Commun 289:234–239
Zuker CS (1996) The biology of vision in Drosophila. Proc Natl Acad Sci USA 93:571–576
Acknowledgments
Thanks are due to Thomas Morgan, Tracy Eggleston, and James Peyer for their help with the sectioning, and to Robert Pope for his help with the microscopy. Thanks are also due to David Hyde and Joseph O’Tousa for their help in interpreting the antibody localization. This work was supported in part by a Summer Faculty Research Grant from the Indiana University South Bend.
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Communicated by G. Reuter.
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Mecklenburg, K.L. Drosophila retinophilin contains MORN repeats and is conserved in humans. Mol Genet Genomics 277, 481–489 (2007). https://doi.org/10.1007/s00438-007-0211-7
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DOI: https://doi.org/10.1007/s00438-007-0211-7