Single choroideremia gene in nonmammalian vertebrates explains early embryonic lethality of the zebrafish model of choroideremia

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 6, 2009, Pages 3009-3016

  Moosajee, Mariya ^a   Tulloch, Merrin ^a,b   Baron, Rudi A ^b   Gregory Evans, Cheryl Y ^a   Pereira Leal, Jose B ^c   Seabra, Miguel C ^b,c,d  

^a Clinical Neuroscience   (United States)

^b NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d NOVA MEDICAL SCHOOL   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXTRACT; CHOROIDEREMIA PROTEIN; ISOPROTEIN; RAB ESCORT PROTEIN; RAB ESCORT PROTEIN 1; RAB ESCORT PROTEIN 2; UNCLASSIFIED DRUG; RAB PROTEIN; REP1 PROTEIN, ZEBRAFISH; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL MODEL; ARTICLE; BIOINFORMATICS; CHOROIDEREMIA; CYTOSOL; DISEASE COURSE; DISEASE SEVERITY; EMBRYO; EMBRYO DEATH; HISTOPATHOLOGY; IMMUNOBLOTTING; IN VITRO STUDY; INVERTEBRATE; LETHALITY; MOLECULAR EVOLUTION; NICK END LABELING; NONHUMAN; PRENYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; RETINA DEGENERATION; SURVIVAL TIME; VERTEBRATE; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; APOPTOSIS; CELL FRACTIONATION; DISEASE MODEL; EMBRYO DEVELOPMENT; GENETICS; LETHAL GENE; METABOLISM; PATHOLOGY; PHENOTYPE; PHOTORECEPTOR CELL; PRENATAL DEVELOPMENT; PROTEIN PRENYLATION; RETINA; TRANSGENIC ANIMAL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CHOROIDEREMIA; DISEASE MODELS, ANIMAL; EMBRYO LOSS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; EVOLUTION, MOLECULAR; GENES, LETHAL; IMMUNOBLOTTING; IN SITU NICK-END LABELING; PHENOTYPE; PHOTORECEPTOR CELLS, VERTEBRATE; PROTEIN PRENYLATION; RAB GTP-BINDING PROTEINS; RETINA; RETINAL DEGENERATION; SUBCELLULAR FRACTIONS; ZEBRAFISH;

EID: 66849111207     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-2755     Document Type: Article

References (48)

