Calcium-activated opsin phosphatase activity in retinal rod outer segments

European Journal of Biochemistry

Volumn 238, Issue 3, 1996, Pages 613-622

  Kutuzov, Mikhaïl A ^a,b   Bennett, Nelly ^a,c  

^a CNRS   (France)

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

^c CEA GRENOBLE   (France)

Author keywords

adaptation; phosphatase; phosphorylation; rhodopsin

Indexed keywords

CALCIUM ION; OKADAIC ACID; OPSIN; PHOSPHOPROTEIN PHOSPHATASE; RHODOPSIN;

ADAPTATION; ANIMAL TISSUE; ARTICLE; CATTLE; CONTROLLED STUDY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RETINA ROD OUTER SEGMENT; VISION;

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 0030037416     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0613w.x     Document Type: Article

References (65)

1. Becker, W., Kentrup, H., Klumpp, S., Schultz, J. E. & Joost, H. G. (1994) Molecular cloning of a protein serine/threonine phosphatase containing a putative regulatory tetratrincopeptide repeat domain. J. Biol. Chem. 269, 22586 22592.
2. Bennett, N. & Sitaramayya, A. (1988) Inactivation of photoexcited rhodopsin in retinal rods: the roles of rhodopsin kinase and 48-kDa protein (arrestin), Biochemistry 27, 1710-1715.
3. Bialojan, C. & Takai, A. (1988) Inhibitory effect of a marine-sponge toxin, okadaie acid, on protein phosphatases: specificity and kinetics, Biochem. J. 256, 283-290.
4. ks222, Visual Neurosci. 7, 35-48.
5. Brewis, N. D., Street, A. J., Prescott, A. R. & Cohen, P. T. W. (1993) PPX, a novel protein serine/threonine phosphatase localized to centrosomes, EMBO J. 12, 987-996.
6. Byk, T., Bar-Yaacov, M., Doza, Y. N., Minke, B. & Selinger, Z. (1993) Regulatory arrestin cycle secures the fidelity and maintenance of the fly photoreceptor cell, Proc. Natl Acad. Sci. USA 90, 1907-1911.
7. 2+-dependent interaction of recoverin with rhodopsin kinase, J. Biol. Chem. 270, 18060-18066.
8. Chen, M. X., McPartlin, A. E., Brown, L., Chen, Y. H., Barker, H. M. & Cohen, P. T. W. (1994) A novel human protein serine/threonine phosphatase, which possesses four tetratricopeptide repeat motifs and localizes to the nucleus, EMBO J. 13, 4278-4290.
9. Cheung, W.-T., Richards, D. E. & Rogers, J. H. (1993) Calcium binding by chick calretinin and rat calbindin D28k synthesised in bacteria, Eur. J. Biochem. 215, 401-410.
10. Cohen, P. & Klee, C. B. (1988) Criteria required to demonstrate calmodulin-dependent effects in vivo, in Molecular aspects of cellular regulation (Cohen, P & Klee, C. B., eds) vol. 5, pp. 357-364, Elsevier, Amsterdam.
11. Cohen, P. (1989) The structure and regulation of protein phosphatases, Annu. Rev. Biochem. 58, 453-508.
12. Cohen, P. & Cohen, P. T. W. (1989) Protein phosphatases come of age, J. Biol. Chem. 264, 21435-21438.
13. Cohen, P., Klumpp, S. & Schelling, D. L. (1989) An improved procedure for identifying and quantitating protein phosphatases in mammalian tissues, FEBS Lett. 250, 596-600.
14. Cook, W. J., Walter, L. J. & Walter, M. R. (1994) Drug binding by calmodulin: crystal structure of a calmodulin-trifluoperazine complex, Biochemistry 33, 15259-15265.
15. De Castro, E., Nef, S., Fiumelli, H., Lenz, S. E., Kawamura, S. & Nef, P. (1995) Regulation of rhodopsin phosphorylation by a family of neuronal calcium sensors, Biochem. Biophys. Res. Commun. 216, 133-140.
16. Ekman, P. & Jäger, O. (1993) Quantification of subnanomolar amounts of phosphate bound to seryl and threonyl residues in phosphoproteins using alkaline hydrolysis and malachite green, Anal. Biochem. 214, 138-141.
17. Fabiato, A. (1988) Computer programs for calculating total from specified or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol, 157, 378-417.
18. Foulkes, J. G., Erikson, E. & Erikson, R. L. (1983) Separation of multiple phosphotyrosyl- and phosphoseryl-protein phosphatases from chicken brain, J. Biol. Chem. 258, 431-438.
