Photoreceptors of Nrl-/- mice coexpress functional S-and M-cone opsins having distinct inactivation mechanisms

Journal of General Physiology

Volumn 125, Issue 3, 2005, Pages 287-304

  Nikonov, Sergei S ^a   Daniele, Lauren L ^a   Zhu, Xuemei ^b   Craft, Cheryl M ^b   Swaroop, Anand ^c   Pugh Jr , Edward N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Cone opsin; GPCR signaling; Grk1; Phototransduction; Spectral sensitivity

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE; LEUCINE ZIPPER PROTEIN; OPSIN; VISUAL PIGMENT;

ANIMAL TISSUE; ARTICLE; MAMMAL; MOUSE STRAIN; NONHUMAN; PHOTORECEPTOR; PHOTOTRANSDUCTION; PROTEIN FUNCTION; RETINA ROD; RETINA ROD OUTER SEGMENT; WAVEFORM;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CONES (RETINA); DNA-BINDING PROTEINS; ELECTROPHYSIOLOGY; EYE PROTEINS; KINETICS; MICE; MICE, KNOCKOUT; OPSIN; PHOTIC STIMULATION; PHOTORECEPTORS, VERTEBRATE; PROTEIN KINASES; RHO GTP-BINDING PROTEINS; RHODOPSIN KINASE; RODS (RETINA); TIME FACTORS; TISSUE DISTRIBUTION;

EID: 15244342823     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.200409208     Document Type: Article

References (72)

