Induction of the unfolded protein response by constitutive g-protein signaling in rod photoreceptor cells

Journal of Biological Chemistry

Volumn 289, Issue 42, 2014, Pages 29310-29321

  Wang, Tian ^a,b   Chen, Jeannie ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; CELL MEMBRANES; PROTEINS; SIGNAL TRANSDUCTION; VISION;

CELL-DEATH PATHWAYS; PHOTON ABSORPTIONS; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; POTENTIAL TARGETS; ROD PHOTORECEPTORS; THERAPEUTIC INTERVENTION; UNFOLDED PROTEIN RESPONSE;

CELL SIGNALING;

AGENTS AFFECTING PROTEIN METABOLISM; GUANOSINE TRIPHOSPHATE; GUANYLYL CYCLASE ACTIVATING PROTEIN 2; PHOSPHODIESTERASE VI; PHOSPHOTRANSFERASE; PROTEIN KINASE LIKE ENDOPLASMIC RETICULUM KINASE; TRANSDUCIN; UNCLASSIFIED DRUG; BETA ARRESTIN; CNGB1 PROTEIN, MOUSE; CYCLIC NUCLEOTIDE GATED CHANNEL; GNAT1 PROTEIN, MOUSE; GRK1 PROTEIN, MOUSE; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; NERVE PROTEIN; RETINA S ANTIGEN; RHODOPSIN; RHODOPSIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; LIGHT DAMAGE; MOUSE; NONHUMAN; PHOTORECEPTOR CELL; PHOTOTRANSDUCTION; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; RETINA DEGENERATION; RETINA ROD; SIGNAL TRANSDUCTION; UBIQUITINATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; LIGHT; METABOLISM; MUTATION; RADIATION RESPONSE;

ANIMALS; ARRESTINS; CELL DEATH; CELL SURVIVAL; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ENDOPLASMIC RETICULUM STRESS; G-PROTEIN-COUPLED RECEPTOR KINASE 1; GTP-BINDING PROTEIN ALPHA SUBUNITS; GTP-BINDING PROTEINS; LIGHT; LIGHT SIGNAL TRANSDUCTION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NERVE TISSUE PROTEINS; RETINAL ROD PHOTORECEPTOR CELLS; RHODOPSIN; SIGNAL TRANSDUCTION; TRANSDUCIN; UNFOLDED PROTEIN RESPONSE;

EID: 84908112250     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.595207     Document Type: Article

References (57)

