Replacing the rod with the cone transducin α subunit decreases sensitivity and accelerates response decay

Journal of Physiology

Volumn 588, Issue 17, 2010, Pages 3231-3241

  Chen, C K ^a   Woodruff, M L ^b   Chen, F S ^a   Shim, H ^a   Cilluffo, M C ^c   Fain, G L ^b,d  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; TRANSDUCIN; TRANSDUCIN ALPHA; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR; PHOSPHODIESTERASE VI; TRANSDUCIN ALPHA SUBUNIT;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA CONE; RETINA ROD; VISION; WILD TYPE; ANIMAL TISSUE; GNAT2C MOUSE; IMMUNOHISTOCHEMISTRY; KINETICS; MOUSE STRAIN; PHOTODYNAMICS; PHOTOSTIMULATION; PROTEIN ANALYSIS; WILD TYPE MOUSE;

ANIMALS; DOWN-REGULATION; EYE PROTEINS; GTP-BINDING PROTEIN ALPHA SUBUNITS; HETEROTRIMERIC GTP-BINDING PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOTIC STIMULATION; PROTEIN SUBUNITS; REACTION TIME; RETINAL CONE PHOTORECEPTOR CELLS; RETINAL ROD PHOTORECEPTOR CELLS; SENSITIVITY AND SPECIFICITY; TRANSDUCIN; UP-REGULATION;

EID: 77956275019     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2010.191221     Document Type: Article

References (39)

