Phototransduction, dark adaption, and rhodopsin regeneration: The proctor lecture

Investigative Ophthalmology and Visual Science

Volumn 47, Issue 12, 2006, Pages 5138-5152

  Lamb, Trevor D ^a   Pugh Jr , Edward N ^b  

^a Biology and Environment   (Australia)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; ION CHANNEL; OPSIN; RHODOPSIN;

BIOCHEMISTRY; BLEACHING; CONFERENCE PAPER; DARK ADAPTATION; DIFFUSION; ELECTRORETINOGRAM; EXPERIMENTAL STUDY; EYE FUNDUS ALBIPUNCTATUS; HUMAN; HYDROLYSIS; HYPOTHESIS; KINETICS; MATHEMATICAL MODEL; NONHUMAN; OGUCHI DISEASE; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PSYCHOPHYSICS; QUANTITATIVE STUDY; REGENERATION; RETINA MACULA AGE RELATED DEGENERATION; RETINA ROD; RETINOL DEFICIENCY; STARGARDT DISEASE; VISUAL SYSTEM; ANIMAL; ARTICLE; AWARDS AND PRIZES; HEALTH CARE ORGANIZATION; HISTORY; OPHTHALMOLOGY; PHYSIOLOGY; RETINA; UNITED STATES;

ANIMALS; AWARDS AND PRIZES; DARK ADAPTATION; FLORIDA; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; OPHTHALMOLOGY; PHOTOTRANSDUCTION; REGENERATION; RETINA; RHODOPSIN; SOCIETIES, SCIENTIFIC;

EID: 33846596863     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-0849     Document Type: Conference Paper

References (81)