1. Ahnelt, P.K. 1998. The photoreceptor mosaic. Eye. 12:531-540.
2. Applebary, M.L., M.P. Antoch, L.C. Baxter, L.L. Chun, J.D. Falk, F. Farhangfar, K. Kage, M.G. Krystolik, L.A. Lyass, and J.T. Robbins, 2000. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron. 27:513-523.
3. Baylor, D.A., T.D. Lamb, and K.-W. Yau. 1979a. Responses of retinal rods to single photons. J. Physiol. 288:613-634.
4. Baylor, D.A., T.D. Lamb, and K.-W. Yan. 1979b. The membrane current of single rod outer segments. J. Physiol. 288:589-611.
5. Baylor, D.A., B.J. Nunn, and J.L. Schnapf. 1984. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. 357:570-607.
6. Blanks, J.C., G.S. Hageman, L.V. Johnson, and C. Spee. 1988. Ultrastructural visualization of primate cone photoreceptor matrix sheaths. J. Comp. Neurol. 270:288-300.
7. Blanks, J.C., and L.V. Johnson. 1983. Selective lectin binding of the developing mouse retina. J. Comp. Neurol. 221:31-41.
8. Burkhardt, D.A. 1994. Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. J. Neurosci. 14:1091-1105.
9. Burns, M.E., A. Mendez, J. Chen, and D.A. Baylor. 2002. Dynamics of cyclic GMP synthesis in retinal rods. Neuron. 36:81-91.
10. Cacnepeel, S., G. Charydczak, S. Sudarsanam, T. Hunter, and G. Manning. 2004. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl. Acad. Sci. USA. 101:11707-11712.
11. Calvert, P.D., V.I. Govardovskii, N. Krasnoperova, R.E. Anderson, J. Lem, and C.L. Makino. 2001. Membrane protein diffusion sets the speed of rod phototransduction. Nature. 411:90-94.
12. Calvert, P.D., N.V. Krasnoperova, A.L. Lyubarsky, T. Isayama, M. Nicolo, B. Kosaras, G. Wong, K.S. Gannon, R.F. Margolskee, R.L. Sidman, et al. 2000. Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha-subunit. Proc. Natl. Acad. Sci. USA. 97:13913-13918.
13. Carter-Dawson, L.D., and M.M. LaVail. 1979. Rods and cones in the mouse retina. 1. Structural analysis using light and electron microscopy. J. Comp. Neurol. 188:245-262.
14. Chen, C.K., M.E. Burns, W. He, T.G. Wensel, D.A. Baylor, and M.I. Simon. 2000. Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature. 403:557-560.
15. Chen, C.K., M.E. Burns, M. Spencer, G.A. Niemi, J. Chen, J.B. Hurley, D.A. Baylor, and M.I. Simon. 1999. Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc. Natl. Acad. Sci. USA. 96:3718-3722.
16. Chen, C.K., R. Zhang, J. Church-Kopish, W. Huang, H. Zhang, Y.J. Chen, J.M. Frederick, and W. Baehr. 2001. Characterization of human GRK7 as a potential cone opsin kinase. Mol. Vis. 7:305-313.
17. Chen, J., C.L. Makino, N.S. Peachey, D.A. Baylor, and M.I. Simon. 1995. Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science. 267(5196):374-377.
18. Cobbs, W.H., and E.N. Pugh Jr. 1987. Kinetics and components of the flash photocurrent of isolated retinal rods of the larval salamander, Ambystoma tigrinum. J. Physiol. 394:529-572.
19. Cornish, E.E., M. Xiao, Z. Yang, J.M. Provis, and A.E. Hendrickson. 2004. The role of opsin expression and apoptosis in determination of cone types in human retina. Exp. Eye Res. 78:1143-1154.
20. Daniele, L.L., C. Lillo, A.L. Lyubarsky, S.S. Nikonov., N. Philp, A.J. Mears, A. Swaroop, D.S. Williams, and E.N. Pugh Jr. 2005. Cone-like morphological, molecular and electrophysiological features of the photoreceptors of the Nrl knockout mouse. Investigative Ophthalmology and Visual Science. In press.
21. Dkhissi-Benyahya, O., A. Szel, W.J. Degrip, and H.M. Cooper. 2001. Short and mid-wavelength cone distribution in a nocturnal Strepsirrhine primate (Microcebus murinus). J. Comp. Neurol. 438:490-504.
22. Ebrey, T., and Y. Koutalos. 2001. Vertebrate photoreceptors. Prog. Retin. Eye Res. 20:49-94.
23. Fei, Y., and T.E. Hughes. 2001. Transgenic expression of the jellyfish green fluorescent protein in the cone photoreceptors of the mouse. Vis. Neurosci. 18:615-623.
24. Gillespie, P.G. 1990. Phosphodiesterases in visual transduction by rods and cones. In Cyclic Nucleotide Phosphodiesterases: Structure, Regulation and Drug Action. J. Beavo and M.D. Houslay, editors. Wiley, New York. 163-184.
