Robust Endoplasmic Reticulum-Associated Degradation of Rhodopsin Precedes Retinal Degeneration

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 679-695

  Chiang, Wei Chieh ^a   Kroeger, Heike ^a   Sakami, Sanae ^c   Messah, Carissa ^a   Yasumura, Douglas ^b   Matthes, Michael T ^b   Coppinger, Judith A ^a,d   Palczewski, Krzysztof ^c   LaVail, Matthew M ^b   Lin, Jonathan H ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Endoplasmic reticulum associated degradation; ER stress; Retinal degeneration; Rhodopsin; Rod photoreceptor; Unfolded protein response

Indexed keywords

MESSENGER RNA; RHODOPSIN; STRESS ACTIVATED PROTEIN KINASE; ERN2 PROTEIN, MOUSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MEMBRANE PROTEIN; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ERAD GENE; FEMALE; GENE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHOTORECEPTOR CELL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; RETINA DEGENERATION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; C57BL MOUSE; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; GENE TARGETING; GENETICS; IMMUNOPRECIPITATION; METABOLISM; NEWBORN; PATHOLOGY; PHOTORECEPTOR INNER SEGMENT; RETINA; UBIQUITINATION; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE KNOCK-IN TECHNIQUES; IMMUNOPRECIPITATION; MEMBRANE PROTEINS; MICE, INBRED C57BL; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; RETINA; RETINAL DEGENERATION; RETINAL PHOTORECEPTOR CELL INNER SEGMENT; RHODOPSIN; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR CHOP; UBIQUITINATION;

EID: 84937977937     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-014-8881-8     Document Type: Article

References (71)

1. Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334(6059):1081–1086. doi:10.1126/science.1209038
2. Smith MH, Ploegh HL, Weissman JS (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334(6059):1086–1090. doi:10.1126/science.1209235
3. Sun S, Shi G, Han X, Francisco AB, Ji Y, Mendonca N, Liu X, Locasale JW, Simpson KW, Duhamel GE, Kersten S, Yates JR 3rd, Long Q, Qi L (2014) Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival. Proc Natl Acad Sci U S A 111(5):E582–591. doi:10.1073/pnas.1318114111
4. Fritz JM, Dong M, Apsley KS, Martin EP, Na CL, Sitaraman S, Weaver TE (2014) Deficiency of the BiP cochaperone ERdj4 causes constitutive endoplasmic reticulum stress and metabolic defects. Mol Biol Cell 25(4):431–440. doi:10.1091/mbc.E13-06-0319
5. Luo S, Mao C, Lee B, Lee AS (2006) GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol 26(15):5688–5697. doi:10.1128/MCB.00779-06
6. Eura Y, Yanamoto H, Arai Y, Okuda T, Miyata T, Kokame K (2012) Derlin-1 deficiency is embryonic lethal, Derlin-3 deficiency appears normal, and Herp deficiency is intolerant to glucose load and ischemia in mice. PLoS ONE 7(3):e34298. doi:10.1371/journal.pone.0034298
7. Muller JM, Deinhardt K, Rosewell I, Warren G, Shima DT (2007) Targeted deletion of p97 (VCP/CDC48) in mouse results in early embryonic lethality. Biochem Biophys Res Commun 354(2):459–465. doi:10.1016/j.bbrc.2006.12.206
8. Cox JS, Walter P (1996) A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87(3):391–404
9. Sidrauski C, Walter P (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90(6):1031–1039
10. Hetz C, Glimcher LH (2009) Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol Cell 35(5):551–561. doi:10.1016/j.molcel.2009.08.021
11. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG, Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415(6867):92–96
12. Yoshida H, Matsui T, Yamamoto A, Okada T, Mori K (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107(7):881–891
13. Lee AH, Iwakoshi NN, Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23(21):7448–7459
14. Shoulders MD, Ryno LM, Genereux JC, Moresco JJ, Tu PG, Wu C, Yates JR 3rd, Su AI, Kelly JW, Wiseman RL (2013) Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 3(4):1279–1292. doi:10.1016/j.celrep.2013.03.024
15. Harding HP, Zhang Y, Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397(6716):271–274
16. Tabas I, Ron D (2011) Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13(3):184–190. doi:10.1038/ncb0311-184
17. Han J, Back SH, Hur J, Lin YH, Gildersleeve R, Shan J, Yuan CL, Krokowski D, Wang S, Hatzoglou M, Kilberg MS, Sartor MA, Kaufman RJ (2013) ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 15(5):481–490. doi:10.1038/ncb2738
18. Rattner A, Sun H, Nathans J (1999) Molecular genetics of human retinal disease. Annu Rev Genet 33:89–131. doi:10.1146/annurev.genet.33.1.89
19. Palczewski K (2006) G protein-coupled receptor rhodopsin. Annu Rev Biochem 75:743–767. doi:10.1146/annurev.biochem.75.103004.142743
20. Lem J, Krasnoperova NV, Calvert PD, Kosaras B, Cameron DA, Nicolo M, Makino CL, Sidman RL (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci U S A 96(2):736–741
21. Humphries MM, Rancourt D, Farrar GJ, Kenna P, Hazel M, Bush RA, Sieving PA, Sheils DM, McNally N, Creighton P, Erven A, Boros A, Gulya K, Capecchi MR, Humphries P (1997) Retinopathy induced in mice by targeted disruption of the rhodopsin gene. Nat Genet 15(2):216–219. doi:10.1038/ng0297-216
22. Illing ME, Rajan RS, Bence NF, Kopito RR (2002) A rhodopsin mutant linked to autosomal dominant retinitis pigmentosa is prone to aggregate and interacts with the ubiquitin proteasome system. J Biol Chem 277(37):34150–34160
23. Sung CH, Schneider BG, Agarwal N, Papermaster DS, Nathans J (1991) Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci U S A 88(19):8840–8844
24. Kaushal S, Khorana HG (1994) Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33(20):6121–6128
25. Chiang WC, Messah C, Lin JH (2012) IRE1 directs proteasomal and lysosomal degradation of misfolded rhodopsin. Mol Biol Cell 23(5):758–770. doi:10.1091/mbc.E11-08-0663
26. Lin JH, Li H, Yasumura D, Cohen HR, Zhang C, Panning B, Shokat KM, LaVail MM, Walter P (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318(5852):944–949. doi:10.1126/science.1146361
