The Y99C mutation in guanylyl cyclase-activating protein 1 increases intracellular Ca2+ and causes photoreceptor degeneration in transgenic mice

Journal of Neuroscience

Volumn 24, Issue 27, 2004, Pages 6078-6085

  Olshevskaya, Elena V ^a   Calvert, Peter D ^b   Woodruff, Michael L ^c   Peshenko, Igor V ^a   Savchenko, Andrey B ^a   Makino, Clint L ^b   Ho, Ye Shih ^e   Fain, Gordon L ^c,d   Dizhoor, Alexander M ^a  

^a PENNSYLVANIA COLLEGE OF OPTOMETRY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JULES STEIN EYE INSTITUTE   (United States)

^e WAYNE STATE UNIVERSITY   (United States)

Author keywords

Calcium; Cone; Guanylyl cyclase; Photoreceptors; Retina; Retinal degeneration; Retinal dystrophy; Transgenic mice

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM ION; GUANYLATE CYCLASE; GUANYLATE CYCLASE ACTIVATING PROTEIN 1; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CONGENITAL BLINDNESS; CONTROLLED STUDY; CYCLIC NUCLEOTIDE GATED CHANNEL; DARK ADAPTATION; DARKNESS; GENE; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; GUCA1A GENE; ILLUMINATION; LASER MICROSCOPY; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DEGRADATION; RETINA CONE; RETINA DYSTROPHY; RETINA ROD; RETINA ROD OUTER SEGMENT; TRANSGENIC MOUSE; Y99C GCAP1 GENE;

AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; CALCIUM; CALCIUM-BINDING PROTEINS; CATTLE; CELL SEPARATION; DARK ADAPTATION; ELECTROPHYSIOLOGY; ELECTRORETINOGRAPHY; GUANYLATE CYCLASE; GUANYLATE CYCLASE-ACTIVATING PROTEINS; INTRACELLULAR FLUID; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION, MISSENSE; PHOTIC STIMULATION; PHOTORECEPTORS, VERTEBRATE; RECEPTORS, CELL SURFACE; RETINA; RETINAL DEGENERATION;

EID: 3042789501     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0963-04.2004     Document Type: Article

References (53)

