Differential modification of phosducin protein in degenerating rd1 retina is associated with constitutively active Ca2+ /calmodulin kinase II in rod outer segments

Molecular and Cellular Proteomics

Volumn 5, Issue 2, 2006, Pages 324-336

  Hauck, Stefanie M ^a   Ekström, Per A R ^b   Ahuja Jensen, Poonam ^b   Suppmann, Sabine ^a   Paquet Durand, Francois ^b   van Veen, Theo ^b   Ueffing, Marius ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ADAPTIN; CALCIUM; CALCIUM ION; ESTERASE; EYE PROTEIN; GUANYLATE KINASE; PHOSDUCIN; PHOSPHODIESTERASE 6 BETA; PROTEIN 14 3 3; PROTEIN CSN8; PROTEIN KINASE (CALCIUM,CALMODULIN) II; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COMPUTER ANALYSIS; CONTROLLED STUDY; DARK ADAPTATION; ENZYME ACTIVATION; GENE MUTATION; HISTOPATHOLOGY; LIGHT ADAPTATION; MASS SPECTROMETRY; MOLECULAR GENETICS; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PHOTORECEPTOR; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RETINA; RETINA ROD OUTER SEGMENT; RETINITIS PIGMENTOSA; TWO DIMENSIONAL GEL ELECTROPHORESIS; WILD TYPE;

ANIMALS; APOPTOSIS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DARK ADAPTATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME ACTIVATION; EYE PROTEINS; GTP-BINDING PROTEIN REGULATORS; MICE; MICE, INBRED C3H; MICE, MUTANT STRAINS; PHOSPHOPROTEINS; PHOSPHORYLATION; RETINAL DEGENERATION; ROD OUTER SEGMENTS;

ANIMALIA;

EID: 33644678324     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M500217-MCP200     Document Type: Article

References (77)

1. Farber, D. B., Park, S., and Yamashita, C. (1988) Cyclic GMP-phosphodiesterase of rd retina: biosynthesis and content. Exp. Eye. Res. 46, 363-374
2. Bowes, C., Li, T., Danciger, M., Baxter, L. C., Applebury, M. L and Farber, D. B. (1990) Retinal degeneration in the rd mouse is cause by a defect in the β subunit of rod cGMP-phosphodiesterase. Nature 347, 677-680
3. McLaughlin, M. E., Ehrhart, T. L., Berson, E. L., and Dryja, T. P. (1995) Mutation spectrum of the gene encoding the β subunit of rod phosphodiesterase among patients with autosomal recessive retinitis pigmentosa. Proc. Natl. Acad. Sci. U. S. A. 92, 3249-3253
4. Farber, D. B., and Lolley, R. N. (1974) Cyclic guanosine monophosphate: elevation in degenerating photoreceptor cells of the C3H mouse retina. Science 186, 449-451
5. Cobbs, W. H., and Pugh, E. N., Jr. (1985) Cyclic GMP can increase rod outer-segment light sensitive current 10-fold without delay of excitation. Nature 313, 585-587
6. Fesenko, E. E., Kolesnikov, S. S., and Lyubarsky, A. L. (1985) Induction by cyclic GMP of a cationic conductance in plasma membrane of retinal rod outer segment. Nature 313, 310-313
7. Fox, D. A., Poblenz, A. T., and He, L. (1999) Calcium overload triggers photoreceptor apoptotic cell death in chemical-induced and inherited retinal degenerations. Ann. N. Y. Acad. Sci. 893, 282-285
8. Fox, D. A., Poblenz, A. T., He, L., Harris, J. B., and Medrano, C. J. (2003) Pharmacological strategies to block rod photoreceptor apoptosis caused by calcium overload: a mechanistic target-site approach to neuroprotection. Eur. J. Ophthalmol. 13, Suppl. 3, S44-S56
9. He, L., Poblenz, A. T., Medrano, C. J., and Fox, D. A. (2000) Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J. Biol. Chem. 275, 12175-12184
