Diffusion of the second messengers in the cytoplasm acts as a variability suppressor of the single photon response in vertebrate phototransduction

Biophysical Journal

Volumn 94, Issue 9, 2008, Pages 3363-3383

  Bisegna, Paolo ^a   Caruso, Giovanni ^b   Andreucci, Daniele ^c   Shen, Lixin ^d,e   Gurevich, Vsevolod V ^d   Hamm, Heidi E ^d,e   Dibenedetto, Emmanuele ^e,f  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b CNR   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^f VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CALCIUM SIGNALING; CALIBRATION; CATALYSIS; CYTOPLASM; DIFFUSION; HUMAN; KINETICS; METABOLISM; PHOTON; PHOTOTRANSDUCTION; PHYSIOLOGY; SECOND MESSENGER; TIME;

ANIMALS; CALCIUM SIGNALING; CALIBRATION; CATALYSIS; CYCLIC GMP; CYTOPLASM; DIFFUSION; HUMANS; KINETICS; MODELS, BIOLOGICAL; PHOTONS; PHOTOTRANSDUCTION; SECOND MESSENGER SYSTEMS; TIME FACTORS;

EID: 43649090740     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.114058     Document Type: Article

References (101)

1. Aho, A. C., K. Donner, C. Hyden, L. O. Larsen, and T. Reuter. 1988. Low retinal noise in animals with low body temperature allows high visual sensitivity. Nature. 334:348-350.
2. Hecht, S., S. Shlaer, and M. Pierenne. 1942. Energy, quanta and vision. J. Gen. Physiol. 25:819-840.
3. Baylor, D. A., T. D. Lamb, and K. W. Yau. 1979. The membrane current of single rod outer segments. J. Physiol. 288:589-611.
4. Baylor, D. A., T. D. Lamb, and K. W. Yau. 1979. Responses of retinal rods to single photons. J. Physiol. 288:613-634.
5. Felber, S., H. P. Breuer, F. Petruccione, J. Honerkamp, and K. P. Hofmann. 1996. Stochastic simulation of the transducin GTPase cycle. Biophys. J. 71:3051-3063.
6. Rieke, F., and D. A. Baylor. 1998. Origin of reproducibility in the responses of retinal rods to single photons. Biophys. J. 75:1836-1857.
7. Rieke, F., and D. A. Baylor. 1998. Single photon detection by rod cells of the retina. Rev. Mod. Phys. 70:1027-1036.
8. Whitlock, G. G., and T. D. Lamb. 1999. Variability in the timecourse of single photon responses from toad rods: termination of rhodopsin's activity. Neuron. 23:337-351.
9. Ramanathan, S., P. B. Detwiler, A. M. Sengupta, and B. I. Shraiman. 2005. G-protein-coupled enzyme cascades have intrinsic properties that improve signal localization and fidelity. Biophys. J. 88:3063-3071.
10. Pugh, E. N. 1999. Variability of single photon responses: a cut in the Gordian knot of rod phototransduction? Neuron. 23:205-208.
11. Liebman, P. A., and E. N. Pugh. 1979. The control of phosphodiesterase in rod disk membranes: kinetics, possible mechanisms, and significance for vision. Vision Res. 19:375-380.
12. Liebman, P. A., K. R. Parker, and E. A. Dratz. 1987. The molecular mechanism of visual excitation and its relation to the structure and composition of the rod outer segment. Annu. Rev. Physiol. 49:765-791.
13. Andreucci,D.,P.Bisegna,G.Caruso, H. E. Hamm, and E. DiBenedetto. 2003. Mathematical model of the spatiotemporal dynamics of second messengers in visual transduction. Biophys. J. 85:1358-1376.
14. Caruso, G., H. Khanal, V. Alexiades, F. Rieke, H. E. Hamm, and E. DiBenedetto. 2005. Mathematical and computational modeling of spatiotemporal signaling in rod phototransduction. IEE Proc. Sys. Biol. 152:119-137.
15. Caruso, G., P. Bisegna, L. Shen, D. Andreucci, H. E. Hamm, and E. DiBenedetto. 2006. Modeling the role of incisures in vertebrate phototransduction. Biophys. J. 91:1192-1212.
16. Pugh, E. N., Jr., and T. D. Lamb. 2000. Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. In Handbook of Biological Physics, Vol. 3. Elsevier Science, St. Louis, MO.
17. Pugh, Jr., E. N., and T. Lamb. 1993. Amplification and kinetics of the activation steps in phototransduction. Biochim. Biophys. Acta. 1141:111-149.
18. Vishnivetskiy, S. A., D. Raman, J. Wei, M. J. Kennedy, J. B. Hurley, and V. V. Gurevich. 2007. Regulation of arrestin binding by rhodopsin phosphorylation level. J. Biol. Chem. 282:32075-32083.
19. Ohguro, H., J. P. Van Hooser, A. H. Milam, and K. Palczewski. 1995. Rhodopsin phosphorylation and dephosphorylation in vivo. J. Biol. Chem. 270:14259-14262.