1. Baylor DA, Nunn BJ, Schnapf JL. Spectral sensitivity of cones of the monkey Macaca fascicularis. J Physiol 1987, 390:145-160.
2. Birnbaumer L. Expansion of signal transduction by G proteins. The second 15 years or so: from 3 to 16 α subunits plus βγ dimers. Biochim Biophys Acta 2007, 1768:772-793.
3. Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicolo M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh EN, Makino CL, Lem J. Phototransduction in transgenic mice after targeted deletion of the rod transducin α-subunit. Proc Natl Acad Sci U S A 2000, 97:13913-13918.
4. Carter-Dawson LD, Lavail MM. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 1979, 188:245-262.
5. Chen CK, Burns ME, He W, Wensel TG, Baylor DA, Simon MI. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 2000, 403:557-560.
6. Chen C-K, Woodruff ML, Chen FS, Chen D, Fain GL. Background light produces a recoverin-dependent modulation of activated-rhodopsin lifetime in mouse rods. J Neurosci 2010, 30:1213-1220.
7. Cowan CW, Fariss RN, Sokal I, Palczewski K, Wensel TG. High expression levels in cones of RGS9, the predominant GTPase accelerating protein of rods. Proc Natl Acad Sci U S A 1998, 95:5351-5356.
8. Deng WT, Sakurai K, Liu J, Dinculescu A, Li J, Pang J, Min SH, Chiodo VA, Boye SL, Chang B, Kefalov VJ, Hauswirth WW. Functional interchangeability of rod and cone transducin α-subunits. Proc Natl Acad Sci U S A 2009, 106:17681-17686.
9. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
10. Ebrey T, Koutalos Y. Vertebrate photoreceptors. Prog Retin Eye Res 2001, 20:49-94.
11. Fain GL, Dowling JE. Intracellular recordings from single rods and cones in the mudpuppy retina. Science 1973, 180:1178-1181.
12. Field GD, Rieke F. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 2002, 34:773-785.
13. Fu Y, Kefalov V, Luo DG, Xue T, Yau KW. Quantal noise from human red cone pigment. Nat Neurosci 2008, 11:565-571.
14. Gross OP, Burns ME. Control of rhodopsin's active lifetime by arrestin-1 expression in mammalian rods. J Neurosci 2010, 30:3450-3457.
15. Kefalov V, Fu Y, Marsh-Armstrong N, Yau KW. Role of visual pigment properties in rod and cone phototransduction. Nature 2003, 425:526-531.
16. Kefalov VJ, Estevez ME, Kono M, Goletz PW, Crouch RK, Cornwall MC, Yau KW. Breaking the covalent bond - a pigment property that contributes to desensitization in cones. Neuron 2005, 46:879-890.
17. Korenbrot JI. Ca2+ flux in retinal rod and cone outer segments: differences in Ca2+ selectivity of the cGMP-gated ion channels and Ca2+ clearance rates. Cell Calcium 1995, 18:285-300.
18. Krispel CM, Chen D, Melling N, Chen YJ, Martemyanov KA, Quillinan N, Arshavsky VY, Wensel TG, Chen CK, Burns ME. RGS expression rate-limits recovery of rod photoresponses. Neuron 2006, 51:409-416.
19. Lobanova ES, Finkelstein S, Song H, Tsang SH, Chen CK, Sokolov M, Skiba NP, Arshavsky VY. Transducin translocation in rods is triggered by saturation of the GTPase-activating complex. J Neurosci 2007, 27:1151-1160.
20. Ma J, Znoiko S, Othersen KL, Ryan JC, Das J, Isayama T, Kono M, Oprian DD, Corson DW, Cornwall MC, Cameron DA, Harosi FI, Makino CL, Crouch RK. A visual pigment expressed in both rod and cone photoreceptors. Neuron 2001, 32:451-461.
21. Mears AJ, Kondo M, Swain PK, Takada Y, Bush RA, Saunders TL, Sieving PA, Swaroop A. Nrl is required for rod photoreceptor development. Nat Genet 2001, 29:447-452.
22. Nikonov SS, Kholodenko R, Lem J, Pugh EN. Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J Gen Physiol 2006, 127:359-374.
23. Perry RJ, McNaughton PA. Response properties of cones from the retina of the tiger salamander. J Physiol 1991, 433:561-587.
24. Picones A, Korenbrot JI. Permeability and interaction of Ca2+ with cGMP-gated ion channels differ in retinal rod and cone photoreceptors. Biophys J 1995, 69:120-127.
25. Pugh EN, Lamb TD. Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1993, 1141:111-149.
26. Rieke F, Baylor DA. Origin and functional impact of dark noise in retinal cones. Neuron 2000, 26:181-186.
27. Rosenzweig DH, Nair KS, Wei J, Wang Q, Garwin G, Saari JC, Chen CK, Smrcka AV, Swaroop A, Lem J, Hurley JB, Slepak VZ. Subunit dissociation and diffusion determine the subcellular localization of rod and cone transducins. J Neurosci 2007, 27:5484-5494.
28. Sakurai K, Onishi A, Imai H, Chisaka O, Ueda Y, Usukura J, Nakatani K, Shichida Y. Physiological properties of rod photoreceptor cells in green-sensitive cone pigment knock-in mice. J Gen Physiol 2007, 130:21-40.
29. Sampath AP, Matthews HR, Cornwall MC, Bandarchi J, Fain GL. Light-dependent changes in outer segment free Ca2+ concentration in salamander cone photoreceptors. J Gen Physiol 1999, 113:267-277.
30. Schnapf JL, Nunn BJ, Meister M, Baylor DA. Visual transduction in cones of the monkey Macaca fascicularis. J Physiol 1990, 427:681-713.
31. Shi G, Yau KW, Chen J, Kefalov VJ. Signaling properties of a short-wave cone visual pigment and its role in phototransduction. J Neurosci 2007, 27:10084-10093.
32. Tachibanaki S, Arinobu D, Shimauchi-Matsukawa Y, Tsushima S, Kawamura S. Highly effective phosphorylation by G protein-coupled receptor kinase 7 of light-activated visual pigment in cones. Proc Natl Acad Sci U S A 2005, 102:9329-9334.
33. Tachibanaki S, Tsushima S, Kawamura S. Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses. Proc Natl Acad Sci U S A 2001, 98:14044-14049.
34. Tsang SH, Woodruff ML, Chen CK, Yamashita CY, Cilluffo MC, Rao AL, Farber DB, Fain GL. GAP-independent termination of photoreceptor light response by excess γ subunit of the c-GMP-phosphodiesterase. J Neurosci 2006, 26:4472-4480.
35. Tsang SH, Woodruff ML, Janisch KM, Cilluffo MC, Farber DB, Fain GL. Removal of phosphorylation sites of γ subunit of phosphodiesterase 6 alters rod light response. J Physiol 2007, 579:303-312.
36. Woodruff ML, Janisch KM, Peshenko IV, Dizhoor AM, Tsang SH, Fain GL. Modulation of phosphodiesterase6 turnoff during background illumination in mouse rod photoreceptors. J Neurosci 2008, 28:2064-2074.
37. Woodruff ML, Olshevskaya EV, Savchenko AB, Peshenko IV, Barrett R, Bush RA, Sieving PA, Fain GL, Dizhoor AM. Constitutive excitation by Gly90Asp rhodopsin rescues rods from degeneration caused by elevated production of cGMP in the dark. J Neurosci 2007, 27:8805-8815.
38. Zhang K, Howes KA, He W, Bronson JD, Pettenati MJ, Chen C, Palczewski K, Wensel TG, Baehr W. Structure, alternative splicing, and expression of the human RGS9 gene. Gene 1999, 240:23-34.
39. Zhang X, Wensel TG, Kraft TW. GTPase regulators and photoresponses in cones of the eastern chipmunk. J Neurosci 2003, 23:1287-1297.