27. Sakami S, Maeda T, Bereta G, Okano K, Golczak M, Sumaroka A, Roman AJ, Cideciyan AV, Jacobson SG, Palczewski K (2011) Probing mechanisms of photoreceptor degeneration in a new mouse model of the common form of autosomal dominant retinitis pigmentosa due to P23H opsin mutations. J Biol Chem 286(12):10551–10567. doi:10.1074/jbc.M110.209759
28. Olsson JE, Gordon JW, Pawlyk BS, Roof D, Hayes A, Molday RS, Mukai S, Cowley GS, Berson EL, Dryja TP (1992) Transgenic mice with a rhodopsin mutation (Pro23His): a mouse model of autosomal dominant retinitis pigmentosa. Neuron 9(5):815–830
29. LaVail MM, Battelle BA (1975) Influence of eye pigmentation and light deprivation on inherited retinal dystrophy in the rat. Exp Eye Res 21(2):167–192
30. Winkler BS (1972) The electroretinogram of the isolated rat retina. Vis Res 12(6):1183–1198
31. Michon JJ, Li ZL, Shioura N, Anderson RJ, Tso MO (1991) A comparative study of methods of photoreceptor morphometry. Invest Ophthalmol Vis Sci 32(2):280–284
32. LaVail MM, Gorrin GM, Repaci MA, Thomas LA, Ginsberg HM (1987) Genetic regulation of light damage to photoreceptors. Invest Ophthalmol Vis Sci 28:1043–1048
33. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM (1992) Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat. J Neurosci 12(9):3554–3567
34. Spira A, Hudy S, Hannah R (1984) Ectopic photoreceptor cells and cell death in the developing rat retina. Anat Embryol 169(3):293–301
35. Hao W, Wenzel A, Obin MS, Chen CK, Brill E, Krasnoperova NV, Eversole-Cire P, Kleyner Y, Taylor A, Simon MI, Grimm C, Reme CE, Lem J (2002) Evidence for two apoptotic pathways in light-induced retinal degeneration. Nat Genet 32(2):254–260. doi:10.1038/ng984
36. LaVail MM, Sidman RL (1974) C57BL-6 J mice with inherited retinal degeneration. Arch Ophthalmol 91(5):394–400
37. McDonald WH, Tabb DL, Sadygov RG, MacCoss MJ, Venable J, Graumann J, Johnson JR, Cociorva D, Yates JR 3rd (2004) MS1, MS2, and SQT-three unified, compact, and easily parsed file formats for the storage of shotgun proteomic spectra and identifications. Rapid Commun Mass Spectrom: RCM 18(18):2162–2168. doi:10.1002/rcm.1603
38. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2(1):43–50
39. Venable JD, Xu T, Cociorva D, Yates JR 3rd (2006) Cross-correlation algorithm for calculation of peptide molecular weight from tandem mass spectra. Anal Chem 78(6):1921–1929. doi:10.1021/ac051636h
40. Caley DW, Johnson C, Liebelt RA (1972) The postnatal development of the retina in the normal and rodless CBA mouse: a light and electron microscopic study. Am J Anat 133(2):179–212. doi:10.1002/aja.1001330205
41. Sanyal S, Bal A (1973) Comparative light and electron microscopic study of retinal histogenesis in normal and rd mutant mice. Z Anat Entwickl Gesch 142(2):219–238. doi:10.1007/bf00519723
42. LaVail MM (1973) Kinetics of rod outer segment renewal in the developing mouse retina. J Cell Biol 58(3):650–661. doi:10.1083/jcb.58.3.650
43. Palczewski K (2012) Chemistry and biology of vision. J Biol Chem 287(3):1612–1619. doi:10.1074/jbc.R111.301150
44. Sakami S, Kolesnikov AV, Kefalov VJ, Palczewski K (2014) P23H opsin knock-in mice reveal a novel step in retinal rod disc morphogenesis. Hum Mol Genet 23(7):1723–1741. doi:10.1093/hmg/ddt561
45. Iwawaki T, Akai R, Kohno K, Miura M (2004) A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med 10(1):98–102. doi:10.1038/nm970
46. Shimazawa M, Inokuchi Y, Ito Y, Murata H, Aihara M, Miura M, Araie M, Hara H (2007) Involvement of ER stress in retinal cell death. Mol Vis 13:578–587
47. Kunte MM, Choudhury S, Manheim JF, Shinde VM, Miura M, Chiodo VA, Hauswirth WW, Gorbatyuk OS, Gorbatyuk MS (2012) ER stress is involved in T17M rhodopsin-induced retinal degeneration. Invest Ophthalmol Vis Sci 53(7):3792–3800. doi:10.1167/iovs.11-9235
48. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, Yu X, Yang L, Tan BK, Rosenwald A, Hurt EM, Petroulakis E, Sonenberg N, Yewdell JW, Calame K, Glimcher LH, Staudt LM (2004) XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21(1):81–93. doi:10.1016/j.immuni.2004.06.010
49. Acosta-Alvear D, Zhou Y, Blais A, Tsikitis M, Lents NH, Arias C, Lennon CJ, Kluger Y, Dynlacht BD (2007) XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol Cell 27(1):53–66. doi:10.1016/j.molcel.2007.06.011
50. Urano F (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664–666