1. Akhmedov NB, Piriev NI, Chang B, Rapoport AL, Hawes NL, Nishina PM, Nusinowitz S, Heckenlively JR, Roderick TH, Kozak CA, Danciger M, Davisson MT, Farber DB (2000) A deletion in a photoreceptor-specific nuclear receptor mRNA causes retinal degeneration in the rd7 mouse. Proc Natl Acad Sci USA 97:5551-5556.
2. Baylor DA, Nunn BJ (1986) Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. J Physiol (Lond) 371:115-145.
3. Baylor DA, Lamb TD, Yau K-W (1979a) The membrane current of single rod outer segments. J Physiol (Lond) 288:589-611.
4. Baylor DA, Lamb TD, Yau K-W (1979b) Responses of retinal rods to single photons. J Physiol (Lond) 288:613-634.
5. Brooks SP, Storey KB (1992) Bound and determined: a computer program for making buffers of defined ion concentrations. Anal Biochem 201:119-126.
6. Burns ME, Mendez A, Chen J, Baylor DA (2002) Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36:81-91.
7. Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, Heckenlively JR (2002) Retinal degeneration mutants in the mouse. Vision Res 42:517-526.
8. Dizhoor AM (2000) Regulation of cGMP synthesis in photoreceptors: role in signal transduction and congenital diseases of the retina. Cell Signal 12:711-719.
9. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB (1994) The human photoreceptor membrane guanylyl cyclase, retGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 12:1345-1352.
10. Dizhoor AM, Boikov SG, Olshevskaya EV (1998) Constitutive activation of photoreceptor guanylate cyclase by Y99C mutant of GCAP-1. Possible role in causing human autosomal dominant cone degeneration. J Biol Chem 273:17311-17314.
11. 2+, and photoreceptor death: new evidence for the equivalent-light hypothesis from arrestin knockout mice. Invest Ophthalmol Vis Sci 40:2770-2772.
12. Fain GL, Matthews HR, Cornwall MC, Koutalos Y (2001) Adaptation in vertebrate photoreceptors. Physiol Rev 81:117-151.
13. Garbers DL (1999) The guanylyl cyclase receptors. Methods 19:477-484.
14. Garbers DL, Lowe DG (1994) Guanylyl cyclase receptors. J Biol Chem 269:30741-30744.
15. Gillespie PG, Beavo JA (1989) cGMP is tightly bound to bovine retinal rod phosphodiesterase. Proc Natl Acad Sci USA 86:4311-4315.
16. Govardovskii VI, Berman AL (1981) Light-induced changes of cyclic GMP content in frog retinal rod outer segments measured with rapid freezing and microdissection. Biophys Struct Mech 7:125-130.
17. Gray-Keller MP, Detwiler PB (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13:849-861.
18. Haverkamp S, Wassle H (2000) Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
19. He L, Poblenz AT, Medrano CJ, Fox DA (2000) Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J Biol Chem 275:12175-12184.
20. Hurley JB, Dizhoor AM (2000) Heterologous expression and assays for photoreceptor guanylyl cyclases and guanylyl cyclase activating proteins. Methods Enzymol 315:708-717.
21. 2+ sensitivity. Eur J Biochem 270:3814-3821.
22. Kelsell RE, Gregory-Evans K, Payne AM, Perrault I, Kaplan J, Yang R-B, Garbers DL, Bird AC, Moore AT, Hunt DM (1998) Mutations in the retinal guanylate cyclase (RETGC-1) gene in dominant cone-rod dystrophy. Hum Mol Genet 7:1179-1184.
23. Kilbride P, Ebrey TG (1979) Light-initiated changes of cyclic guanosine monophosphate levels in the frog retina measured with quick-freezing techniques. J Gen Physiol 74:415-426.
24. Koch K-W, Stryer L (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334:64-66.
25. Krylov DM, Niemi GA, Dizhoor AM, Hurley JB (1999) Mapping sites in guanylyl cyclase activating protein-1 required for regulation of photoreceptor membrane guanylyl cyclases. J Biol Chem 274:10833-10839.
26. Lem J, Fain GL (2004) Constitutive opsin signaling: night blindness or retinal degeneration? Trends Mol Med 10:150-157.
27. Liu X, Seno K, Nishizawa Y, Hayashi F, Yamazaki A, Matsumoto H, Wakabayashi T, Usukura J (1994) Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Exp Eye Res 59:761-768.
28. Lyubarsky AL, Lem J, Chen J, Falsini B, Iannaccone A, Pugh Jr EN (2002) Functionally rodless mice: transgenic models for the investigation of cone function in retinal disease and therapy. Vision Res 42:401-415.
29. Ma J, Norton JC, Allen AC, Burns JB, Hasel KW, Burns JL, Sutcliffe JG, Travis GH (1995) Retinal degeneration slow (rds) in mouse results from simple insertion of a t haplotype-specific element into protein-coding exon II. Genomics 28:212-219.