1. LaVail, M. M., Gorrin, G. M., Yasumura, D., and Matthes, M. T. (1999) Increased susceptibility to constant light in nr and pcd mice with inherited retinal degenerations. Invest. Ophthalmol. Vis. Sci. 40, 1020-1024
2. Athanasiou, D., Aguilà, M., Bevilacqua, D., Novoselov, S. S., Parfitt, D. A., and Cheetham, M. E. (2013) The cell stress machinery and retinal degeneration. FEBS Lett. 587, 2008-2017
3. Mitchell, P., Smith, W., and Wang, J. J. (1998) Iris color, skin sun sensitivity, and age-related maculopathy: the Blue Mountains Eye Study. Ophthalmology 105, 1359-1363
4. Sui, G. Y., Liu, G. C., Liu, G. Y., Gao, Y. Y., Deng, Y., Wang, W. Y., Tong, S. H., and Wang, L. (2013) Is sunlight exposure a risk factor for age-related macular degeneration? A systematic review and meta-analysis. Br. J. Ophthalmol. 97, 389-394
5. Noell, W. K., Walker, V. S., Kang, B. S., and Berman, S. (1966) Retinal damage by light in rats. Invest. Ophthalmol. 5, 450-473
6. Youssef, P. N., Sheibani, N., and Albert, D. M. (2011) Retinal light toxicity. Eye 25, 1-14
7. Grimm, C., Wenzel, A., Hafezi, F., Yu, S., Redmond, T. M., and Remé, C. E. (2000) Protection of Rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat. Genet. 25, 63-66
8. Hao, W., Wenzel, A., Obin, M. S., Chen, C. K., Brill, E., Krasnoperova, N. V., Eversole-Cire, P., Kleyner, Y., Taylor, A., Simon, M. I., Grimm, C., Remé, C. E., and Lem, J. (2002) Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat. Genet. 32, 254-260
9. Donovan, M., Carmody, R. J., and Cotter, T. G. (2001) Light-induced photoreceptor apoptosis in vivo requires neuronal nitric-oxide synthase and guanylate cyclase activity and is caspase-3-independent. J. Biol. Chem. 276, 23000-23008
10. Grimm, C., Wenzel, A., Hafezi, F., and Remé, C. E. (2000) Gene expression in the mouse retina: the effect of damaging light. Mol. Vis. 6, 252-260
11. Hafezi, F., Steinbach, J. P., Marti, A., Munz, K., Wang, Z. Q., Wagner, E. F., Aguzzi, A., and Remé, C. E. (1997) The absence of c-fos prevents lightinduced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 3, 346-349
12. Wilden, U., and Kühn, H. (1982) Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21, 3014-3022
13. Wilden, U., Hall, S. W., and 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. U.S.A. 83, 1174-1178
14. Xu, J., Dodd, R. L., Makino, C. L., Simon, M. I., Baylor, D. A., and Chen, J. (1997) Prolonged photoresponses in transgenic mouse rods lacking arrestin. Nature 389, 505-509
15. Chen, J., Simon, M. I., Matthes, M. T., Yasumura, D., and LaVail, M. M. (1999) Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest. Ophthalmol. Vis. Sci. 40, 2978-2982
16. Chen, C. K., Burns, M. E., Spencer, M., Niemi, G. A., Chen, J., Hurley, J. B., Baylor, D. A., and Simon, M. I. (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc. Natl. Acad. Sci. U.S.A. 96, 3718-3722
17. Chen, J., Shi, G., Concepcion, F. A., Xie, G., Oprian, D., and Chen, J. (2006) Stable rhodopsin/arrestin complex leads to retinal degeneration in a transgenic mouse model of autosomal dominant retinitis pigmentosa. J. Neurosci. 26, 11929-11937
18. Moaven, H., Koike, Y., Jao, C. C., Gurevich, V. V., Langen, R., and Chen, J. (2013) Visual arrestin interaction with clathrin adaptor AP-2 regulates photoreceptor survival in the vertebrate retina. Proc. Natl. Acad. Sci. U.S.A. 110, 9463-9468
19. Fuchs, S., Nakazawa, M., Maw, M., Tamai, M., Oguchi, Y., and Gal, A. (1995) A homozygous 1-base pair deletion in the arrestin gene is a frequent cause of Oguchi disease in Japanese. Nat. Genet. 10, 360-362
20. Yamamoto, S., Sippel, K. C., Berson, E. L., and Dryja, T. P. (1997) Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat. Genet. 15, 175-178