51. Christianson JC, Olzmann JA, Shaler TA, Sowa ME, Bennett EJ, Richter CM, Tyler RE, Greenblatt EJ, Harper JW, Kopito RR (2012) Defining human ERAD networks through an integrative mapping strategy. Nat Cell Biol 14(1):93–105. doi:10.1038/ncb2383
52. Calvert PD, Krasnoperova NV, Lyubarsky AL, Isayama T, Nicoló M, Kosaras B, Wong G, Gannon KS, Margolskee RF, Sidman RL, Pugh EN, Makino CL, Lem J (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin α-subunit. Proc Natl Acad Sci 97(25):13913–13918. doi:10.1073/pnas.250478897
53. Elbein AD, Tropea JE, Mitchell M, Kaushal GP (1990) Kifunensine, a potent inhibitor of the glycoprotein processing mannosidase I. J Biol Chem 265(26):15599–15605
54. Tokunaga F, Brostrom C, Koide T, Arvan P (2000) Endoplasmic reticulum (ER)-associated degradation of misfolded N-linked glycoproteins is suppressed upon inhibition of ER mannosidase I. J Biol Chem 275(52):40757–40764
55. Wang Q, Li L, Ye Y (2008) Inhibition of p97-dependent protein degradation by eeyarestatin I. J Biol Chem 283(12):7445–7454. doi:10.1074/jbc.M708347200
56. Fiebiger E, Hirsch C, Vyas JM, Gordon E, Ploegh HL, Tortorella D (2004) Dissection of the dislocation pathway for type I membrane proteins with a new small molecule inhibitor, eeyarestatin. Mol Biol Cell 15(4):1635–1646. doi:10.1091/mbc.E03-07-0506
57. Gorbatyuk MS, Knox T, LaVail MM, Gorbatyuk OS, Noorwez SM, Hauswirth WW, Lin JH, Muzyczka N, Lewin AS (2010) Restoration of visual function in P23H rhodopsin transgenic rats by gene delivery of BiP/Grp78. Proc Natl Acad Sci U S A 107(13):5961–5966. doi:10.1073/pnas.0911991107
58. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12(7):982–995
59. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E, Mori M (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109(4):525–532. doi:10.1172/JCI14550
60. Pennuto M, Tinelli E, Malaguti M, Del Carro U, D'Antonio M, Ron D, Quattrini A, Feltri ML, Wrabetz L (2008) Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron 57(3):393–405. doi:10.1016/j.neuron.2007.12.021
61. Gardner BM, Walter P (2011) Unfolded proteins are Ire1-activating ligands that directly induce the unfolded protein response. Science 333(6051):1891–1894. doi:10.1126/science.1209126
62. Zhou J, Liu CY, Back SH, Clark RL, Peisach D, Xu Z, Kaufman RJ (2006) The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response. Proc Natl Acad Sci U S A 103(39):14343–14348. doi:10.1073/pnas.0606480103
63. Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D, Katze MG (2002) Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci U S A 99(25):15920–15925
64. Yamani L, Latreille M, Larose L (2014) Interaction of Nck1 and PERK phosphorylated at Y561 negatively modulates PERK activity and PERK regulation of pancreatic β-cell proinsulin content. Mol Biol Cell 25(5):702–711. doi:10.1091/mbc.E13-09-0511
65. Sung CH, Chuang JZ (2010) The cell biology of vision. J Cell Biol 190(6):953–963. doi:10.1083/jcb.201006020
66. Rosenfeld PJ, Cowley GS, McGee TL, Sandberg MA, Berson EL, Dryja TP (1992) A null mutation in the rhodopsin gene causes rod photoreceptor dysfunction and autosomal recessive retinitis pigmentosa. Nat Genet 1(3):209–213
67. Liang Y, Fotiadis D, Maeda T, Maeda A, Modzelewska A, Filipek S, Saperstein DA, Engel A, Palczewski K (2004) Rhodopsin signaling and organization in heterozygote rhodopsin knockout mice. J Biol Chem 279(46):48189–48196. doi:10.1074/jbc.M408362200
68. Kroeger H, Messah C, Ahern K, Gee J, Joseph V, Matthes MT, Yasumura D, Gorbatyuk MS, Chiang WC, Lavail MM, Lin JH (2012) Induction of endoplasmic reticulum stress genes, BiP and Chop, in genetic and environmental models of retinal degeneration. Invest Ophthalmol Vis Sci 53(12):7590–7599. doi:10.1167/iovs.12-10221
69. Yang LP, Wu LM, Guo XJ, Li Y, Tso MO (2008) Endoplasmic reticulum stress is activated in light-induced retinal degeneration. J Neurosci Res 86(4):910–919. doi:10.1002/jnr.21535
70. Salminen A, Kauppinen A, Hyttinen JM, Toropainen E, Kaarniranta K (2010) Endoplasmic reticulum stress in age-related macular degeneration: trigger for neovascularization. Mol Med 16(11–12):535–542. doi:10.2119/molmed.2010.00070
71. Ambati J, Fowler BJ (2012) Mechanisms of age-related macular degeneration. Neuron 75(1):26–39. doi:10.1016/j.neuron.2012.06.018