20. Wilden, U., S. W. Hall, and H. Kuhn. 1986. Phosphodiesterase activation by photoexcited rhodopsin is quenched when rhodopsin is phosphorylated and binds the intrinsic 48-kDa protein of rod outer segments. Proc. Natl. Acad. Sci. USA. 83:1174-1178.
21. 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. 267:374-377.
22. 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.
23. Krispel, C. M., D. Chen, N. Melling, Y. J. Chen, K. A. Martemyanov, N. Quillinan, V. Y. Arshavsky, T. G. Wensel, C. K. Chen, and M. E. Burns. 2006. RGS expression rate-limits recovery of rod photoresponses. Neuron. 51:409-416.
24. Baylor, D. A., G. Matthews, and K. W. Yau. 1980. Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. 309:591-621.
25. Rieke, F., and D. A. Baylor. 1996. Molecular origin of continuous dark noise in rod photoreceptors. Biophys. J. 71:2553-2572.
26. 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.
27. Sakitt, B. 1972. Counting every quantum. J. Physiol. 223:131-150.
28. Field, G. D., and F. Rieke. 2002. Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron. 35:733-747.
29. Andreucci, D., P. Bisegna, and E. DiBenedetto. 2003. Homogenization and concentrated capacity for the heat equation with nonlinear variational data in reticular almost disconnected structures and applications to visual transduction. Ann. Mat. Pure Appl. 182:375-407.
30. Andreucci, D., P. Bisegna, and E. DiBenedetto. 2006. Homogenization and concentration of capacity in phototransduction in vertebrate photoreception. Appl. Anal. 85:303-331 (Special Issue in honor of C. Pucci.).
31. Makino,C.L., R.L.Dodd, J. Chen, M. E. Burns, A. Roca, M.I. Simon, and D. A. Baylor. 2004. Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J. Gen. Physiol. 123:729-741.
32. Wilden, U. 1995. Duration and amplitude of the light-induced cGMP hydrolysis in vertebrate photoreceptors are regulated by multiple phosphorylation of rhodopsin and by arrestin binding. Biochemistry. 34:1446-1454.
33. Gibson, S. K., J. H. Parkes, and P. A. Liebman. 2000. Phosphorylation modulates the affinity of light-activated rhodopsin for G protein and arrestin. Biochemistry. 39:5738-5749.
34. 2+-dependent control of rhodopsin phosphorylation: recoverin and rhodopsin kinase. Adv. Exp. Med. Biol. 514:69-99.
35. Pullen, N., N. G. Brown, R. P. Sharma, and M. Akhtar. 1993. Cooperativity during multiple phosphorylations catalyzed by rhodopsin kinase: supporting evidence using synthetic phosphopeptides. Biochemistry. 32:3958-3964.
36. Brannock, M. T., K. Weng, and P. R. Robinson. 1999. Rhodopsin's carboxyl-terminalthreonines arerequired forwild-typearrestin-mediated quench of transducin activation in vitro. Biochemistry. 38:3770-3777.
37. Aton, B. R., B. J. Litman, and M. L. Jackson. 1984. Isolation and identification of the phosphorylated species of rhodopsin. Biochemistry. 23:1737-1741.
38. Wilden, U., and H. Kuhn. 1982. Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry. 21:3014-3022.
39. Pulvermuller, A., K. Palczewski, and K. P. Hofmann. 1993. Interaction between photoactivated rhodopsin and its kinase: stability and kinetics of complex formation. Biochemistry. 32:14082-14088.
40. 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.
41. Nair, K. S., S. M. Hanson, A. Mendez, E. V. Gurevich, M. J. Kennedy, V. I. Shestopalov, S. A. Vishnivetskiy, J. Chen, J. B. Hurley, V. V. Gurevich, and V. Z. Slepak. 2005. Light-dependent redistribution of arrestin in vertebrate rods is an energy-independent process governed by protein-protein interactions. Neuron. 46:555-567.
42. Hanson, S. M., E. V. Gurevich, S. A. Vishnivetskiy, M. R. Ahmed, X. Song, and V. V. Gurevich. 2007. Each rhodopsin molecule binds its own arrestin. Proc. Natl. Acad. Sci. USA. 104:3125-3128.
43. Strissel, K. J., M. Sokolov, L. H. Trieu, and V. Y. Arshavsky. 2006. Arrestin translocation is induced at a critical threshold of visual signaling and is superstoichiometric to bleached rhodopsin. J. Neurosci. 26:1146-1153.