21. Lisman, J., and Fain, G. (1995) Support for the equivalent light hypothesis for RP. Nat. Med. 1, 1254-1255
22. Wenzel, A., Reme, C. E., Williams, T. P., Hafezi, F., and Grimm, C. (2001) The Rpe65 Leu450Met variation increases retinal resistance against lightinduced degeneration by slowing rhodopsin regeneration. J. Neurosci. 21, 53-58
23. Rapp, L. M., and Williams, T. P. (1980) The role of ocular pigmentation in protecting against retinal light damage. Vision Res. 20, 1127-1131
24. Hunter, J. J., Morgan, J. I., Merigan, W. H., Sliney, D. H., Sparrow, J. R., and Williams, D. R. (2012) The susceptibility of the retina to photochemical damage from visible light. Prog. Retin. Eye Res. 31, 28-42
25. Burns, M. E., and Pugh, E. N., Jr. (2010) Lessons from photoreceptors: turning off G-protein signaling in living cells. Physiology 25, 72-84
26. Heck, M., and Hofmann, K. P. (2001) Maximal rate and nucleotide dependence of rhodopsin-catalyzed transducin activation: initial rate analysis based on a double displacement mechanism. J. Biol. Chem. 276, 10000-10009
27. Concepcion, F., Mendez, A., and Chen, J. (2002) The carboxyl-terminal domain is essential for rhodopsin transport in rod photoreceptors. Vision Res. 42, 417-426
28. Mendez, A., Burns, M. E., Sokal, I., Dizhoor, A. M., Baehr, W., Palczewski, K., Baylor, D. A., and Chen, J. (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc. Natl. Acad. Sci. U.S.A. 98, 9948-9953
29. Palczewski, K., Sokal, I., and Baehr, W. (2004) Guanylate cyclase-activating proteins: structure, function, and diversity. Biochem. Biophys. Res. Commun. 322, 1123-1130
30. Schnetkamp, P. P. (1986) Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J. Physiol. 373, 25-45
31. Ames, J. B., Dizhoor, A. M., Ikura, M., Palczewski, K., and Stryer, L. (1999) Three-dimensional structure of guanylyl cyclase activating protein-2, a calcium-sensitive modulator of photoreceptor guanylyl cyclases. J. Biol. Chem. 274, 19329-19337
32. Lin, J. H., Walter, P., and Yen, T. S. (2008) Endoplasmic reticulum stress in disease pathogenesis. Annu. Rev. Pathol. 3, 399-425
33. Shinde, V. M., Sizova, O. S., Lin, J. H., LaVail, M. M., and Gorbatyuk, M. S. (2012) ER stress in retinal degeneration in S334ter Rho rats. PLoS One 7, e33266
34. Salminen, A., Kauppinen, A., Hyttinen, J. M., Toropainen, E., and Kaarniranta, K. (2010) Endoplasmic reticulum stress in age-related macular degeneration: trigger for neovascularization. Mol. Med. 16, 535-542
35. Choudhury, S., Bhootada, Y., Gorbatyuk, O., and Gorbatyuk, M. (2013) Caspase-7 ablation modulates UPR, reprograms TRAF2-JNK apoptosis and protects T17M rhodopsin mice from severe retinal degeneration. Cell Death Dis. 4, e528
36. Griciuc, A., Aron, L., and Ueffing, M. (2011) ER stress in retinal degeneration: a target for rational therapy? Trends Mol. Med. 17, 442-451
37. Pfaffenbach, K. T., and Lee, A. S. (2011) The critical role of GRP78 in physiologic and pathologic stress. Curr. Opin. Cell Biol. 23, 150-156
38. Zhong, H., Molday, L. L., Molday, R. S., and Yau, K. W. (2002) The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420, 193-198
39. Hüttl, S., Michalakis, S., Seeliger, M., Luo, D. G., Acar, N., Geiger, H., Hudl, K., Mader, R., Haverkamp, S., Moser, M., Pfeifer, A., Gerstner, A., Yau, K. W., and Biel, M. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J. Neurosci. 25, 130-138
40. Zhang, Y., Molday, L. L., Molday, R. S., Sarfare, S. S., Woodruff, M. L., Fain, G. L., Kraft, T. W., and Pittler, S. J. (2009) Knockout of GARPs and the β-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J. Cell Sci. 122, 1192-1200
