Mutation of cGMP phosphodiesterase 6α′-subunit gene causes progressive degeneration of cone photoreceptors in zebrafish

Mechanisms of Development

Volumn 125, Issue 11-12, 2008, Pages 932-946

  Nishiwaki, Yuko ^a,b   Komori, Atsuko ^b   Sagara, Hiroshi ^c   Suzuki, Emiko ^c   Manabe, Tomonori ^d   Hosoya, Toshihiko ^d   Nojima, Yasuhiro ^d   Wada, Hironori ^d   Tanaka, Hideomi ^d   Okamoto, Hitoshi ^d   Masai, Ichiro ^a,b  

^a Okinawa Institute of Science and Technology Promotion Corporation   (Japan)

^b INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

cGMP phosphodiesterase 6; Cone; Degeneration; Mutant; Photoreceptor; Phototransduction; Proliferation; Retina; Rod; Zebrafish

Indexed keywords

CYCLIC GMP; ESTERASE; PHOSPHODIESTERASE 6 ALPHA; UNCLASSIFIED DRUG;

ARTICLE; DEGENERATION; GENE EXPRESSION; GENE MUTATION; MISSENSE MUTATION; MOLECULAR CLONING; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTOKINETIC STIMULATION; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RETINA CONE; VISUAL IMPAIRMENT; ZEBRA FISH;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 6; GENE EXPRESSION REGULATION; HUMANS; LIGHT SIGNAL TRANSDUCTION; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; SEQUENCE HOMOLOGY, AMINO ACID; VISION, OCULAR; ZEBRAFISH;

DANIO RERIO; MAMMALIA;

EID: 55249100207     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2008.09.001     Document Type: Article

References (64)

