Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings

Journal of General Physiology

Volumn 127, Issue 4, 2006, Pages 359-374

  Nikonov, Sergei S ^a   Kholodenko, Roman ^a,b   Lem, Janis ^c   Pugh Jr , Edward N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; OPSIN; TRANSDUCIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DARK ADAPTATION; GENOTYPE; MATHEMATICAL ANALYSIS; MOUSE; NONHUMAN; PHOTORECEPTOR; PHOTOSTIMULATION; PHOTOTRANSDUCTION; RETINA CONE;

ANIMALS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CONES (RETINA); DARK ADAPTATION; ELECTRORETINOGRAPHY; EYE PROTEINS; GENE EXPRESSION REGULATION; LIGHT; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OPSIN; PHOTOTRANSDUCTION; RETINA; RODS (RETINA); TRANSDUCIN;

EID: 33645278072     PISSN: 00221295     EISSN: 00221295     Source Type: Journal    
DOI: 10.1085/jgp.200609490     Document Type: Article

References (59)

1. Applebury, M.L., M.P. Antoch, L.C. Baxter, L.L. Chun, J.D. Falk, F. Farhangfar, K. Kage, M.G. Krzystolik, 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.
2. 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. 357:575-607.
3. Berntson, A., and W.R. Taylor. 2000. Response characteristics and receptive field widths of on-bipolar cells in the mouse retina. J. Physiol. 524(Pt 3):879-889.
4. 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.
5. Caenepeel, 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.
6. Calderone, J.B., and G.H. Jacobs. 1995. Regional variations in the relative sensitivity to UV light in the mouse retina. Vis. Neurosci. 12:463-468.
7. 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 α-subunit. Proc. Natl. Acad. Sci. USA. 97:13913-13918 (published erratum appears in Proc. Natl. Acad. Sci. USA. 2000. 98:10515).
8. Carter-Dawson, L.D., and M.M. LaVail. 1979. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J. Comp. Neurol. 188:245-262.
9. 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.
10. Chen, C.K., K. 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.
11. Cornwall, M.C., and G.L. Fain. 1994. Bleached pigment activates transduction in isolated rods of the salamander retina. J. Physiol. 480(Pt 2):261-279.
12. Cornwall, M.C., H.R. Matthews, R.K. Crouch, and G.L. Fain. 1995. Bleached pigment activates transduction in salamander cones. J. Gen. Physiol. 106:543-557.
13. Dacey, D.M. 1996. Circuitry for color coding in the primate retina. Proc. Natl. Acad. Sci. USA. 93:582-588.
14. Dacey, D.M. 2000. Parallel pathways for spectral coding in primate retina. Annu. Rev. Neurosci. 23:743-775.
15. 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. Invest. Ophthalmol. Vis. Sci. 46:2156-2167.
16. Engel, S.A., G.H. Glover, and B.A. Wandell. 1997. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex. 7:181-192.
17. 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.
18. + current in rod inner segments. J. Gen. Physiol. 111:583-599.
19. Ghosh, K.K., S. Bujan, S. Haverkamp, A. Feigenspan, and H. Wassle. 2004. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 469:70-82.
20. 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.
21. 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.
22. Hestrin, S. 1987. The properties and function of inward rectification in rod photoreceptors of the tiger salamander. J. Physiol. 390:319-333.
23. Jacobs, G.H., J. Neitz, and J.F. Deegan. 1991. Retinal receptors in rodents maximally sensitive to ultraviolet light. Nature. 353:655-656.
24. Jeon, C.J., E. Strettoi, and R.H. Masland. 1998. The major cell populations of the mouse retina. J. Neurosci. 18:8936-8946.
25. Kenkre, J.S., N.A. Moran, T.D. Lamb, and O.A. Mahroo. 2005. Extremely rapid recovery of human cone circulating current at the extinction of bleaching exposures. J. Physiol. 567:95-112.
26. Klein, R., B.E. Klein, S.C. Tomany, S.M. Meuer, and G.H. Huang. 2002. Ten-year incidence and progression of age-related maculopathy: the beaver dam eye study. Ophthalmology. 109:1767-1779.
27. Lamb, T.D. 1981. The involvement of rod photoreceptors in dark adaptation. Vision Res. 21:1773-1782.