10. Chang, G. Q., Hao, Y., and Wong, F. (1993) Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron 11, 595-605
11. Lolley, R. N., Rong, H., and Craft, C. M. (1994) Linkage of photoreceptor degeneration by apoptosis with inherited defect in phototransduction. Investig. Ophthalmol. Vis. Sci. 35, 358-362
12. Portera-Cailliau, C., Sung, C. H., Nathans, J., and Adler, R. (1994) Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa. Proc. Natl. Acad. Sci. U. S. A. 91, 974-978
13. Frasson, M., Sahel, J. A., Fabre, M., Simonutti, M., Dreyfus, H., and Picaud, S. (1999) Retinitis pigmentosa: rod photoreceptor rescue by a calcium-channel blocker in the rd mouse. Nat. Med. 5, 1183-1187
14. Takano, Y., Ohguro, H., Dezawa, M., Ishikawa, H., Yamazaki, H., Ohguro, I., Mamiya, K., Metoki, T., Ishikawa, F., and Nakazawa, M. (2004) Study of drug effects of calcium channel blockers on retinal degeneration of rd mouse. Biochem. Biophys. Res. Commun. 313, 1015-1022
15. Jomary, C., Neal, M. J., and Jones, S. E. (2001) Characterization of cell death pathways in murine retinal neurodegeneration implicates cytochrome c release, caspase activation, and bid cleavage. Mol. Cell. Neurosci. 18, 335-346
16. Kim, D. H., Kim, J.-A., Choi, J.-S., and Joo, C. K. (2002) Activation of caspase-3 during degeneration of the outer nuclear layer in the rd mouse. Ophthalmic Res. 34, 150-157
17. Sharma, A. K., and Rohrer, B. (2004) Calcium-induced calpain mediates apoptosis via caspase-3 in a mouse photoreceptor cell line. J. Biol. Chem. 279, 35564-35572
18. Doonan, F., Donovan, M., and Cotter, T. G. (2003) Caspase-independent photoreceptor apoptosis in mouse models of retinal degeneration. J. Neurosci. 23, 5723-5731
19. Yoshizawa, K., Kiuchi, K., Nambu, H., Yang, J., Senzaki, H., Kiyozuka, Y., Shikata, N., and Tsubura, A. (2002) Caspase-3 inhibitor transiently delays inherited retinal degeneration in C3H mice carrying the rd gene. Graefe's Arch. Clin. Exp. Ophthalmol. 240, 214-219
20. Zeiss, C. J., Neal, J., and Johnson, E. A. (2004) Caspase-3 in postnatal retinal development and degeneration. Investig. Ophthalmol. Vis. Sci. 45, 964-970
21. Hopp, R. M., Ransom, N., Hilsenbeck, S. G., Papermaster, D. S., and Windle, J. J. (1998) Apoptosis in the murine rd1 retinal degeneration is predominantly p53-independent. Mol. Vis. 4, 5-8
22. Hafezi, F., Abegg, M., Grimm, C., Wenzel, A., Stuermer, J., Farber, D. B., and Reme, C. E. (1998) Retinal degeneration in the rd mouse in the absence of c-fos. Investig. Ophthalmol. Vis. Sci. 38, 2239-2244
23. Hafezi, F., Steinbach, J. P., Marti, A., Munz, K., Wang, Z. Q., Wagner, E. F., Aguzzi, A., and Reme, C. E. (1997) The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 3, 346-349
24. Chen, J., Flannery, J. G., LaVail, M. M., Steinberg, R. H., Xu, J., and Simon, M. I. (1996) bcl-2 overexpression reduces apoptotic photoreceptor cell death in three different retinal degenerations. Proc. Natl. Acad. Sci. U. S. A. 93, 7042-7047
25. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., Huarte, J., and Martinou, J. C. (1994) Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc. Natl. Acad. Sci. U. S. A. 91, 3309-3313