44. Hanson, S. M., N. Van-Eps, D. J. Francis, C. Altenbach, S. A. Vishnivetskiy, V. Y. Arshavsky, C. S. Klug, W. L. Hubbell, and V. V. Gurevich. 2007. Structure and function of the visual arrestin oligomer. EMBO J. 26:1726-1736.
45. Doan, T., A. Mendez, P. B. Detwiler, J. Chen, and F. Rieke. 2006. Multiple phosphorylation sites confer reproducibility of the rod's single-photon responses. Science. 313:530-533.
46. Hamer, R. D., S. C. Nicholas, D. Tranchina, P. A. Liebman, and T. D. Lamb. 2003. Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. J. Gen. Physiol. 122:419-444.
47. 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.
48. 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.
49. Nikonov, S., T. D. Lamb, and E. N. Pugh, Jr. 2000. The role of steady phosphodiesterase activity in the kinetics and sensitivity of the lightadapted salamander rod photoresponse. J. Gen. Physiol. 116:795-824.
50. 2+. J. Gen. Physiol. 107:19-34.
51. Lyubarsky, A. L., and E. N. Pugh, Jr. 1996. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J. Neurosci. 16:563-571.
52. Hood, D. C., and D. G. Birch. 1995. Phototransduction in human cones measured using the α-wave of the ERG. Vision Res. 35:2801-2810.
53. Gray-Keller, M., W. Denk, B. Shraiman, and P. B. Detwiler. 1999. Longitudinal spread of second messenger signals in isolated rod outer segments of lizards. J. Physiol. 519:679-692.
54. 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.
55. Olson, A., and E. N. Pugh, Jr. 1993. Diffusion coefficient of cyclic GMP in salamander rod outer segments estimated with two fluorescent probes. Biophys. J. 65:1335-1352.
56. Cohen, A. I. 1960. The ultrastructure of the rods of the mouse retina. Am. J. Anat. 107:23-48.
57. Carter-Dawson, L. D., and M. M. Lavail. 1979. Rods and cones in the mouse retina. J. Comp. Neurol. 188:245-262.
58. Rieke, F., and D. A. Baylor. 2000. Origin and functional impact of dark noise in retinal cones. Neuron. 26:181-186.
59. Holcman, D., and J. I. Korenbrot. 2004. Longitudinal diffusion in retinal rod and cone outer segment cytoplasm: the consequence of cell structure. Biophys. J. 86:2566-2582.
60. Chang, G. Q., Y. Hao, and F. Wong. 1993. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 11:595-605.
61. 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.
62. 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.
63. Koutalos, Y., K. Nakatani, and K. W. Yau. 1995. Cyclic GMP diffusion coefficients in rod photoreceptor outer segments. Biophys. J. 68: 373-382.
64. Nakatani, K., C. Chen, and Y. Koutalos. 2002. Calcium diffusion coefficient in rod photoreceptor outer segments. Biophys. J. 82:728-739.
65. Eckmiller, M. S. 2000. Microtubules in a rod-specific cytoskeleton associated with outer segment incisures. Vis. Neurosci. 17:711-722.
66. Tsukamoto, Y. 1987. The number, depth and elongation ofdiskincisures in the retinal rod of Rana catesbiana. Exp. Eye Res. 45:105-116.
67. Papermaster, D. S., P. Reilly, and B. G. Schneider. 1982. Cone lamellae and red and green rod outer segment disks contain a large intrinsic membrane protein on their margins: an ultrastructural immunocytochemical study of frog retinas. Vision Res. 22:1417-1428.
68. Liang, Y., D. Fotiadis, S. Filipek, D. A. Saperstein, K. Palczewski, and A. Engel. 2003. Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278:21655-21662.
69. Roof, D., M. Adamian, D. Jacobs, and A. Hayes. 1991. Cytoskeletal specializations at the rod photoreceptor distal tip. J. Comp. Neurol. 305:289-303.
70. 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.
71. Tsang, S. H., M. E. Burns, P. D. Calvert, P. Gouras, D. A. Baylor, S. P. Goff, and V. Y. Arshavsky. 1998. Role for the target enzyme in deactivation of photoreceptor G protein in vivo. Science. 282:117-121.
72. Burns, M. E., A. Mendez, J. Chen, and D. A. Baylor. 2002. Dynamics of cyclic GMP synthesis in retinal rods. Neuron. 36:81-91.
73. Pugh, E. N., Jr., T. Duda, A. Sitaramayya, and R. K. Sharma. 1997. Photoreceptor guanylate cyclases: a review. Biosci. Rep. 17:429-473.
74. Pugh, E. N., Jr., and T. Lamb. 1990. Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors. Vision Res. 30:1923-1948.