25. Gillespie, P.G., and J.A. Beavo. 1988. Characterization of a bovine cone photoreceptor phosphodiesterase purified by cyclic GMP-sepharose chromatography. J. Biol. Chem. 263:8133-8141.
26. Govardovskii, V.I., N. Fyhrquist, T. Reuter, D.G. Kuzmin, and K. Donner. 2000. In search of the visual pigment template. Vis. Neurosci. 17:509-528.
27. Hageman, G.S., M.F. Marmor, X.Y. Yao, and L.V. Johnson. 1995. The interphotoreceptor matrix mediates primate retinal adhesion. Arch. Ophthalmol. 113:655-660.
28. Hagins, W.A., R.D. Penn, and S. Yoshikami. 1970. Dark current and photocurrent in retinal rods. Biophys. J. 10:380-412.
29. Harosi, F.I. 1982. Polarized microspectrophotometry for pigment orientation and concentration. Methods Enzymol. 81:642-647.
30. Hendrickson, A., and D. Hicks. 2002. Distribution and density of medium- and short-wavelength selective cones in the domestic pig retina. Exp. Eye Res. 74:435-444.
31. Howes, K.A., M.E. Pennesi, I, Sokal, J. Church-Kopish, B. Schmidt, D. Margolis, J.M. Frederick, F. Rieke, K. Palczewski, S.M. Wu, et al. 2002. GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO J. 21:1545-1554.
32. Jacobs, G.H., G.A. Williams, and J.A. Fenwick. 2004. Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res. 44:1615-1622.
33. Johnson, L.V., G.S. Hageman, and J.C. Blanks. 1986. Interphotoreceptor matrix domains ensheath vertebrate cone photoreceptor cells. Invest. Ophthalmol. Vis. Sci. 27:129-135.
34. Kraft, T.W. 1988. Photocurrents of cone photoreceptors of the golden-mantled ground squirrel. J. Physiol. 404:199-213.
35. Lamb, T.D. 1995. Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res. 35:3083-3091.
36. Lamb, T.D., and E.N. Pugh Jr. 1992. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J. Physiol. 449:719-758.
37. Lem, J., N.V. Krasnoperova, P.D. Calvert, B. Kosaras, D.A. Cameron, M. Nicolo, C.L. Makino, and R.L. Sidman. 1999. Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc. Natl. Acad. Sci. USA. 96:736-741.
38. Leskov, I.B., V.A. Klenchin, J.W. Handy, G.G. Whitlock, V.I. Govardovskii, M.D. Bownds, T.D. Lamb, E.N. Pugh Jr., and V.Y. Arshavsky. 2000. The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements. Neuron. 27:525-537.
39. Liebman, P.A. 1972. Microspectrophotometry of photoreceptors. In Handbook of Sensory Physiology. H.J.A. Dartnall, editor. Springer, New York. 481-528.
40. Lukats, A., O. Dkhissi-Benyahya, Z. Szepessy, P. Rohlich, B. Vigh, N.C. Bennett, H.M. Cooper, and A. Szel. 2002. Visual pigment co-expression in all cones of two rodents, the Siherian hamster, and the pouched mouse. Invest. Ophthalmol. Vis. Sci. 43:2468-2473.
41. Lyubarsky, A.L., C. Chen, M.I. Simon, and E.N. Pugh Jr. 2000. Mice lacking G-protein receptor kinase 1 have profoundly slowed recovery of cone-driven retinal responses. J. Neurosci. 20:2209-2217.
42. Lyubarsky, A.L., B. Falsini, M.E. Pennesi, P. Valentini, and E.N. Pugh Jr. 1999. UV- and midwave-sensitive cone-driven retinal responses of the mouse: a possible phenotype for coexpression of cone photopigments. J. Neurosci. 19:442-455.
43. Lyubarsky, A.L., F. Naarendorp, X. Zhang, T. Wensel, M.I. Simon, and E.N. Pugh Jr. 2001. RGS9-1 is required for normal inactivation of mouse cone phototransduction. Mol. Vis. 7:71-78.
44. Lyubarsky, A.L., L.L. Daniele, and E.N. Pugh. 2004. From candelas to photoisomerizations in the mouse eye by rhodopsin bleaching in situ and the light-rearing dependence of the major components of the mouse ERG. Vision Research. 44:3235-3251.
45. Makino, C.L., and R.L. Dodd. 1996. Multiple visual pigments in a photoreceptor of the salamander retina. J. Gen. Physiol. 108:27-34.
46. Mears, A.J., M. Kondo, P.K. Swain, Y. Takada, R.A. Bush, T.L. Saunders, P.A. Sieving, and A. Swaroop. 2001. Nrl is required for rod photoreceptor development. Nat. Genet. 29:447-452.
47. Mendez, A., M.E. Burns, A. Roca, J. Lem, L.W. Wu, M.I. Simon, D.A. Baylor, and J. Chen. 2000. Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron. 28:153-164.
48. Mendez, A., M.E. Burns, I. Sokal, A.M. Dizhoor, W. Baehr, K. Palczewski, D.A. Baylor, and J. Chen. 2001. Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc. Natl. Acad. Sci. USA. 98:9948-9953.
