Kinetics of rhodopsin deactivation and its role in regulating recovery and reproducibility of rod photoresponse

PLoS Computational Biology

Volumn 6, Issue 12, 2010, Pages

  Caruso, Giovanni ^a   Bisegna, Paolo ^b   Lenoci, Leonardo ^c   Andreucci, Daniele ^d   Gurevich, Vsevolod V ^c   Hamm, Heidi E ^c   DiBenedetto, Emmanuele ^e  

^a CNR   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYST ACTIVITY; CONTINUOUS TIME SYSTEMS; MARKOV PROCESSES; PARTICLE BEAMS;

CONTINOUS TIME MARKOV CHAIN; ELECTRICAL RESPONSE; PHOTON RESPONSE; PHOTORESPONSES; PHOTOTRANSDUCTION; RANDOM NUMBERS; REPRODUCIBILITIES; SINGLE PHOTONS; SOJOURN TIME; SPATIO-TEMPORAL MODELS;

PHOSPHORYLATION;

RHODOPSIN; RETINA S ANTIGEN; RHODOPSIN KINASE;

ANIMAL EXPERIMENT; ARTICLE; CATALYSIS; COEFFICIENT OF VARIATION; CONSTANTS AND COEFFICIENTS; CONTROLLED STUDY; MATHEMATICAL MODEL; MOUSE; MUTANT; NONHUMAN; PHOSPHORYLATION; PHOTOTRANSDUCTION; PROBABILITY; RANDOMNESS; REPRODUCIBILITY; SIMULATION; SINGLE PHOTON RESPONSE; STATISTICAL PARAMETERS; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; GENETICS; KINETICS; METABOLISM; PHOTON; PHYSIOLOGY; RETINA ROD; TRANSGENIC MOUSE;

MUS; VERTEBRATA;

ANIMALS; ARRESTIN; COMPUTATIONAL BIOLOGY; G-PROTEIN-COUPLED RECEPTOR KINASE 1; KINETICS; MARKOV CHAINS; MICE; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; PHOSPHORYLATION; PHOTONS; REPRODUCIBILITY OF RESULTS; RETINAL ROD PHOTORECEPTOR CELLS; RHODOPSIN;

EID: 78651391344     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1001031     Document Type: Article

References (49)