1. Aguirre G., Farber D., Lolley R., Fletcher R.T., and Chader G.J. Rod-cone dysplasia in Irish setters: a defect in cyclic GMP metabolism in visual cells. Science 201 (1978) 1133-1134
2. Allwardt B.A., Lall A.B., Brockerhoff S.E., and Dowling J.E. Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant. J. Neurosci. 21 (2001) 2330-2342
3. Aravind L., and Ponting C.P. The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22 (1997) 458-459
4. Besch D., Jägle H., Scholl H.P.N., Seeliger M.W., and Zrenner E. Inherited multifocal RPE-diseases: mechanisms for local dysfunction in global retinoid cycle gene defects. Vision Res. 43 (2003) 3095-3108
5. Bernardos R.L., Barthel L.K., Meyers J.R., and Raymond P.A. Late-stage neuronal progenitors in the retina are radial Müller glia that function as retinal stem cells. J. Neurosci. 27 (2007) 7028-7040
6. Bilotta J., Saszik S., and Sutherland S.E. Rod contributions to the electroretinogram of the dark-adapted developing zebrafish. Dev. Dyn. 222 (2001) 564-570
7. Brockerhoff S.E., Hurley J.B., Janssen-Bienhold U., Neuhauss S.C.F., Driever W., and Dowling J.E. A behavioral screen for isolating zebrafish mutants with visual system defects. Proc. Natl. Acad. Sci. USA 92 (1995) 10545-10549
8. Brockerhoff S.E., Dowling J.E., and Hurley J.B. Zebrafish retinal mutants. Vision Res. 38 (1998) 1335-1339
9. 2+ and suppression of current in cones from the zebrafish mutant nof. J. Neurosci. 23 (2003) 470-480
10. Burns M.E., and Arshavsky V.Y. Beyond counting photons: trials and trends in vertebrate visual transduction. Neuron 48 (2005) 387-401
11. Cote R.H., Bownds M.D., and Arshavsky V.Y. cGMP binding sites on photoreceptor phosphodiesterase: role in feedback regulation of visual transduction. Proc. Natl. Acad. Sci. USA 91 (1994) 4845-4849
12. D'Amours M.R., and Cote R.H. Regulation of photoreceptor phosphodiesterase catalysis by its non-catalytic cGMP-binding sites. Biochem. J. 340 (1999) 863-869
13. Danciger M., Blaney J., Gao Y.Q., Zhao D.Y., Heckenlively J.R., Jacobson S.G., and Farber D.B.F. Mutations in the PDE6B gene in autosomal recessive retinitis pigmentosa. Genomics 30 (1995) 1-7
14. Doerre G., and Malicki J. Genetic analysis of photoreceptor cell development in the zebrafish retina. Mech. Dev. 110 (2002) 125-138
15. Dryja T.P., Rucinski D.E., Chen S.H., and Berson E.L. Frequency of mutations in the gene encoding the α subunit of rod cGMP-phosphodiesterase in autosomal recessive retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 40 (1999) 1859-1865
16. Eley L., Yates L.M., and Goodship J.A. Cilia and disease. Curr. Opin. Genet. Dev. 15 (2005) 308-314
17. Emran F., Rihel J., Adolph A.R., Wong K.Y., Kraves S., and Dowling J.E. OFF ganglion cells cannot drive the optokinetic reflex in zebrafish. Proc. Natl. Acad. Sci. USA 104 (2007) 19126-19131
18. Gao Y.Q., Danciger M., Longmuir R., Piriev N.I., Zhao D.Y., Heckenlively J.R., Fishman G.A., Weleber R.G., Jacobson S.G., Stone E.M., and Farber D.B. Screening of the gene encoding the α′-subunit of cone cGMP-PDE in patients with retinal degenerations. Invest. Ophthalmol. Vis. Sci. 40 (1999) 1818-1822
19. Gal A., Orth U., Baehr W., Schwinger E., and Rosenberg T. Heterozygous missense mutation in the rod cGMP phosphodiesterase β-subunit gene in autosomal dominant stationary night blindness. Nat. Genet. 7 (1994) 64-68
20. Gross J.M., Perkins B.D., Amsterdam A., Egaña A., Darland T., Matsui J.I., Sciascia S., Hopkins N., and Dowling J.E. Identification of zebrafish insertional mutants with defects in visual system development and function. Genetics 170 (2005) 245-261
21. -/-mice: cone bipolar cells react on the missing cone input and form ectopic synapses with rods. J. Neurosci. 26 (2006) 5248-5255
22. Huang D., Hinds T.R., Martinez S.E., Doneanu C., and Beavo J.A. Molecular determinants of cGMP binding to chicken cone photoreceptor phosphodiesterase. J. Biol. Chem. 279 (2004) 48143-48151