49. Nikonov, S., N. Engheta, and E.N. Pugh Jr. 1998. Kinetics of recovery of the dark-adapted salamander rod photoresponse. J. Gen. Physiol. 111:7-37.
50. Okano, T., Y. Fukada, Y. Shichida, and T. Yoshizawa. 1992. Photosensitivities of iodopsin and rhodopsins. Photochem. Photobiol. 56: 995-1001.
51. Paupoo, A.A., O.A. Mahroo, C. Friedburg, and T.D. Lamb. 2000. Human cone photoreceptor responses measured by the electroretinogram a-wave during and after exposure to intense illumination. J. Physiol. 529:469-482.
52. Pennesi, M.E., K.A. Howes, W. Baehr, and S.M. Wu. 2003. Guanylate cyclase-activating protein (GCAP) 1 rescues cone recovery kinetics in GCAP1/GCAP2 knockout mice. Proc. Natl. Acad. Sci. USA. 100:6783-6788.
53. Pepperberg, D.R., J. Jin, and G.J. Jones. 1994. Modulation of transduction gain in light adaptation of retinal rods. Vis. Neurosci. 11: 53-62.
54. Pierce, E.A. 2001. Pathways to photoreceptor cell death in inherited retinal degenerations. Bioessays. 23:605-618.
55. Pugh, E.N., Jr., and T.D. Lamb. 1993. Amplification and kinetics of the activation steps in phototransduction. Biochim. Biophys. Acta. 1141:111-149.
56. Pugh, E.N., Jr., S. Nikonov, and T.D. Lamb. 1999. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr. Opin. Neurobiol. 9:410-418.
57. Rohlich, P., T. van Veen, and A. Szel. 1994. Two different visual pigments in one retinal cone cell. Neuron. 13:1159-1166.
58. Saari, J.C., M. Nawrot, B.N. Kennedy, G.G. Garwin, J.B. Hurley, J. Huang, D.E. Possin, and J.W. Crabb. 2001. Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron. 29: 739-748.
59. Schnapf, J.L., B.J. Nunn, M. Meister, and D.A. Baylor. 1990. Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. 427:681-713.
60. Smith, N.P., and T.D. Lamb. 1997. The a-wave of the human electroretinogram recorded with a minimally invasive technique. Vision Res. 37:2943-2952.
61. Stone, E.M., T.A. Braun, S.R. Russell, M.H. Kuehn, A.J. Lotery, P.A. Moore, C.G. Eastman, T.L. Casavant, and V.C. Sheffield. 2004. Missense variations in the fibulin 5 gene and age-related macular degeneration. N. Engl. J. Med. 351:346-353.
62. Sun, H., J.P. Macke, and J. Nathans. 1997. Mechanisms of spectral tuning in the mouse green cone pigment. Proc. Natl. Acad. Sci. USA. 94:8860-8865.
63. Tachibanaki, S., S. Tsushima, and S. Kawamura. 2001. Low amplification and fast visual pigment phosphorylation as mechanisms characterizing cone photoresponses. Proc. Natl. Acad. Sci. USA. 98:14044-14049.
64. Voughl, B.W., A. Dukkipatti, M. Max, B.E. Knox, and R.R. Birge. 1999. Photochemistry of the primary event in short-wavelength visual opsins at low temperature. Biochemistry. 38:11287-11297.
65. Weiss, E.R., M.H. Ducceschi, T.J. Horner, A. Li, C.M. Craft, and S. Osawa. 2001. Species-specific differences in expression of G-protein-coupled receptor kinase (GRK) 7 and GRK1 in mammalian cone photoreceptor cells: implications for cone cell phototransduction. J. Neurosci. 21:9175-9184.
66. Xiao, M., and A. Hendrickson. 2000. Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones. J. Comp. Neurol. 425(4):545-559.
67. Xu, J., R.L. Dodd, C.L. Makino, M.I. Simon. D.A. Baylor, and J. Chen. 1997. Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature. 389:505-509.
68. Yau, K.-W. 1994. Cyclic nucleotide-gated channels: an expanding new family of ion channels. Proc. Natl. Acad. Sci. USA. 91:3481-3483.
69. Yokoyama, R., and S. Yokoyama. 2000. Comparative molecular biology of visual pigments. In Molecular Mechanisms in Visual Transduction. D.G. Stavenga, W.J. de Grip, and E.N. Pugh Jr., editors. Elsevier Science Publishing Co. Inc., New York. 257-296.
70. Yokoyama, S., F.B. Radlwimmer, and S. Kawamura. 1998. Regeneration of ultraviolet pigments of vertebrates. FEBS Lett. 423:155-158.
71. -/- mouse retina: identification of retinal disease candidates and transcriptional regulatory targets of Nrl. Hum. Mol. Genet. 13:1487-1503.
72. Zhu, X., B. Brown, A. Li, A.J. Mears, A. Swaroop, and C.M. Craft. 2003. GRK1-dependent phosphorylation of S- and M-opsins and their binding to cone arrestin during cone phototransduction in the mouse retina. J. Neurosci. 23:6152-6160.