RGS Expression Rate-Limits Recovery of Rod Photoresponses

Neuron

Volumn 51, Issue 4, 2006, Pages 409-416

  Krispel, Claudia M ^a,b   Chen, Desheng ^c   Melling, Nathan ^a,b   Chen, Yu Jiun ^c   Martemyanov, Kirill A ^d   Quillinan, Nidia ^a,b   Arshavsky, Vadim Y ^d   Wensel, Theodore G ^e   Chen, Ching Kang ^c   Burns, Marie E ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^d MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE; RGS PROTEIN; RHODOPSIN KINASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; MAMMAL; MOUSE; NONHUMAN; PHOTOREACTIVITY; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETINA ROD; SIGNAL TRANSDUCTION; VISION;

ANIMALS; BLOTTING, WESTERN; GENE EXPRESSION; GTP-BINDING PROTEIN BETA SUBUNITS; LIGHT; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; PHOTIC STIMULATION; PHOTOTRANSDUCTION; RECOVERY OF FUNCTION; RETINA; RGS PROTEINS; RHODOPSIN KINASE; RODS (RETINA); TIME FACTORS;

EID: 33746898592     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.07.010     Document Type: Article

References (43)

1. Baylor D.A., Lamb T.D., and Yau K.W. Responses of retinal rods to single photons. J. Physiol. 288 (1979) 613-634
2. Burns M.E., Mendez A., Chen J., and Baylor D.A. Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36 (2002) 81-91
3. Burns M.E., Mendez A., Chen C.K., Almuete A., Quillinan N., Simon M.I., Baylor D.A., and Chen J. Deactivation of phosphorylated and nonphosphorylated rhodopsin by arrestin splice variants. J. Neurosci. 26 (2006) 1036-1044
4. Chen C.K., Inglese J., Lefkowitz R.J., and Hurley J.B. Ca(2+)-dependent interaction of recoverin with rhodopsin kinase. J. Biol. Chem. 270 (1995) 18060-18066
5. Chen C.K., Burns M.E., Spencer M., Niemi G.A., Chen J., Hurley J.B., Baylor D.A., and Simon M.I. Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc. Natl. Acad. Sci. USA 96 (1999) 3718-3722
6. Chen C.K., Burns M.E., He W., Wensel T.G., Baylor D.A., and Simon M.I. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403 (2000) 557-560
7. Chen C.K., Eversole-Cire P., Zhang H., Mancino V., Chen Y.J., He W., Wensel T.G., and Simon M.I. Instability of GGL domain-containing RGS proteins in mice lacking the G protein beta-subunit Gbeta5. Proc. Natl. Acad. Sci. USA 100 (2003) 6604-6609
8. Cowan C.W., Fariss R.N., Sokal I., Palczewski K., and Wensel T.G. High expression levels in cones of RGS9, the predominant GTPase accelerating protein of rods. Proc. Natl. Acad. Sci. USA 95 (1998) 5351-5356
9. Gold S.J., Heifets B.D., Pudiak C.M., Potts B.W., and Nestler E.J. Regulation of regulators of G protein signaling mRNA expression in rat brain by acute and chronic electroconvulsive seizures. J. Neurochem. 82 (2002) 828-838
10. Hamer R.D. Analysis of Ca++-dependent gain changes in PDE activation in vertebrate rod phototransduction. Mol. Vis. 6 (2000) 265-286
11. Hamer R.D., Nicholas S.C., Tranchina D., Liebman P.A., and Lamb T.D. Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. J. Gen. Physiol. 122 (2003) 419-444
12. He W., Cowan C.W., and Wensel T.G. RGS9, a GTPase accelerator for phototransduction. Neuron 20 (1998) 95-102
13. Heck M., and Hofmann K.P. Maximal rate and nucleotide dependence of rhodopsin-catalyzed transducin activation: initial rate analysis based on a double displacement mechanism. J. Biol. Chem. 276 (2001) 10000-10009
14. Hu G., and Wensel T.G. R9AP, a membrane anchor for the photoreceptor GTPase accelerating protein, RGS9-1. Proc. Natl. Acad. Sci. USA 99 (2002) 9755-9760
15. Ingi T., Krumins A.M., Chidiac P., Brothers G.M., Chung S., Snow B.E., Barnes C.A., Lanahan A.A., Siderovski D.P., Ross E.M., et al. Dynamic regulation of RGS2 suggests a novel mechanism in G-protein signaling and neuronal plasticity. J. Neurosci. 18 (1998) 7178-7188
16. Kawamura S. Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362 (1993) 855-857
17. Kennedy M.J., Sowa M.E., Wensel T.G., and Hurley J.B. Acceleration of key reactions as a strategy to elucidate the rate-limiting chemistry underlying phototransduction inactivation. Invest. Ophthalmol. Vis. Sci. 44 (2003) 1016-1022
18. Keresztes G., Martemyanov K.A., Krispel C.M., Mutai H., Yoo P.J., Maison S.F., Burns M.E., Arshavsky V.Y., and Heller S. Absence of the RGS9.Gbeta5 GTPase-activating complex in photoreceptors of the R9AP knockout mouse. J. Biol. Chem. 279 (2004) 1581-1584