26. Johnson, L. E., van Veen, T., and Ekström, P. A. (2005) Differential Akt activation in the photoreceptors of normal and rd1 mice. Cell Tissue Res. 320, 213-222
27. Jones, S. E., Jomary, C., Grist, J., Stewart, H. J., and Neal, M. J. (2000) Identification by array screening of altered nm23-M2/PuF mRNA expression in mouse retinal degeneration. Mol. Cell Biol. Res. Commun. 4, 20-25
28. Hackam, A. S., Strom, R., Liu, D., Qian, J., Wang, C., Otteson, D., Gunatilaka, T., Farkas, R. H., Chowers, I., Kageyama, M., Leveillard, T., Sahel, J. A., Campochiaro, P. A., Parmigiani, G., and Zack, D. J. (2004) Identification of gene expression changes associated with the progression of retinal degeneration in the rd1 mouse. Investig. Ophthalmol. Vis. Sci. 45, 2929-2942
29. Rohrer, B., Pinto, F. R., Hulse, K. E., Lohr, H. R., Zhang, L., and Almeida, J. S. (2004) Multidestructive pathways triggered in photoreceptor cell death of the rd mouse as determined through gene expression profiling. J Biol. Chem. 279, 41903-41910
30. Cavusoglu, N., Thierse, D., Mohand-Said, S., Chalmel, F., Poch, O., Van Dorsselaer, A., Sahel, J. A., and Leveillard, T. (2003) Differential proteomic analysis of the mouse retina: the induction of crystallin proteins by retinal degeneration in the rd1 mouse. Mol. Cell. Proteomics 2, 494-505
31. Hauck, S. M., Schöffmann, S., Deeg, C. A., Gloeckner, J. C., Swiatek-de Lange, M., and Ueffing, M. (2005) Proteomic analysis of porcine interphotoreceptor matrix. Proteomics 14, 3623-3636
32. Blum, H., Beier, H., and Gross, H. J. (1987) Improved silver staining of plant proteins, RNA, and DNA in polyacrylamide gels. Electrophoresis 8, 93-99
33. Gharahdaghi, F., Weinberg, C. R., Meagher, D. A., Imai, B. S., and Mische, S. M. (1999) Mass spectrometric identification of proteins from silver-stained polyacrylamide gel: a method for the removal of silver ions to enhance sensitivity. Electrophoresis 20, 601-605
34. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence data-bases using mass spectrometry data. Electrophoresis 20, 3551-3567
35. Bowes, C., Danciger, M., Kozak, C. A., and Farber, D. B. (1989) Isolation of a candidate cDNA for the gene causing retinal degeneration in the rd mouse. Proc. Natl. Acad. Sci. U. S. A. 86, 9722-9726
36. Farber, D. B., and Lolley, R. N. (1976) Enzymatic basis for cyclic GMP accumulation in degenerative photoreceptor cells of mouse retina. J. Cyclic Nucleotide Res. 2, 139-148
37. Lee, R. H., Ting, T. D., Lieberman, B. S., Tobias, D. E., Lolley, R. N., and Ho, Y. K. (1992) Regulation of retinal cGMP cascade by phosducin in bovine rod photoreceptor cells. Interaction of phosducin and transducin. J. Biol. Chem. 267, 25104-25112
38. Yoshida, T., Willardson, B. M., Wilkins, J. F., Jensen, G. J., Thornton, B. D., and Bitensky, M. W. (1994) The phosphorylation state of phosducin determines its ability to block transducin subunit interactions and inhibit transducin binding to activated rhodopsin. J. Biol. Chem. 269, 24050-24057
39. Lee, R. H., Brown, B. M., and Lolley, R. N. (1990) Protein kinase A phosphorylates retinal phosducin on serine 73 in situ. J. Biol. Chem. 265, 15860-15866
40. Ruiz-Gomez, A., Humrich, J., Murga, C., Quitterer, U., Lohse, M. J., and Mayor, F., Jr. (2000) Phosphorylation of phosducin and phosducin-like protein by G protein-coupled receptor kinase 2. J. Biol. Chem. 275, 29724-29730