41. Mockel, A., Obringer, C., Hakvoort, T. B., Seeliger, M., Lamers, W. H., Stoetzel, C., Dollfus, H., and Marion, V. (2012) Pharmacological modulation of the retinal unfolded protein response in Bardet-Biedl syndrome reduces apoptosis and preserves light detection ability. J. Biol. Chem. 287, 37483-37494
42. Roca, A., Shin, K. J., Liu, X., Simon, M. I., and Chen, J. (2004) Comparative analysis of transcriptional profiles between two apoptotic pathways of light-induced retinal degeneration. Neuroscience 129, 779-790
43. Rzymski, T., Milani, M., Singleton, D. C., and Harris, A. L. (2009) Role of ATF4 in regulation of autophagy and resistance to drugs and hypoxia. Cell Cycle 8, 3838-3847
44. Tsang, S. H., Gouras, P., Yamashita, C. K., Kjeldbye, H., Fisher, J., Farber, D. B., and Goff, S. P. (1996) Retinal degeneration in mice lacking the gamma subunit of the rod cGMP phosphodiesterase. Science 272, 1026-1029
45. Raport, C. J., Lem, J., Makino, C., Chen, C. K., Fitch, C. L., Hobson, A., Baylor, D., Simon, M. I., and Hurley, J. B. (1994) Downregulation of cGMP phosphodiesterase induced by expression of GTPase-deficient cone transducin in mouse rod photoreceptors. Invest. Ophthalmol. Vis. Sci. 35, 2932-2947
46. Kerov, V., Chen, D., Moussaif, M., Chen, Y. J., Chen, C. K., and Artemyev, N. O. (2005) Transducin activation state controls its light-dependent translocation in rod photoreceptors. J. Biol. Chem. 280, 41069-41076
47. Mao, W., Miyagishima, K. J., Yao, Y., Soreghan, B., Sampath, A. P., and Chen, J. (2013) Functional comparison of rod and cone Gαt on the regulation of light sensitivity. J. Biol. Chem. 288, 5257-5267
48. Cachafeiro, M., Bemelmans, A. P., Samardzija, M., Afanasieva, T., Pournaras, J. A., Grimm, C., Kostic, C., Philippe, S., Wenzel, A., and Arsenijevic, Y. (2013) Hyperactivation of retina by light in mice leads to photoreceptor cell death mediated by VEGF and retinal pigment epithelium permeability. Cell Death Dis. 4, e781
49. Wenzel, A., Grimm, C., Samardzija, M., and Remé, C. E. (2005) Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog. Retin. Eye Res. 24, 275-306
50. Hoyo, N. L., López-Begines, S., Rosa, J. L., Chen, J., and Méndez, A. (2014) Functional EF-hands in neuronal calcium sensor GCAP2 determine its phosphorylation state and subcellular distribution in vivo, and are essential for photoreceptor cell integrity. PLoS Genet. 10, e1004480
51. Bennett, E. J., Bence, N. F., Jayakumar, R., and Kopito, R. R. (2005) Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell 17, 351-365
52. Chertov, A. O., Holzhausen, L., Kuok, I. T., Couron, D., Parker, E., Linton, J. D., Sadilek, M., Sweet, I. R., and Hurley, J. B. (2011) Roles of glucose in photoreceptor survival. J. Biol. Chem. 286, 34700-34711
53. Okawa, H., Sampath, A. P., Laughlin, S. B., and Fain, G. L. (2008) ATP consumption by mammalian rod photoreceptors in darkness and in light. Curr. Biol. 18, 1917-1921
54. Kunte, M. M., Choudhury, S., Manheim, J. F., Shinde, V. M., Miura, M., Chiodo, V. A., Hauswirth, W. W., Gorbatyuk, O. S., and Gorbatyuk, M. S. (2012) ER stress is involved in T17M rhodopsin-induced retinal degeneration. Invest. Ophthalmol. Vis. Sci. 53, 3792-3800
55. Gorbatyuk, M. S., Knox, T., LaVail, M. M., Gorbatyuk, O. S., Noorwez, S. M., Hauswirth, W. W., Lin, J. H., Muzyczka, N., and Lewin, A. S. (2010) Restoration of visual function in P23H rhodopsin transgenic rats by gene delivery of BiP/Grp78. Proc. Natl. Acad. Sci. U.S.A. 107, 5961-5966
56. Kudo, T., Kanemoto, S., Hara, H., Morimoto, N., Morihara, T., Kimura, R., Tabira, T., Imaizumi, K., and Takeda, M. (2008) A molecular chaperone inducer protects neurons from ER stress. Cell Death Differ. 15, 364-375
57. Tsaytler, P., Harding, H. P., Ron, D., and Bertolotti, A. (2011) Selective inhibition of a regulatory subunit of protein phosphatase 1 restores proteostasis. Science 332, 91-94