23. Huang S.H., Pittler S.J., Huang X., Oliveria L., Berson E.L., and Dryja T.P. Autosomal recessive retinitis pigmentosa caused by mutations in the α subunit of rod cGMP phosphodiesterase. Nat. Genet. 11 (1995) 468-471
24. Johns P.R., and Fernald R.D. Genesis of rods in teleost fish retina. Nature 293 (1981) 141-142
25. Kennan A., Aherne A., and Humphries P. Light in retinitis pigmentosa. Trends Genet. 21 (2005) 103-110
26. Larison K.D., and BreMiller R. Early onset of phenotype and cell patterning in the embryonic zebrafish retina. Development 109 (1990) 567-576
27. Lolley R.N., Farber D.B., Rayborn M.E., and Hollyfield J.G. Cyclic GMP accumulation causes degeneration of photoreceptor cells: simulation of an inherited disease. Science 196 (1976) 664-666
28. Malicki J., Neuhauss S.C.F., Schier A.F., Solnica-Krezel L., Stemple D.L., Stainier D.Y.R., Abdelilah S., Zwartkruis F., Rangini Z., and Driever W. Mutations affecting development of the zebrafish retina. Development 123 (1996) 263-273
29. Masai I., Lele Z., Yamaguchi M., Komori A., Nakata A., Nishiwaki Y., Wada H., Tanaka H., Nojima Y., Hammerschmidt M., Wilson S.W., and Okamoto H. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neuritis. Development 130 (2003) 2479-2494
30. McLaughlin M.E., Sandberg M.A., Berson E.L., and Dryja T.P. Recessive mutations in the gene encoding the β-subunit of rod phosphodiesterase in patients with retinitis pigmentosa. Nat. Genet. 4 (1993) 130-134
31. McLaughlin M.E., Ehrhart T.L., Berson E.L., and Dryja T.P. Mutation spectrum of the gene encoding the β subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc. Natl. Acad. Sci. USA 92 (1995) 3249-3253
32. Morris A.C., Scholz T.L., Brockerhoff S.E., and Fadool J.M. Genetic dissection reveals two separate pathways for rod and cone regeneration in the teleost retina. Dev. Neurobiol. 68 (2008) 605-619
33. Muradov K.G., Boyd K.K., Martinez S.E., Beavo J.A., and Artemyev N.O. The GAFa domains of rod cGMP-phosphodiesterase 6 determine the selectivity of the enzyme dimerization. J. Biol. Chem. 278 (2003) 10594-10601
34. Muradov K.G., Granovsky A.E., and Artemyev N.O. Mutation in rod PDE6 linked to congenital stationary night blindness impairs the enzyme inhibition by its γ-subunit. Biochemistry 42 (2003) 3305-3310
35. Muto A., Orger M.B., Wehman A.M., Smear M.C., Kay J.N., Page-McCaw P.S., Gahtan E., Xiao T., Nevin L.M., Grosse N.J., Staub W., Finger-Baier K., and Baier H. Forward genetic analysis of visual behavior in zebrafish. PLoS Genet. 1 (2005) 575-588
36. Neuhauss S.C.F., Biehlmaier O., Seeliger M.W., Das T., Kohler K., Harris W.A., and Baier H. Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish. J. Neurosci. 19 (1999) 8603-8615
37. Omori Y., Zhao C., Saras A., Mukhopadhyay S., Kim W., Furukawa T., Sengupta P., Veraksa A., and Malicki J. elipsa is an early determinant of ciliogenesis that links the IFT particle to membrane-associated small GTPase Rab8. Nat. Cell Biol. 10 (2008) 437-444
38. Otteson D.C., and Hitchcock P.F. Stem cells in the teleost retina: persistent neurogenesis and injury-induced regeneration. Vision Res. 43 (2003) 927-936
39. Pacione L.R., Szego M.J., Ikeda S., Nishina P.M., and McInnes R.R. Progress toward understanding the genetic and biochemical mechanisms of inherited photoreceptor degenerations. Annu. Rev. Neurosci. 26 (2003) 657-700
40. Paquet-Durand F., Azadi S., Hauck S.M., Ueffing M., van Veen T., and Ekström P. Calpain is activated in degenerating photoreceptor in the rd1 mouse. J. Neurochem. 96 (2006) 802-814
41. Paquet-Durand F., Silva J., Talukdar T., Johnson L.E., Azadi S., van Veen T., Ueffing M., Hauck S.M., and Ekström P.A.R. Excessive activation of poly (ADP-ribose) polymerase contributes to inherited photoreceptor degeneration in the retinal degeneration 1 mouse. J. Neurosci. 27 (2007) 10311-10319