1. Lamb TD, Pugh EN Jr. A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol. 1992;449:719-758.
2. Pugh EN Jr, Lamb TD. Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta. 1993;1141:111-149.
3. Pugh EN Jr, Lamb TD. Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In: Handbook of Biological Physics, Vol. 3. Amsterdam: Elsevier; 2000:183-255.
4. Arshavsky VY, Lamb TD, Pugh EN Jr. G proteins and phototransduction. Ann Rev Physiol. 2002;64:153-187.
5. Burns ME, Lamb TD. Visual transduction by rod and cone photoreceptors. In: Chalupa LM, Werner JS, ed. The Visual Neurosciences. Cambridge, MA: MIT Press;1993:215-233.
6. Fisher SK, Anderson DH, Erickson PA, Guérin CJ, Lewis GP, Linberg KA. Light and electron microscopy of vertebrate photoreceptors. In: Hargrave PA, ed. Methods in Neurosciences. Vol. 15. 1993:3-36.
7. Lamb TD, Pugh EN Jr. Dark adaptation and the retinoid cycle of vision. Prog Retinal Eye Res. 2004;23:307-380.
8. Pugh EN Jr, Nikonov S, Lamb TD. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol. 1999;9:410-418.
9. Leskov IB, Klenchin VA, Handy JW, et al. The gain of rod phototransduction: reconciliation of biochemical and electrophysiological measurements. Neuron. 2000;27:525-537.
10. Baylor DA, Nunn BJ. Electrical properties of the light-sensitive conductance of rods of the salamander Ambystoma tigrinum. J Physiol. 1986;371:115-145.
11. Torre V, Matthews HR, Lamb TD. Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc Natl Acad Sci USA. 1986;83:7109-7113.
12. Kraft TW, Schneeweis DM, Schnapf JL. Visual transduction in human rod photoreceptors. J Physiol. 1993;464:747-765.
13. Lyubarsky AL, Pugh EN Jr. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci. 1996;16:563-571.
14. Friedburg C, Thomas MM, Lamb TD. Time course of the flash response of dark- and light-adapted human rod photoreceptors derived from the electroretinogram. J Physiol. 2001;534:217-242.
15. Smith NP, Lamb TD. The a-wave of the human electroretinogram recorded with a minimally invasive technique. Vision Res. 1997;37:2943-2952.
16. Brown KT, Wiesel TN. Localization of origins of electroretinogram components by intraretinal recording in the intact cat eye. J Physiol. 1961;158:257-280.
17. Hagins WA, Penn RD, Yoshikami S. Dark current and photocurrent in retinal rods. Biophys J. 1970;10:380-412.
18. Kang Derwent JJ, Linsenmeier RA. Intraretinal analysis of the a-wave of the electroretinogram (ERG) in dark-adapted intact cat retina. Vis Neurosci. 2001;18:353-363.
19. Jamison JA. Rod photoreceptor contribution to the mammalian electroretinogram. PhD thesis. Ann Arbor, MI: University of Michigan; 2003.
20. Breton ME, Schueller AW, Lamb TD, Pugh EN Jr. Analysis of ERG a-wave amplification and kinetics in terms of the G-protein cascade of phototransduction. Invest Ophthalmol Vis Sci. 1994;35:295-309.
21. -/- mice coexpress functional S- and M-cone opsins having distinct inactivation mechanisms. J Gen Physiol. 2005;125:287-304.
22. Nymark S, Heikkinen H, Haldin C, Donner K, Koskelainen A. Light responses and light adaptation in rat retinal rods at different temperatures. J Physiol. 2005;567:923-938.
23. Burns ME, Mendez A, Chen C-K, et al. Deactivation of phosphorylated and nonphosphorylated rhodopsin by arrestin splice variants. J Neurosci. 2006;26:1036-1044.
24. Whitlock GG, Lamb TD. Variability in the time course of single photon responses from toad rods: termination of rhodopsin's activity. Neuron. 1999;23:337-351.
25. Baylor DA, Burns ME. Control of rhodopsin activity in vision. Eye. 1998;12:521-525.
26. Lamb TD, Matthews HR, Torre V. Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. J Physiol. 1986;372:315-349.
27. Dowling JE. The chemistry of visual adaptation in the rat. Nature. 1960;188:114-118.
28. Rushton WAH. The Ferrier Lecture, 1962. Visual adaptation. Proc Roy Soc B. 1965;162:20-46.