41. 2+/ calmodulin-dependent protein kinase II phosphorylation and 14-3-3 protein binding. J. Biol. Chem. 276, 23805-23815
42. Lee, B. Y., Thulin, C. D., and Willardson, B. M. (2004) Site-specific phosphorylation of phosducin in intact retina. Dynamics of phosphorylation and effects on G protein βγ dimer binding. J. Biol. Chem. 279, 54008-54017
43. Sokolov, M., Strissel, K. J., Leskov, I. B., Michaud, N. A., Govardovskii, V. I., and Arshavsky, V. Y. (2004) Phosducin facilitates light-driven transducin translocation in rod photoreceptors. Evidence from the phosducin knockout mouse. J. Biol. Chem. 279, 19149-19156
44. 2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu. Rev. Biochem. 71, 473-510
45. Pochet, R., Pasteels, B., Seto-Ohshima, A., Bastianelli, E., Kitajima, S., and Van Eldik, L. J. (1991) Calmodulin and calbindin localization in retina from six vertebrate species. J. Comp. Neurol. 314, 750-762
46. 2+ /calmodulin-dependent protein kinase II in the mouse retina. Brain Res. Mol. Brain Res. 82, 150-166
47. Means, A. R. (2000) Regulatory cascades involving calmodulin-dependent protein kinases. Mol. Endocrinol. 14, 4-13
48. Kennedy, M. B. (1998) Signal transduction molecules at the glutamatergic postsynaptic membrane. Brain Res. Brain Res. Rev. 26, 243-257
49. Fei, Y. (2003) Development of the cone photoreceptor mosaic in the mouse retina revealed by fluorescent cones in transgenic mice. Mol. Vis. 9, 31-42
50. Nakano, K., Chen, J., Tarr, G. E., Yoshida, T., Flynn, J. M., and Bitensky, M. W. (2001) Rethinking the role of phosducin: light-regulated binding of phosducin to 14-3-3 in rod inner segments. Proc. Natl. Acad. Sci. U. S. A. 98, 4693-4698
51. Lykke-Andersen, K., and Wei, N. (2003) Gene structure and embryonic expression of mouse COP9 signalosome subunit 8 (Csn8). Gene (Amst.) 321, 65-72
52. Harari-Steinberg, 0., and Chamovitz, D. A. (2004) The COP9 signalosome: mediating between kinase signaling and protein degradation. Curr. Protein Pept. Sci. 3, 185-189
53. Suh, G. S., Poeck, B., Chouard, T., Oron, E., Segal, D., Chamovitz, D. A., and Zipursky, S. L. (2002) Drosophila JAB1/CSN5 acts in photoreceptor cells to induce glial cells. Neuron 33, 35-46
54. Roseboom, P. H., Weller, J. L., Babila, T., Aitken, A., Sellers, L. A., Moffett, J. R., Namboodiri, M. A., and Klein, D. C. (1994) Cloning and characterization of the ε and ζ isoforms of the 14-3-3 proteins. DNA Cell Biol. 13, 629-640
55. Ponnambalam, S., Robinson, M. S., Jackson, A. P., Peiperl, L., and Parham, P. (1990) Conservation and diversity in families of coated vesicle adaptins. J. Biol. Chem. 265, 4814-4820
56. Robinson, M. S. (1994) The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 4, 538-544
57. Druck, T., Gu, Y., Prabhala, G., Cannizzaro, L. A., Park, S.-H., Huebner, K., and Keen, J. H. (1995) Chromosome localization of human genes for clathrin adaptor polypeptides AP2-β and AP50 and the clathrin-binding protein, VCP. Genomics 30, 94-97
58. Santini, F., Gaidarov, I., and Keen, J. H. (2002) G protein-coupled receptor/arrestin3 modulation of the endocytic machinery. J. Cell Biol. 156, 665-676