19. Fowles, C., Akhtar, M. & Cohen, P (1989) Interplay of phosphorylation and dephosphorylation in vision: protein phosphatases of bovine rod outer segments, Biochemistry 28, 9385-9391.
20. Gorodovikova, E. N. & Philippov, P. P. (1993) The presence of a calcium-sensitive p26-containing complex in bovine retina rod cells, FEBS Lett. 335, 277-279.
21. Gorodovikova, E. N., Gimelbrant, A. A., Senin, I. I. & Philippov, P. P. (1994) Recoverin mediates the calcium effect upon rhodopsin phosphorylation and cGMP hydrolysis in bovine retina rod cells. FEBS Lett. 349, 187-190.
22. Gray-Keller, M. P. & Detwiler, P. B. (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods, Neuron 13, 849-861.
23. Greene, N. M., Williams, D. S. & Newton, A. C. (1995) Kinetics and localisation of the phosphorylation of rhodopsin by protein kinase C, J. Biol. Chem. 270, 6710-6717.
24. Haystead, T. A. J., Sim, A. T. R., Carling, D., Honnor, R. C., Tsukitani, Y., Cohen, P. & Hardie, D. G. (1989) Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism, Nature 337, 78-81.
25. Honkanen, R. E., Zwiller, J., Daily, S. L., Khatra, B. S., Dukelow, M. & Boynton, A. L. (1991) Identification, purification, and characterization of a novel serine/threonine protein phosphatase from bovine brain. J. Biol. Chem. 268, 6614-6619.
26. Hsu, Y.-T. & Molday, R. S. (1993) Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361, 76-79.
27. Ingebritsen, T. S. & Cohen, P. (1983) Protein phosphatases: properties and role in cellular regulation, Science 221, 331-338.
28. 2+ in vertebrate photoreceptor excitation and adaptation. Annu. Rev. Physiol. 153, 153-175.
29. Kawamura, S. (1993) Rhodopsin phosphorylation as a mechanism of cyclic GMP phosphodiesterase regulation by S-modulin. Nature 362, 855-857.
30. Kawamura, S., Hisatomi, O., Kayada, S., Tokunaga, F. & Kuo, C.-H. (1993) Recoverin has S-modulin activity in frog rods, J. Biol. Chem. 268, 14579-14582.
31. King, A. J., Anjelkovic, N., Hemmings, B. A. & Akhtar, M. (1994) The phosphoopsin phosphatase from bovine rod outer segments. An insight into the mechanism of stimulation of type-2A protein phosphatase activity by protamine. Eur. J. Biochem. 225, 383-394.
32. Klenchin, V. A., Calvert, P. D. & Bownds, M. D. (1995) Inhibition of rhodopsin kinase by recoverin. Further evidence for a negative feedback system in phototransduction. J. Biol. Chem. 270, 16147-16152.
33. Koch, K.-W. & Stryer, L. (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions, Nature 334, 64-66.
34. Kühn, H. (1974) Light-dependent phosphorylation of rhodopsin in living frogs. Nature 250, 588-590.
35. Kutuzov, M. A. & Bennett, N. (1995) Calcium-activated opsin dephosphorylation in retinal rod outer segments. Abstr. 23rd FEBS Meet., no. P27.9.
36. Lagnado, L. & Baylor, D. A. (1994) Calcium controls light-triggered formation of catalytically active rhodopsin. Nature 367, 273-277.
37. Lambrecht, H.-G. & Koch, K.-W. (1991) A 26 kd calcium binding protein from bovine rod outer segments as modulator of photoreceptor guanylate cyclase, EMBO J. 10, 793-798.
38. Lawson, J. E., Niu, S.-D., Browning, K. S., Trong, H. L., Yan, J. & Reed, L. J. (1993) Molecular cloning and expression of the catalytic subunit of bovine pyruvate dehydrogenase phosphatase and sequence similarity with protein phosphatase 2C. Biochemistry 32, 8987-8993.
39. McCarthy, S. T., Younger, J. P. & Owen, W. G. (1994) Free calcium concentrations in the bullfrog rods determined in the presence of multiple forms of Fura-2, Biophys. J. 67, 2076-2089.
40. McDowell, J. H., Nawrocki, J. P. & Hargrave, P. (1993) Phosphorylation sites in bovine rhodopsin, Biochemistry 32, 4968-4964.
41. McNaughton, P. A., Cervetto, L. & Nunn, B. J. (1986) Measurement of the intracellular free calcium concentration in salamander rods, Nature 322, 261-263.