29. Lamb TD. The involvement of rod photoreceptors in dark adaptation. Vision Res. 1981;21:1773-1782.
30. Pugh EN Jr. Rushton's paradox: rod dark adaptation after flash photolysis. J Physiol. 1975;248:413-431.
31. Jackson GR, Owsley C, McGwin G Jr. Aging and dark adaptation. Vision Res. 1999;39:3975-3982.
32. Stiles WS, Crawford BH. Equivalent adaptational levels in localized retinal areas. In: Report of a Joint Discussion on Vision. Cambridge, UK: Cambridge University Press; 1932:194-211.
33. Lamb TD, Cideciyan AV, Jacobson SG, Pugh EN Jr. Towards a molecular description of human dark adaptation. J Physiol. 1998; 506:88P.
34. Cornwall MC, Fain GL. Bleached pigment activates transduction in isolated rods of the salamander retina. J Physiol. 1994;480:261-279.
35. Melia TJ, Cowan CW, Angleson JK, Wensel TG. A comparison of the efficiency of G protein activation by ligand-free and light-activated forms of rhodopsin. Biophys J. 1997;73:3182-3191.
36. Pepperberg DR, Brown PK, Lurie M, Dowling JE. Visual pigment and photoreceptor sensitivity in the isolated skate retina. J Gen Physiol. 1978;71:369-396.
37. Corson DW, Cornwall MC, MacNichol EF, et al. Sensitization of bleached rod photoreceptors by 11-cis-locked analogues of retinal. Proc Natl Acad Sci USA. 1990;87:6823-6827.
38. Hagins WA, Rushton WAH. The measurement of rhodopsin in the decerebrate albino rabbit. J Physiol. 1953;120:61P.
39. Rushton WAH, Campbell FW, Hagins WA, Brindley GS. The bleaching and regeneration of rhodopsin in the living eye of the albino rabbit and man. Optica Acta. 1955;1:183-190.
40. van de Kraats J, Berendschot TTJM, van Norren D. The pathways of light measured in fundus reflectometry. Vision Res. 1996;36: 2229-2247.
41. Alpern M. Rhodopsin kinetics in the human eye. J Physiol. 1971; 217:447-471.
42. Rushton WAH, Powell DS. The rhodopsin content and the visual threshold of human rods. Vision Res. 1972;12:1073-1081.
43. van Norren D, van de Kraats J. Retinal densitometer with the size of a fundus camera. Vision Res. 1989;29:369-374.
44. Liem AT, Keunen JE, van Norren D, van de Kraats J. Rod densitometry in the aging human eye. Invest Ophthalmol Vis Sci. 1991;32:2676-2682.
45. Thomas MM, Lamb TD. Light adaptation and dark adaptation of human rod photoreceptors measured from the a-wave of the electroretinogram. J Physiol. 1999;518:479-496.
46. Bonds AB, MacLeod DIA. The bleaching and regeneration of rhodopsin in the cat. J Physiol. 1974;242:237-253.
47. Ripps H, Mehaffey L III, Siegel IM. Rhodopsin kinetics in the cat retina. J Gen Physiol. 1981;77:317-334.
48. Mahroo OAR, Lamb TD. Recovery of the human photopic electroretinogram after bleaching exposures: estimation of pigment regeneration kinetics. J Physiol. 2004;554:417-437.
49. Bok D. The retinal pigment epithelium, a versatile partner in vision. J Cell Sci. 1993;17:189-195.
50. Bridges CD, Alvarez RA, Fong S-L. Vitamin A in human eyes: amount, distribution, and composition. Invest Ophthalmol Vis Sci. 1982;22:706-714.
51. Jin MH, Li SH, Moghrabi WN, Sun H & Travis GH. Rpe65 is the retinoid isomerase in bovine retinal pigment epithelium. Cell. 2005;122:449-459.
52. Moiseyev G, Chen Y, Takahashi Y, Wu BX, Ma J. RPE65 is the isomerohydrolase in the retinoid visual cycle. Proc Natl Acad Sci USA. 2005;102:12413-12418.
53. Redmond TM, Poliakov E, Yu S, Tsai J-Y, Lu Z, Gentleman, S. Mutation of key residues of RPE65 abolishes its enzymatic role as isomerohydrolase in the visual cycle. Proc Natl Acad Sci USA. 1005;102:13658-13663.
54. Corless RM, Gonnet GH, Hare DEG, Jeffrey DJ, Knuth DE. On the Lambert W function. Adv Comput Math. 1996;5:329-359.
55. Hamel CP, Griffoin J-M, Lasquellec L, Bazalgette C, Arnaud B. Retinal dystrophies caused by mutations in RPE65: assessment of visual functions. Br J Ophthalmol. 2001;85:424-427.
56. Carr RE, Ripps H, Siegel IM. Visual pigment kinetics and adaptation in fundus albipunctatus. Doc Ophthalmol Proc Series. 1974;4:193-204.