28. Lamb, T.D. 1995. Photoreceptor spectral sensitivities: common shape in the long-wavelength region. Vision Res. 35:3083-3091.
29. 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.
30. Lerea, C.L., A.H. Bunt-Milam, and J.B. Hurley. 1989. α-Transducin is present in blue-, green-, and red-sensitive cone photoreceptors in the human retina. Neuron. 3:367-376.
31. Lerea, C.L., D.E. Somers, J.B. Hurley, I.B. Klock, and A.H. Bunt-Milam. 1986. Identification of specific transducin α subunits in retinal rod and cone photoreceptors. Science. 234:77-80.
32. Lukats, A., O. Dkhissi-Benyahya, Z. Szepessy, P. Rohlich, B. Vigh, N.C. Bennett, H.M. Cooper, and A. Szel. 2002. Visual pigment coexpression in all cones of two rodents, the Siberian hamster, and the pouched mouse. Invest. Ophthalmol. Vis. Sci. 43:2468-2473.
33. 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.
34. 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.
35. 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.
36. Lyubarsky, A.L., and E.N. Pugh Jr. 1996. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J. Neurosci. 16(2):563-571.
37. Matthews, H.R., M.C. Cornwall, and G.L. Fain. 1996. Persistent activation of transducin by bleached rhodopsin in salamander rods. J. Gen. Physiol. 108:557-563.
38. 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.
39. Nakatani, K., T. Tamura, and K.W. Yau. 1991. Light adaptation in retinal rods of the rabbit and two other nonprimate mammals. J. Gen. Physiol. 97:413-435.
40. Nikonov, S., N. Engheta, and E.N. Pugh Jr. 1998. Kinetics of recovery of the dark-adapted salamander rod photoresponse. J. Gen. Physiol. 111(1):7-37.
41. Nikonov, S., T.D. Lamb, and E.N. Pugh Jr. 2000. The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse. J. Gen. Physiol. 116:795-824.
42. -/- mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms. J. Gen. Physiol. 125:287-304.
43. 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(Pt 2):469-482.
44. Pennesi, M.E., J.H. Cho, Z. Yang, S.H. Wu, J. Zhang, S.M. Wu, and M.J. Tsai. 2003a. BETA2/NeuroD1 null mice: a new model for transcription factor-dependent photoreceptor degeneration. J. Neurosci. 23:453-461.
45. Pennesi, M.E., K.A. Howes, W. Baehr, and S.M. Wu. 2003b. Guanylate cyclase-activating protein (GCAP) 1 rescues cone recovery kinetics in GCAP1/GCAP2 knockout mice. Proc. Natl. Acad. Sci. USA. 100:6783-6788.
46. Pugh, E.N., Jr., and T.D. Lamb. 1993. Amplification and kinetics of the activation steps in phototransduction. Biochim. Biophys. Acta. 1141:111-149.
47. Pugh, E.N., Jr., S. Nikonov, and T.D. Lamb. 1999. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr. Opin. Neurobiol. 9:410-418.
48. 2+-dependent modulation of cGMP-gated ion channels is detectable in cones but not in rods. J. Gen. Physiol. 123:63-75.
49. Robson, J.G., H. Maeda, S.M. Saszik, and L.J. Frishman. 2004. In vivo studies of signaling in rod pathways of the mouse using the electroretinogram. Vision Res. 44:3253-3268.
50. Rohlich, P., T. van Veen, and A. Szel. 1994. Two different visual pigments in one retinal cone cell. Neuron. 13:1159-1166.
51. 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.
52. 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.
53. 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.
54. Wilkie, T.M., Y. Chen, D.J. Gilbert, K.J. Moore, L. Yu, M.I. Simon, N.G. Copeland, and N.A. Jenkins. 1993. Identification, chromosomal location, and genome organization of mammalian G-protein-coupled receptors. Genomics. 18:175-184.
55. 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.
56. Ying, S., S.L. Fong, W.B. Fong, C.W. Kao, R.L. Converse, and W.W. Kao. 1998. A CAT reporter construct containing 277bp GNAT2 promoter and 214bp IRBP enhancer is specifically expressed by cone photoreceptor cells in transgenic mice. Curr. Eye Res. 17:777-782.
57. 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.
58. -/- mouse retina: identification of retinal disease candidates and transcriptional regulatory targets of Nrl. Hum. Mol. Genet. 13:1487-1503.
59. Zhang, X., T.G. Wensel, and T.W. Kraft. 2003. GTPase regulators and photoresponses in cones of the eastern chipmunk. J. Neurosci. 23:1287-1297.