30. Marks PW, Maxfield FR (1991) Preparation of solutions with free calcium concentration in the nanomolar range using 1,2-bis(o-aminophenoxy) ethane-N,N,N′,N′-tetraacetic acid. Anal Biochem 193:61-71.
31. McLaughlin ME, Ehrhart TL, Berson EL, Dryja TP (1995) Mutation spectrum of the gene encoding the β-subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc Natl Acad Sci USA 92:3249-3253.
32. Mendez A, Burns ME, Sokal I, Dizhoor AM, Baehr W, Palczewski K, Baylor DA, Chen J (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc Natl Acad Sci USA 98:9948-9953.
33. Olshevskaya EV, Hughes RE, Hurley JB, Dizhoor AM (1997) Calcium binding, but not a calcium-myristoyl switch, controls the ability of guanylyl cyclase-activating protein GCAP-2 to regulate photoreceptor guanylyl cyclase. J Biol Chem 272:14327-14333.
34. Olshevskaya EV, Ermilov AN, Dizhoor AM (2002) Factors that affect regulation of cGMP synthesis in vertebrate photoreceptors and their genetic link to human retinal degeneration. Mol Cell Biochem 230:139-147.
35. 2+-binding proteins in the retina: structure, function, and the etiology of human visual diseases. BioEssays 22:337-350.
36. Payne AM, Downes SM, Bessant DAR, Taylor R, Holder GE, Warren MJ, Bird AC, Bhattacharya SS (1998) A mutation in guanylate cyclase activator 1A (GUCA1A) in an autosomal dominant cone dystrophy pedigree mapping to a new locus on chromosome 6p21.1. Hum Mol Genet 7:273-277.
37. 2+ sensors: implications for photoreceptor guanylyl cyclase (retGC) regulation in mammalian photoreceptors. J Biol Chem 279:16903-16906.
38. Petersen-Jones SM (1998) Animal models of human retinal dystrophies. Eye 12:566-570.
39. Pittler SJ, Baehr W (1991) Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase β-subunit gene of the rd mouse. Proc Natl Acad Sci USA 88:8322-8326.
40. Pugh Jr EN, Duda T, Sitaramayya A, Sharma RK (1997) Photoreceptor guanylate cyclases: a review. Biosci Rep 17:429-473.
41. Ramamurthy V, Tucker C, Wilkie SE, Daggett V, Hunt DM, Hurley JB (2001) Interactions within the coiled-coil domain of RetGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity. J Biol Chem 276:26218-26229.
42. Raport CJ, Lem J, Makino C, Chen CK, Fitch CL, Hobson A, Baylor D, Simon MI, Hurley JB (1994) Downregulation of cGMP phosphodiesterase induced by expression of GTPase-deficient cone transducin in mouse rod photoreceptors. Invest Ophthalmol Vis Sci 35:2932-2947.
43. 2+ in salamander rods. J Gen Physiol 111:53-64.
44. 2+ concentration in salamander cone photoreceptors. J Gen Physiol 113:267-277.
45. Sokal I, Li N, Surgucheva I, Warren MJ, Payne AM, Bhattacharya SS, Baehr W, Palczewski K (1998) GCAP1 (Y99C) mutant is constitutively active in autosomal dominant cone dystrophy. Mol Cell 2:129-133.
46. 2+ with quin2. Methods Enzymol 172:230-262.
47. Tucker CL, Woodcock SC, Kelsell RE, Ramamurthy V, Hunt DM, Hurley JB (1999) Biochemical analysis of a dimerization domain mutation in RetGC-1 associated with dominant cone-rod dystrophy. Proc Natl Acad Sci USA 96:9039-9044.
48. Watanabe S-I, Matthews G (1988) Regional distribution of cGMP-activated ion channels in the plasma membrane of the rod photoreceptor. J Neurosci 8:2334-2337.
49. Wilkie SE, Newbold RJ, Deery E, Walker CE, Stinton I, Ramamurthy V, Hurley JB, Bhattacharya SS, Warren MJ, Hunt DM (2000) Functional characterization of missense mutations at codon 838 in retinal guanylate cyclase correlates with disease severity in patients with autosomal dominant cone-rod dystrophy. Hum Mol Genet 9:3065-3073.
50. Wilkie SE, Li Y, Deery EC, Newbold RJ, Garibaldi D, Bateman JB, Zhang H, Lin W, Zack DJ, Bhattacharya SS, Warren MJ, Hunt DM, Zhang K (2001) Identification and functional consequences of a new mutation (E155G) in the gene for GCAP1 that causes autosomal dominant cone dystrophy. Am J Hum Genet 69:471-480.
51. Woodford BJ, Chen J, Simon MI (1994) Expression of rhodopsin promoter transgene product in both rods and cones. Exp Eye Res 58:631-635.
52. Woodruff ML, Sampath AP, Matthews HR, Krasnoperova NV, Lem J, Fain GL (2002) Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice. J Physiol (Lond) 542:843-854.
53. Woodruff ML, Wang Z, Chung HY, Redmond TM, Fain GL, Lem J (2003) Spontaneous activity of opsin apoprotein is a cause of Leber congenital amaurosis. Nat Genet 35:158-164.