57. Cideciyan AV, Haeseleer F, Fariss RN, et al. Rod and cone visual cycle consequences of a null mutation in the 11-cis-retinol dehydrogenase gene in man. Vis Neurosci. 2000;17:667-678.
58. Cideciyan AV, Pugh EN Jr, Lamb TD, Huang Y, Jacobson SG. Rod plateaux during dark adaptation in Sorsby's fundus dystrophy and vitamin A deficiency. Invest Ophthalmol Vis Sci. 1997;38:1786-1794.
59. Steinmetz RL, Haimovici R, Jubb C, Fitzke FW, Bird AC. Symptomatic abnormalities of dark adaptation in patients with age-related Bruch's membrane change. Br J Ophthalmol. 1993;77:549-554.
60. Brown B, Adams AJ, Coletta NJ, Haegerstrom-Portnoy G. Dark adaptation in age-related maculopathy. Ophthalmic Physiol Opt. 1986;6:81-84.
61. Owsley C, Jackson GR, White M, Feist R, Edwards D. Delays in rod-mediated dark adaptation in early age-related maculopathy. Ophthalmol. 2001;108:1196-1202.
62. Bird AC. Bruch's membrane change with age. Br J Ophthalmol. 1992;763:166-188.
63. Moore DJ, Hussain AA, Marshall J. Age-related variation in the hydraulic conductivity of Bruch's membrane. Invest Ophthalmol Vis Sci. 1995;36:1290-1297.
64. Bird AC. The Bowman lecture. Towards an understanding of age-related macular disease. Eye. 2003;17:457-466.
65. Starita C, Hussain AA, Pagliarini S, Marshall J. Hydrodynamics of ageing Bruch's membrane: implications for macular disease. Exp Eye Res. 1996;62:565-572.
66. Curcio CA, Owsley C, Jackson GR. Spare the rods, save the cones in aging and age-related maculopathy. Invest Ophthalmol Vis Sci. 2000;41:2015-2018.
67. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Survey Ophthalmol. 2006;51:137-152.
68. Age-Related Eye Disease Study Research Group. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene, and zinc for age-related macular degeneration and vision loss: AREDS report no. 8. Arch Ophthalmol. 2001;119:1417-1436.
69. McBee JK, Palczewski K, Baehr W, Pepperberg DR. Confronting complexity: the interlink of phototransduction and retinoid metabolism in the vertebrate retina. Prog Retin Eye Res. 2001;20: 469-529.
70. Thompson DA, Gal A. Vitamin A metabolism in the retinal pigment epithelium: genes, mutations and diseases. Prog Retin Eye Res. 22:683-703.
71. Baehr W, Wu SM, Bird AC, Palczewski K. The retinoid cycle and retina disease. Vision Res. 2003;43:2957-2958.
72. Yamamoto S, Sippel KC, Berson EL, Dryja TP. Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat Genet. 1997;15:175-178.
73. Steinmetz RL, Polkinghorne PC, Fitzke FW, Kemp CM, Bird AC. Abnormal dark adaptation and rhodopsin kinetics in Sorsby's fundus dystrophy. Invest Ophthalmol Vis Sci. 1992;33:1633-1636.
74. Burstedt MSI, Sandgren O, Golovleva I, Wachtmeister L. Retinal function in Bothnia dystrophy: an electrophysiological study. Vision Res. 2003;43:2559-2571.
75. Saari JC, Nawrot M, Kennedy BN, et al. Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron. 2001;29:739-748.
76. Sun H, Molday RS, Nathans J. Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt disease. J Biol Chem. 1999;274:8269-8281.
77. Weng J, Mata NL, Azarian SM, Tzekov RT, Birch DG, Travis GH. Insights into the function of Rim protein in photoreceptors and etiology of Stargardt's disease from the phenotype in abcr knockout mice. Cell. 1999;98:13-23.
78. Sparrow JR, Fishkin N, Zhou J, et al. A2E, a byproduct of the visual cycle. Vision Res. 2003;43:2983-2990.
79. Fishman GA, Farbman JS, Alexander KR. Delayed rod dark adaptation in patients with Stargardt's disease. Ophthalmol. 1991;98: 957-962.
80. Cideciyan AV, Aleman TS, Swider M, et al. Mutations in ABCA4 result in accumulation of lipofuscin before slowing of the retinoid cycle: a reappraisal of the human disease sequence. Hum Mol Gen. 2004;13:525-534.
81. Segel IH. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady State Enzyme Systems. New York: Wiley; 1975.