59. Gaidarov, I. O., Suslov, O. N., and Abdulaev, N. G. (1993) Enzymes of the cyclic GMP metabolism in bovine retina. I. Cloning and expression of the gene for guanylate kinase. FEBS Lett. 335, 81-84
60. Gray-Keller, M. P., and Detwiler, P. B. (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13, 849-861
61. Brown, B. M., Carlson, B. L., Zhu, X., Lolley, R. N., and Craft, C. M. (2002) Light-driven translocation of the protein phosphatase 2A complex regulates light/dark dephosphorylation of phosducin and rhodopsin. Biochemistry 41, 13526-13538
62. Lee, R. H., Brown, B. M., and Lolley, R. N. (1984) Light-induced dephosphorylation of a 33K protein in rod outer segments of rat retina. Biochemistry 23, 1972-1977
63. Tian, N., and Copenhagen, D. R. (2001) Visual deprivation alters development of synaptic function in inner retina after eye opening. Neuron 32, 439-449
64. Xue, J., Li, G., Laabich, A., and Cooper, N. G. (2001) Visual-mediated regulation of retinal CaMKII and its GluR1 substrate is age-dependent. Mol. Brain Res. 93, 95-104
65. Benke, T. A., Luthi, A., Isaa, J. T., and Collinridge, G. L. (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793-797
66. 2+/calmodulin-kinase II enhances channel conductance of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. U. S. A. 96, 3269-3274
67. Wakakura, M., and Yamamoto, N. (1987) Immunological localization of calmodulin in feline rod outer segments. Exp. Eye Res. 44, 451-458
68. Hsu, Y. T., and Molday, R. S. (1994) Interaction of calmodulin with the cyclic GMP-gated channel of rod photoreceptor cells. Modulation of activity, affinity purification, and localization. J. Biol. Chem. 269, 29765-29770
69. Kovacs, B., and Gulya, K. (2003) Calmodulin gene expression in the neural retina of the adult rat. Life Sci. 73, 3213-3224
70. Hargrave, P. A. (1986) Molecular dynamics of the rod cell, in The Retina. A Model for Cell Biology Studies. Part I. (Adler, R., and Farber, D., eds) pp. 207-237, Academic Press, New York
71. 2+-binding protein (CABP) subfamily with similarity to calmodulin. J. Biol. Chem. 275, 1247-1260
72. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci. 10, 1079-1087
73. Haeseleer, F., Imanishi, Y., Sokal, I., Filipek, S., and Palczewski, K. (2002) Calcium-binding proteins: intracellular sensors from the calmodulin superfamily. Biochem. Biophys. Res. Commun. 290, 615-623
74. Palczewski, K., Sokal, I., and Baehr, W. (2004) Guanylate cyclase-activating proteins: structure, function, and diversity. Biochem. Biophys. Res. Commun. 322, 1123-1130
75. Nishiguchi, K. M., Sokal, I., Yang, L., Roychowdhury, N., Palczewski, K., Berson, E. L., Dryja, T. P., and Baehr, W. (2004) A novel mutation (1143NT) in guanylate cylase-activating protein 1 (GCAP1) associated with autosomal dominant cone degeneration. Investig. Ophthalmol. Vis. Sci. 45, 3863-3870
76. Sokal, I., Dupps, W. J., Grassi, M. A., Brown, J., Jr., Affatigato, L. M., Roychowdhury, N., Yang, L., Filipek, S., Palczewski, K., Stone, E. M., and Baehr, W. (2005) A novel GCAP1 missense mutation (L151F) in a large family with autosomal dominant cone-rod dystrophy (adCORD). Investig. Ophthalmol. Vis. Sci. 46, 1124-1132
77. 2+ and causes photoreceptor degeneration in transgenic mice. J. Neurosci. 24, 6078-6085