1. Doan T, Mendez A, Detwiler P, Chen J, Rieke F (2006) Multiple phosphorylation sites confer reproducibility of the rod's single-photon responses. Science 313: 530-533.
2. Doan T, Azevedo W, Hurley J, Rieke F (2009) Arrestin competition influences the kinetics and variability of the single-photon responses of mammalian rod photoreceptors. J of Neurosci 29: 11879-11867.
3. Mendez A, Burns ME, Roca A, Lem J, Wu LW, et al. (2000) Rapid and reproducible deactivation of rhodopsin requires multiple phosphorylation sites. Neuron 28: 153-164.
4. Field GD, Rieke F (2002) Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35: 733-747.
5. Whitlock GG, Lamb TD (1999) Variability in the time course of single photon responses from toad rods: termination of rhodopsin's activity. Neuron 23: 337-351.
6. Rieke F, Baylor DA (1998) Origin of reproducibility in the responses of retinal rods to single photons. Biophys J 75: 1836-1857.
7. Burns ME, Mendez A, Chen J, Baylor DA (2002) Dynamics of cyclic GMP synthesis in retinal rods. Neuron 36: 81-91.
8. Bisegna P, Caruso G, Andreucci D, Shen L, Gurevich VV, et al. (2008) Diffusion of the second messengers in the cytoplasm acts as a variability suppressor of the single photon response in vertebrate phototransduction. Biophys J 94: 3363-3383.
9. Andreucci D, Bisegna P, Caruso G, Hamm HE, DiBenedetto E (2003) Mathematical model of the spatio-temporal dynamics of second messengers in visual transduction. Biophys J 85: 1358-1376.
10. Caruso G, Khanal H, Alexiades V, Rieke F, Hamm HE, et al. (2005) Mathematical and computational modeling of spatio-temporal signaling in rod phototransduction. IEE Proc Syst Biol 152: 119-137.
11. Caruso G, Bisegna P, Shen L, Andreucci D, Hamm HE, et al. (2006) Modeling the role of incisures in vertebrate phototransduction. Biophys J 91: 1192-1212.
12. Burns ME, Mendez A, Chen CK, Almuete A, Quillinan N, et al. (2006) Deactivation of phosphorylated and nonphosphorylated rhodopsin by arrestin splice variants. J Neurosci 26: 1036-1044.
13. Shi G, Yau KW, Chen J, Kefalov VJ (2007) Signaling properties of a short-wave cone visual pigment and its role in phototransduction. J Neurosci 27: 10084-93.
14. Varadhan S (2001) Probability Theory. Providence, R.I.: AMS.
15. Gikhman I, Skorokhod A (1969) Introduction to the Theory of Random Processes. New York: Dover.
16. Reingruber J, Holcman D (2008) The dynamics of phosphodiesterase activation in rods and cones. Biophys J 94: 1954-1970.
17. Hanson SM, Francis DJ, Vishnivetskiy SA, Klug CS, Gurevich VV (2006) Visual arrestin binding to microtubules involves a distinct conformational change. J Biol Chem 281: 9765-9772.
18. Hanson SM, Gurevich EV, Vishnivetskiy SA, Ahmed MR, X S, et al. (2007) Each rhodopsin molecule binds its own arrestin. Proc Natl Acad Sci USA 104: 3125-3128.
19. Raman D, Kennedy MJ, Hurley JB, Gurevich VV (2005) Threshold mechanism of arrestin activation: two rhodopsin-attached phosphates are necessary and sufficient for high-affinity arrestin binding. In: Association for Research in Vision and Ophthalmology Annual Meeting; 1-4 May 2005; Fort Lauderdale, Florida, United States of America.
20. Vishnivetskiy SA, Raman D, Wei J, Kennedy MJ, Hurley JB, et al. (2007) Regulation of arrestin binding by rhodopsin phosphorylation level. J Biol Chem 282: 32075-32083.
21. Rieke F, Baylor DA (1998) Single photon detection by rod cells of the retina. Rev Mod Phys 70: 1027-1036.
22. Hamer RD, Nicholas SC, Tranchina D, Liebman PA, Lamb TD (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.
23. Chen CK, Burns ME, Spencer M, Niemi GA, Chen J, et al. (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96: 3718-3722.
24. Xu J, Dodd RL, Makino CL, Simon MI, Baylor DA, et al. (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389: 505-509.
25. Chen J, Makino CL, Peachey NS, Baylor DA, Simon MI (1995) Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267: 374-377.
26. 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.
27. Wen XH, Shen L, Brush RS, Michaud N, Al-Ubaidi MR, et al. (2009) Overexpression of rhodopsin alters the structure and photoresponse of rod photoreceptors. Biophys J 9: 939-950.
28. Gross P, Burns M (2010) Control of rhodopsin's active lifetime by arrestin-1 expression in mammalian rods. J Neurosci 30: 3450-3457.
29. Krispel CM, Chen D, Melling N, Chen YJ, Martemyanov KA, et al. (2006) RGS expression rate-limits recovery of rod photoresponses. Neuron 51: 409-416.
30. Burns M, Pugh EN (2009) Rgs9 concentration matters in rod phototransduction. Biophys J 97: 1538-1547.
31. Chen CK, Woodruff ML, Chen FS, Chen D, Fain G (2010) Background light produces a recoverin-dependent modulation of activated-rhodopsin lifetime in mouse rods. J Neurosci 30: 1213-1220.
32. Gibson SK, Parkes JH, Liebman PA (2000) Phosphorylation modulates the affinity of light-activated rhodopsin for G protein and arrestin. Biochemistry 39: 5738-5749.
33. Wilden U, Hall SW, Kuhn H (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.
34. Kennedy MJ, Lee KA, Niemi GA, Craven KB, Garwin GG, et al. (2001) Multiple phosphorylation of rhodopsin and the in vivo chemistry underlying rod photoreceptor dark adaptation. Neuron 31: 87-101.
35. Vishnivetskiy SA, Paz CL, Schubert C, Hirsch JA, Sigler PB, et al. (1999) How does arrestin respond to the phosphorylated state of rhodopsin? J Biol Chem 274: 11451-11454.
36. Pullen N, Brown NG, Sharma RP, Akhtar M (1993) Cooperativity during multiple phosphorylations catalyzed by rhodopsin kinase: supporting evidence using synthetic phosphopeptides. Biochemistry 32: 3958-3964.
37. Shen L, Caruso G, Bisegna P, Andreucci D, Gurevich VV, et al. (2010) Dynamics of mouse rod phototransduction and its sensitivity to variation of key parameters. IET Syst Biol 4: 12-32.
38. Palczewski K, Buczylko J, Ohguro H, Annan RS, Carr SA, et al. (1994) Characterization of a truncated form of arrestin isolated from bovine rod outer segments. Protein Sci 3: 314-324.
39. Buczylko J, Gutmann C, Palczewski K (1991) Regulation of rhodopsin kinase by autophosphorylation. Proc Natl Acad Sci USA 88: 2568-2572.
40. Gurevich VV, Benovic JL (1992) Cell-free expression of visual arrestin. truncation mutagenesis identifies multiple domains involved in rhodopsin interaction. J Biol Chem 267: 21919-21923.
41. Gurevich VV, Benovic JL (1993) Visual arrestin interaction with rhodopsin: Sequential multisite binding ensures strict selectivity towards light-activated phosphorylated rhodopsin. J Biol Chem 268: 11628-11638.
42. Song X, Vishnivetskiy SA, Gross OP, Emilianoff K, Mendez A, et al. (2009) Enhanced arrestin facilitates recovery and protects rods lacking rhodopsin phosphorylation. Curr Biol 19: 700-705.
43. Wilden U, Kuhn H (1982) Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21: 3014-3022.
44. Schleicher A, Kuhn H, Hoffman KP (1989) Kinetics, binding constant, and activation energy of the 48-kda protein-rhodopsin complex by extrametarhodopsin ii. Biochem 28: 1770-1775.
45. Chen CK, Burns ME, He W, Wensel TG, Baylor DA, et al. (2000) Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature 403: 557-560.
46. Makino CL, Dodd RL, Chen J, Burns ME, Roca A, et al. (2004) Recoverin regulates light-dependent phosphodiesterase activity in retinal rods. J Gen Physiol 123: 729-741.
47. Krispel CM, Chen CK, Simon MI, Burns ME (2003) Novel form of adaptation in mouse retinal rods speeds recovery of phototransduction. J Gen Physiol 122: 703-712.
48. Krispel CM, Chen CK, Simon MI, Burns ME (2003) Prolonged photoresponses and defective adaptation in rods of Gbeta5-/- mice. J Neurosci 23: 6965-6971.
49. Mendez A, Burns ME, Sokal I, Dizhoor AM, Baehr W, et al. (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc Natl Acad Sci USA 98: 9948-9953.