1. Scriver CR, Sly WS, Beaudet AL, Valle D, eds. The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill, Inc; 1995;4311-4324.
2. Heckenlively JR, Bird AJ. Choroideremia. In: Heckenlively JR, Daiger SP, eds. Retinitis Pigmentosa. Philadelphia: JB Lippincott; 1988;176-187.
3. Cremers FP, van de Pol DJ, van Kerkhoff LP, Wieringa B, Ropers HH. Cloning of a gene that is rearranged in patients with choroideraemia. Nature. 1990;347:674-677.
4. Seabra MC, Brown MS, Goldstein JL. Retinal degeneration in choroideremia: deficiency of rab geranylgeranyl transferase. Science. 1993;259:377-381.
5. Seabra MC, Brown MS, Slaughter CA, Sudhof TC, Goldstein JL. Purification of component A of Rab geranylgeranyl transferase: possible identity with the choroideremia gene product. Cell. 1992; 70:1049-1057.
6. Cremers FP, Molloy CM, van de Pol DJ, et al. An autosomal homologue of the choroideremia gene colocalizes with the Usher syndrome type II locus on the distal part of chromosome 1q. Hum Mol Genet. 1992;1:71-75.
7. Andres DA, Seabra MC, Brown MS, et al. cDNA cloning of component A of Rab geranylgeranyl transferase and demonstration of its role as a Rab escort protein. Cell. 1993;73:1091-1099.
8. Seabra MC, Wasmeier C. Controlling the location and activation of Rab GTPases. Curr Opin Cell Biol. 2004;16:451-457.
9. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2:107-117.
10. Casey PJ, Seabra MC. Protein prenyltransferases. J Biol Chem. 1996;271:5289-5292.
11. Desnoyers L, Anant JS, Seabra MC. Geranylgeranylation of Rab proteins. Biochem Soc Trans. 1996;24:699-703.
12. Seabra MC. New insights into the pathogenesis of choroideremia: a tale of two REPs. Ophthalmic Genet. 1996;17:43-46.
13. Seabra MC, Ho YK, Anant JS. Deficient geranylgeranylation of Ram/Rab27 in choroideremia. J Biol Chem. 1995;270:24420-24427.
14. Tolmachova T, Anders R, Abrink M, et al. Independent degeneration of photoreceptors and retinal pigment epithelium in conditional knockout mouse models of choroideremia. J Clin Invest. 2006;116:386-394.
15. van den Hurk JA, Hendriks W, van de Pol DJ, et al. Mouse choroideremia gene mutation causes photoreceptor cell degeneration and is not transmitted through the female germline. Hum Mol Genet. 1997;6:851-858.
16. Shi W, van den Hurk JA, Alamo-Bethencourt V, et al. Choroideremia gene product affects trophoblast development and vascularization in mouse extra-embryonic tissues. Dev Biol. 2004;272:53-65.
17. Goldsmith P, Harris WA. The zebrafish as a tool for understanding the biology of visual disorders. Semin Cell Dev Biol. 2003;14:11-18.
18. Starr CJ, Kappler JA, Chan DK, Kollmar R, Hudspeth AJ. Mutation of the zebrafish choroideremia gene encoding Rab escort protein 1 devastates hair cells. Proc Natl Acad Sci U S A. 2004;101:2572-2577.
19. Krock BL, Bilotta J, Perkins BD. Noncell-autonomous photoreceptor degeneration in a zebrafish model of choroideremia. Proc Natl Acad Sci U S A. 2007;104:4600-4605.
20. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio). 4th ed. Seattle: University of Oregon Press; 2000.
21. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203:253-310.
22. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403-410.
23. Bateman A, Coin L, Durbin R, et al. The Pfam protein families database. Nucleic Acids Res. 2004;32:D138-141.
24. Wilson D, Madera M, Vogel C, Chothia C, Gough J. The SUPERFAMILY database in 2007: families and functions. Nucleic Acids Res. 2007;35:D308-D313.
25. Pylypenko O, Rak A, Reents R, et al. Structure of Rab escort protein-1 in complex with Rab geranylgeranyltransferase. Mol Cell. 2003;11:483-494.
26. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876-4882.
27. Felsenstein J. PHYLIP-Phylogeny Inference Package (version 3. 2). Cladistics. 1989;5:164-166.
28. Schmitt EA, Dowling JE. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol. 1999;404:515-536.
29. Waldherr M, Ragnini A, Schweyer RJ, Boguski MS. MRS6-yeast homologue of the choroideraemia gene. Nat Genet. 1993;3:193-194.
30. Rasteiro R, Pereira-Leal JB. Multiple domain insertions and losses in the evolution of the Rab prenylation complex. BMC Evol Biol. 2007;7:140.
31. Halford S, Freedman MS, Bellingham J, et al. Characterization of a novel human opsin gene with wide tissue expression and identification of embedded and flanking genes on chromosome 1q43. Genomics. 2001;72:203-208.
32. BJ. Ancestry influences the fate of duplicated genes millions of years after polyploidization of clawed frogs (Xenopus). Genetics. 2007;176-1119-1130.
33. Evans BJ, Kelley DB, Tinsley RC, Melnick DJ, Cannatella DC. A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Mol Phylogenet Evol. 2004;33:197-213.
34. Pelegri F. Maternal factors in zebrafish development. Dev Dyn. 2003;228:535-554.
35. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A. 2004;101:12792-12797.
36. Driever W, Solnica-Krezel L, Schier AF, et al. A genetic screen for mutations affecting embryogenesis in zebrafish. Development. 1996;123:37-46.
37. Golling G, Amsterdam A, Sun Z, et al. Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development. Nat Genet. 2002;31:135-140.
38. Gross JM, Perkins BD, Amsterdam A, et al. Identification of zebrafish insertional mutants with defects in visual system development and function. Genetics. 2005;170:245-261.
39. Kane DA, Maischein HM, Brand M, et al. The zebrafish early arrest mutants. Development. 1996;123:57-66.
40. Wagner DS, Dosch R, Mintzer KA, Wiemelt AP, Mullins MC. Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev Cell. 2004;6:781-790.
41. Alory C, Balch WE. Molecular basis for Rab prenylation. J Cell Biol. 2000;150:89-103.
42. Alory C, Balch WE. Molecular evolution of the Rab-escort-protein/ guanine-nucleotide-dissociation-inhibitor superfamily. Mol Biol Cell. 2003;14:3857-3867.
43. Betran E, Emerson JJ, Kaessmann H, Long M. Sex chromosomes and male functions: where do new genes go? Cell Cycle. 2004;3: 873-875.
44. Emerson JJ, Kaessmann H, Betran E, Long M. Extensive gene traffic on the mammalian X chromosome. Science. 2004;303:537-540.
45. Vinckenbosch N, Dupanloup I, Kaessmann H. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci U S A. 2006;103:3220-3225.
46. Mankin AS, Liebman SW. Baby, don't stop! Nat Genet. 1999;23:8-10.
47. Welch EM, Barton ER, Zhuo J, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature. 2007;447:87-91.
48. Moosajee M, Gregory-Evans K, Ellis CD, Seabra MC, Gregory-Evans CY. Translational bypass of nonsense mutations in zebrafish rep1, pax2. 1 and lamb1 highlights a viable therapeutic option for untreatable genetic eye disease. Hum Mol Genet. 2008;17:3987-4000.