19. Klenchin V.A., Calvert P.D., and Bownds M.D. Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J. Biol. Chem. 270 (1995) 16147-16152
20. Krispel C.M., Chen C.K., Simon M.I., and Burns M.E. Novel form of adaptation in mouse retinal rods speeds recovery of phototransduction. J. Gen. Physiol. 122 (2003) 703-712
21. Leskov I.B., Klenchin V.A., Handy J.W., Whitlock G.G., Govardovskii V.I., Bownds M.D., Lamb T.D., Pugh Jr. E.N., and Arshavsky V.Y. The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements. Neuron 27 (2000) 525-537
22. Li S., Chen D., Sauve Y., McCandless J., Chen Y.J., and Chen C.K. Rhodopsin-iCre transgenic mouse line for Cre-mediated rod-specific gene targeting. Genesis 41 (2005) 73-80
23. Lyubarsky A., Nikonov S., and Pugh Jr. E.N. The kinetics of inactivation of the rod phototransduction cascade with constant Ca2+i. J. Gen. Physiol. 107 (1996) 19-34
24. Makino C.L., Wen X.H., and Lem J. Piecing together the timetable for visual transduction with transgenic animals. Curr. Opin. Neurobiol. 13 (2003) 404-412
25. Makino C.L., Dodd R.L., Chen J., Burns M.E., Roca A., Simon M.I., and Baylor D.A. Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J. Gen. Physiol. 123 (2004) 729-741
26. Makino E.R., Handy J.W., Li T., and Arshavsky V.Y. The GTPase activating factor for transducin in rod photoreceptors is the complex between RGS9 and type 5 G protein beta subunit. Proc. Natl. Acad. Sci. USA 96 (1999) 1947-1952
27. Matthews H.R. Effects of lowered cytoplasmic calcium concentration and light on the responses of salamander rod photoreceptors. J. Physiol. 484 (1995) 267-286
28. Matthews H.R. Actions of Ca2+ on an early stage in phototransduction revealed by the dynamic fall in Ca2+ concentration during the bright flash response. J. Gen. Physiol. 109 (1997) 141-146
29. Mirnics K., Middleton F.A., Stanwood G.D., Lewis D.A., and Levitt P. Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia. Mol. Psychiatry 6 (2001) 293-301
30. Murnick J.G., and Lamb T.D. Kinetics of desensitization induced by saturating flashes in toad and salamander rods. J. Physiol. 495 (1996) 1-13
31. Nikonov S., Engheta N., and Pugh Jr. E.N. Kinetics of recovery of the dark-adapted salamander rod photoresponse. J. Gen. Physiol. 111 (1998) 7-37
32. Nikonov S., Lamb T.D., and Pugh Jr. E.N. The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse. J. Gen. Physiol. 116 (2000) 795-824
33. Nishiguchi K.M., Sandberg M.A., Kooijman A.C., Martemyanov K.A., Pott J.W., Hagstrom S.A., Arshavsky V.Y., Berson E.L., and Dryja T.P. Defects in RGS9 or its anchor protein R9AP in patients with slow photoreceptor deactivation. Nature 427 (2004) 75-78
34. Pepperberg D.R., Cornwall M.C., Kahlert M., Hofmann K.P., Jin J., Jones G.J., and Ripps H. Light-dependent delay in the falling phase of the retinal rod photoresponse. Vis. Neurosci. 8 (1992) 9-18
35. Rieke F., and Baylor D.A. Origin of reproducibility in the responses of retinal rods to single photons. Biophys. J. 75 (1998) 1836-1857
36. Sagoo M.S., and Lagnado L. G-protein deactivation is rate-limiting for shut-off of the phototransduction cascade. Nature 389 (1997) 392-395
37. Tekumalla P.K., Calon F., Rahman Z., Birdi S., Rajput A.H., Hornykiewicz O., Di Paolo T., Bedard P.J., and Nestler E.J. Elevated levels of DeltaFosB and RGS9 in striatum in Parkinson's disease. Biol. Psychiatry 50 (2001) 813-816
38. Traynor J.R., and Neubig R.R. Regulators of G protein signaling & drugs of abuse. Mol. Interv. 5 (2005) 30-41
39. Wang Z., Wen X.H., Ablonczy Z., Crouch R.K., Makino C.L., and Lem J. Enhanced shutoff of phototransduction in transgenic mice expressing palmitoylation-deficient rhodopsin. J. Biol. Chem. 280 (2005) 24293-24300
40. Watson A.J., Katz A., and Simon M.I. A fifth member of the mammalian G-protein beta-subunit family. Expression in brain and activation of the beta 2 isotype of phospholipase C. J. Biol. Chem. 269 (1994) 22150-22156
41. Whitlock G.G., and Lamb T.D. Variability in the time course of single photon responses from toad rods: termination of rhodopsin's activity. Neuron 23 (1999) 337-351
42. Xu J., Dodd R.L., Makino C.L., Simon M.I., Baylor D.A., and Chen J. Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389 (1997) 505-509
43. Zhang X., Wensel T.G., and Kraft T.W. GTPase regulators and photoresponses in cones of the eastern chipmunk. J. Neurosci. 23 (2003) 1287-1297