75. Detwiler, P. B., S. Ramanathan, A. Sengupta, and B. I. Shraiman. 2000. Engineering aspects of enzymatic signal transduction: photoreceptors in the retina. Biophys. J. 79:2801-2817.
76. Gray-Keller, M. P., and P. B. Detwiler. 1994. The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron. 13:849-861.
77. Korenbrot, J. I., and D. Miller. 1989. Cytoplasmic free calcium concen-trationindark-adapted retinal rod outersegments. Vision Res. 29:939-948.
78. Lagnado, L., L. Cervetto, and P. A. McNaughton. 1992. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. J. Physiol. 455:111-142.
79. McCarthy, S. T., J. P. Younger, and W. G. Owen. 1994. Free calcium concentrations in bullfrog rods determined in the presence of multiple forms of Fura-2. Biophys. J. 67:2076-2089.
80. Ratto, G. M., R. Payne, W. G. Owen, and R. Y. Tsien. 1988. The concentration of cytosolic free calcium in vertebrate rod outer segments measured with Fura-2. J. Neurosci. 8:3240-3246.
81. 2+ in salamander rods. J. Gen. Physiol. 111:53-64.
82. Woodruff, M. L., A. P. Sampath, H. R. Matthews, N. V. Krasnoperova, J. Lem, and G. L. Fain. 2002. Measurement of cytoplasmic calcium concentration in the rods of wild-type and transducin knock-out mice. J. Physiol. 542:843-854.
83. Fotiadis, D., Y. Liang, S. Filipek, D. A. Saperstein, A. Engel, and K. Palczewski. 2003. Rhodopsin dimers in native disk membranes. Nature. 421:127-128.
84. Reilander, H., A. Achilles, U. Friedel, G. Maul, F. Lottspeich, and N. J. Cook. 1992. Primary structure and functional expression ofthe Na/Ca,Kexchanger from bovine rod photoreceptors. EMBO J. 11:1689-1695.
85. Schnetkamp, P. P. 1990. Cation selectivity of and cation binding to the cGMP-dependent channel in bovine rod outer segment membranes. J. Gen. Physiol. 96:517-534.
86. Liang, Y., D. Fotiadis, T. Maeda, A. Maeda, A. Modzelewska, S. Filipek, D. A. Saperstein, A. Engel, and K. Palczewski. 2004. Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J. Biol. Chem. 279:48189-48196.
87. Lyubarsky, A. L., L. L. Daniele, and E. N. Pugh, Jr. 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 Res. 44:3235-3251.
88. Fan, J., M. L. Woodruff, M. C. Cilluffo, R. K. Crouch, and G. L. Fain. 2005. Opsin activation of transduction in the rods of dark-reared Rpe65 knockout mice. J. Physiol. 568:83-95.
89. Krispel, C. M., C. K. Chen, M. I. Simon, and M. E. Burns. 2003. Novel form of adaptation in mouse retinal rods speeds recovery of phototransduction. J. Gen. Physiol. 122:703-712.
90. Krispel, C. M., C. K. Chen, M. I. Simon, and M. E. Burns. 2003. Prolonged photoresponses and defective adaptation in rods of Gβ35-/- mice. J. Neurosci. 23:6965-6971.
91. 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.
92. Mendez, A., and J. Chen. 2002. Mouse models to study GCAP functions in intact photoreceptors. Adv. Exp. Med. Biol. 514:361-388.
93. Wang, Z., X. H. Wen, Z. Ablonczy, R. K. Crouch, C. L. Makino, and J. Lem. 2005.Enhanced shutoff of phototransduction in transgenic mice expressing palmitoylation-deficient rhodopsin. J. Biol. Chem. 280:24293-24300.
94. 2+ release. J. Physiol. 557:821-828.
95. Schnetkamp, P. P. 1989. Na-Ca or Na-Ca-K exchange in rod photoreceptors. Prog. Biophys. Mol. Biol. 54:1-29.
96. Schnetkamp, P. P. 1991. Optical measurements of Na-Ca-K exchange currents in intact outer segments isolated from bovine retinal rods. J. Gen. Physiol. 98:555-573.
97. + fluxes through the bovine rod outer segment Na-Ca-K exchanger. J. Biol. Chem. 266:198-206.
98. Qin, N., and W. Baehr. 1994. Expression and mutagenesis of mouse rod photoreceptor cGMP phosphodiesterase. J. Biol. Chem. 269: 3265-3271.
99. Kennedy, M. J., M. E. Sowa, T. G. Wensel, and J. B. Hurley. 2003. Acceleration of key reactions as a strategy to elucidate the ratelimiting chemistry underlying phototransduction inactivation. Invest. Ophthalmol. Vis. Sci. 44:1016-1022.
100. Sitaramayya, A., J. Harkness, J. H. Parkes, C. Gonzalez-Oliva, and P. A. Liebman. 1986. Kinetic studies suggest that light-activated cyclic GMP phosphodiesterase is a complex with G-protein subunits. Biochemistry. 25:651-656.
101. 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.