42. Rattner A., Sun H., and Nathans J. Molecular genetics of human retinal disease. Annu. Rev. Genet. 33 (1999) 89-131
43. Raymond P.A., Barthel L.K., Rounsifer M.E., Sullivan S.A., and Knight J.K. Expression of rod and cone visual pigments in goldfish and zebrafish: a rhodopsin-like gene is expressed in cones. Neuron 10 (1993) 1161-1174
44. Read D.S., McCall M.A., and Gregg R.G. Absence of voltage-dependent calcium channels delays photoreceptor degeneration in rd mice. Exp. Eye Res. 75 (2002) 415-420
45. Reynolds E.S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17 (1963) 208-212
46. Ridge K.D., Abdulaev N.G., Sousa M., and Palczewski K. Phototransduction: crystal clear. Trends Biochem. Sci. 28 (2003) 479-487
47. Sahel J.A., Mohand-Said S., Léveillard T., Hicks D., Picaud S., and Dreyfus H. Rod-cone interdependence: implications for therapy of photoreceptor cell diseases. Prog. Brain Res. 131 (2001) 649-661
48. Sanges D., Comitato A., Tammaro R., and Marigo V. Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc. Natl. Acad. Sci. USA 103 (2006) 17366-17371
49. Schmitt E.A., and Dowling J.E. Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J. Comp. Neurol. 404 (1999) 515-536
50. Seeliger M.W., Biesalski H.K., Wissinger B., Gollnick H., Gielen S., Frank J., Beck S., and Zrenner E. Phenotype in retinol deficiency due to a hereditary defect in retinol binding protein synthesis. Invest. Opthal. Vis. Sci. 40 (1999) 3-11
51. Seeliger M.W., Rilk A., and Neuhauss S.C. Ganzfeld ERG in zebrafish larvae. Doc. Ophthalmol. 104 (2002) 57-68
52. Sharma A.K., and Rohrer B. Sustained elevation of intracellular cGMP causes oxidative stress triggering calpain-mediated apoptosis in photoreceptor degeneration. Curr. Eye Res. 32 (2007) 259-269
53. Solnica-Krezel L., Schier A.F., and Driever W. Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 136 (1994) 1401-1420
54. Stearns G., Evangelista M., Fadool J.M., and Brockerhoff S.E. A mutation in the cone-specific pde6 gene causes rapid cone photoreceptor degeneration in zebrafish. J. Neurosci. 27 (2007) 13866-13874
55. Tsang S.H., Gouras P., Yamashita C.K., Kjeldbye H., Fisher J., Farber D.B., and Goff S.P. Retinal degeneration in mice lacking the γ subunit of the rod cGMP phosphodiesterase. Science 272 (1996) 1026-1029
56. Tsujikawa M., and Malicki J. Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42 (2004) 703-716
57. Tsujikawa M., and Malicki J. Genetics of photoreceptor development and function in zebrafish. Int. J. Dev. Biol. 48 (2004) 925-934
58. Van Epps H.A., Hayashi M., Lucast L., Stearns G.W., Hurley J.B., De Camilli P., and Brockerhoff S.E. The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. J. Neurosci. 24 (2004) 8641-8650
59. Vihtelic T.S., Doro C.J., and Hyde D.R. Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Vis. Neurosci. 16 (1999) 571-585
60. Westerfield M. The Zebrafish Book: a Guide for the Laboratory use of Zebrafish (Brachydanio rerio) (1995), University of Oregon, Eugene, Oregon
61. Williams D.S. Transport to the photoreceptor outer segment by myosin VIIa and kinesin II. Vision Res. 42 (2002) 455-462
62. Woodruff M.L., Olshevskaya E.V., Savchenko A.B., Peshenko I.V., Barrett R., Bush R.A., Sieving P.A., Fain G.L., and Dizhoor A.M. Constitutive excitation by Gly90Asp rhodopsin rescues rods from degeneration caused by elevated production of cGMP in the dark. J. Neurosci. 27 (2007) 8805-8815
63. Yang R.B., Robinson S.W., Xiong W.H., Yau K.W., Birch D.G., and Garbers D.L. Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. J. Neurosci. 19 (1999) 5889-5897
64. Zoraghi R., Corbin J.D., and Francis S.H. Properties and functions of GAF domains in cyclic nucleotide phosphodieseterases and other proteins. Mol. Pharmacol. 65 (2004) 267-278