42. Ohguro, H., Palczewski, K., Ericsson, L. H., Walsh, K. A. & Johnson, R. S. (1993) Sequential phosphorylation of rhodopsin at multiple sites, Biochemistry 28, 5718-5724.
43. Ohguro, H., Johnson, R. S., Ericsson, L. H., Walsh, K. A. & Palczewski, K. (1994) Control of rhodopsin multiple phosphorylation, Biochemistry 33, 1023-1028.
44. Ohguro, H., Van Hooser, J. P., Milam, A. H. & Palczewski, K. (1995) Rhodopsin phosphorylation and dephosphorylation in vivo, J. Biol. Chem. 270, 14259-14262.
45. Palczewski, K., Hargrave, P. A., McDowell, J. H. & Ingebritsen, T. S. (1989a) The catalytic subunit of phosphatase 2A dephosphorylates phosphoopsin, Biochemistry 28, 415-419.
46. Palczewski, K., McDowell, J. H., Jakes, S., Ingebritsen, T. S. & Hargrave, P. A. (1989b) Regulation of rhodopsin dephosphorylation by arrestin, J. Biol. Chem. 264, 15770-15773.
47. Papac, D. I., Oatis, J. E. Jr. Crouch, R. K. & Knapp, D. R. (1993) Mass spectrometric identification of phosphorylation sites in bleached bovine rhodopsin, Biochemistry 32, 5930-5934.
48. Posas, F., Bollen, M., Stalmans, W. & Ariño, J. (1995) Biochemical characterization of recombinant yeast PPZI, a protein phosphatase involved in salt tolerance, FEBS Lett. 368, 39-44.
49. Premont, R. T., Inglese, J. & Lefkowitz, R. J. (1995) Protein kinases that phosphorylate activated G-protein coupled receptors, FASEB J. 9, 175-182.
50. Pugh, E. N. Jr & Lamb, T. D. (1990) Cyclic GMP and calcium: the internal messengers of excitation and adaptation in vertebrate photoreceptors, Vision Res. 30, 1923-1948.
51. Pullen, N. & Akhtar, M. (1994). Rhodopsin kinase: studies on the sequence of and the recognition motif for multiphosphorylation. Biochemistry 33, 14536-14542.
52. Ratto, G. M., Payne, R., Owen, W. G. & Tsien, R. Y. (1988) The concentration of cytosolic free calcium in vertebrate rod outer segments measured with Fura-2, J. Neurosci. 8, 3240-3246.
53. Shuster, T. A., Nagy, A. K., Conly, D. C. & Farber, D. B. (1992) Direct zinc binding to purified rhodopsin and disc membranes, Biochem. J. 282, 123-128.
54. Sitaramayya, A. (1986) Rhodopsin kinase prepared from bovine rod disk membranes quenches light activation of cGMP phosphodiesterase in reconstituted system. Biochemistry 25, 5460-5468.
55. Steele, F. R., Washburn, T., Rieger, R. & O'Tousa, J. E. (1992) Drosophila retinal degeneration C (rdgC) encodes a novel serine/threonine protein phosphatase, Cell 59, 669-676.
56. Stemmer, P. M. & Klee, C. B. (1994) Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B, Biochemistry 33, 6859-6866.
57. 2+/calmodulin-dependent protein phosphatase (2B) from rabbit skeletal muscle, Eur. J. Biochem. 132, 289-295.
58. Stryer, L. (1987) Visual transduction: design and recurring motifs, Chem. Scr. 27B, 161-171.
59. Sugino, Y. & Miyoshi, Y. (1964) The specific precipitation of orthophosphate and some biochemical applications, J. Biol. Chem. 239, 2360-2364.
60. Ting, T. D. & Ho, Y. K. (1991) Molecular mechanism of GTP hydrolysis by bovine transducin: pre-steady-state kinetic analysis. Biochemistry 30, 8996-9007.
61. 2+-calmodulin, Nature Struct. Biol. 1, 795-801.
62. Vivaudou, M. B., Arnoult, C. & Villaz, M. (1991) Skeletal muscle ATP-sensitive K+ channels recorded from sarcolemmal blebs of split fibers: ATP inhibition is reduced by magnesium and ADP, J. Membr. Biol. 122, 165-175.
63. Wilden, U. & Kühn, H. (1982) Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites, Biochemistry 21, 3014-3022.
64. Wilden, U., Hall, S. W. & Kühn, 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.
65. Yokoyama, N. & Wang, J. H. (1991) Demonstration and purification of multiple bovine brain and bovine lung calmodulin-stimulated phosphatase isozymes, J. Biol. Chem. 266, 14822-14829.