IRE1 directs proteasomal and lysosomal degradation of misfolded rhodopsin

Molecular Biology of the Cell

Volumn 23, Issue 5, 2012, Pages 758-770

  Chiang, Wei Chieh ^a   Messah, Carissa ^a   Lin, Jonathan H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; P23H RHODOPSIN; PROTEASOME; PROTEIN IRE1; RHODOPSIN; RIBONUCLEASE; TRANSMEMBRANE CONDUCTANCE REGULATOR; UNCLASSIFIED DRUG;

ARTICLE; CELL DEATH; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; LYSOSOME; MAMMAL CELL; MISSENSE MUTATION; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN MISFOLDING; SIGNAL TRANSDUCTION; WILD TYPE;

ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENDORIBONUCLEASES; HEK293 CELLS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN-SERINE-THREONINE KINASES; PROTEOLYSIS; RHODOPSIN; UNFOLDED PROTEIN RESPONSE;

EUKARYOTA; MAMMALIA;

EID: 84863250283     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-08-0663     Document Type: Article

References (67)

1. Ahmad ST, Natochin M, Barren B, Artemyev NO, O'Tousa JE (2006). Heterologous expression of bovine rhodopsin in Drosophila photoreceptor cells. Invest Ophthalmol Vis Sci 47, 3722-3728. (Pubitemid 46044282)
2. Bence NF, Sampat RM, Kopito RR (2001). Impairment of the ubiquitin-proteasome system by protein aggregation. Science 292, 1552-1555. (Pubitemid 32493425)
3. Bernales S, McDonald KL, Walter P (2006). Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4, e423.
4. Bernales S, Schuck S, Walter P (2007). ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3, 285-287. (Pubitemid 46752700)
5. Berson EL (1993). Retinitis pigmentosa. Invest Ophthalmol Vis Sci 34, 1659-1676.
6. Bishop AC et al. (2000). A chemical switch for inhibitor-sensitive alleles of any protein kinase. Nature 407, 395-401.
7. Buchberger A, Bukau B, Sommer T (2010). Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol Cell 40, 238-252.
8. 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, 92-96. (Pubitemid 34062456)
9. Carlsson SR, Roth J, Piller F, Fukuda M (1988). Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2Major sialoglycoproteins carrying polylactosaminoglycan. J Biol Chem 263, 18911-18919. (Pubitemid 19016351)
10. Cox JS, Shamu CE, Walter P (1993). Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206. (Pubitemid 23180493)
11. Cuervo AM, Dice JF (2000). Age-related decline in chaperone-mediated autophagy. J Biol Chem 275, 31505-31513.
12. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, Kenyon C (2010). Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol 8, e1000450.
13. Dryja TP, McGee TL, Reichel E, Hahn LB, Cowley GS, Yandell DW, Sandberg MA, Berson EL (1990). A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343, 364-366.
14. Eriksson KK, Vago R, Calanca V, Galli C, Paganetti P, Molinari M (2004). EDEM contributes to maintenance of protein folding efficiency and secretory capacity. J Biol Chem 279, 44600-44605. (Pubitemid 39430867)
15. Farinha CM, Amaral MD (2005). Most F508del-CFTR is targeted to degradation at an early folding checkpoint and independently of calnexin. Mol Cell Biol 25, 5242-5252. (Pubitemid 40781121)
16. Gonzalez TN, Sidrauski C, Dorfler S, Walter P (1999). Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J 18, 3119-3132. (Pubitemid 29255620)
17. 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 USA 107, 5961-5966.
18. Griciuc A, Aron L, Roux MJ, Klein R, Giangrande A, Ueffing M (2010). Inactivation of VCP/ter94 suppresses retinal pathology caused by misfolded rhodopsin in Drosophila. PLoS Genet 6, piie1001075.
19. Han D, Lerner AG, Vande Walle L, Upton JP, Xu W, Hagen A, Backes BJ, Oakes SA, Papa FR (2009). IRE1alpha kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138, 562-575.
20. Harding HP, Zhang Y, Ron D (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274. (Pubitemid 29051178)
21. Hargrave PA (2001). Rhodopsin structure, function, and topography. Invest Ophthalmol Vis Sci 42, 3-9.
22. Hetz C, Glimcher LH (2009). Fine-tuning of the unfolded protein response: assembling the IRE1alpha interactome. Mol Cell 35, 551-561.
23. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS (2009). Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J Cell Biol 186, 323-331.
24. Hollien J, Weissman JS (2006). Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107. (Pubitemid 44051264)
25. 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, 34150-34160.
26. Iwawaki T, Akai R, Kohno K (2010). IRE1alpha disruption causes histological abnormality of exocrine tissues, increase of blood glucose level, and decrease of serum immunoglobulin level. PLoS One 5, e13052.
27. Kang MJ, Ryoo HD (2009). Suppression of retinal degeneration in Drosophila by stimulation of ER-associated degradation. Proc Natl Acad Sci USA 106, 17043-17048.
28. Kaushal S (2006). Effect of rapamycin on the fate of P23H opsin associated with retinitis pigmentosa (an American Ophthalmological Society thesis). Trans Am Ophthalmol Soc 104, 517-529.
29. Kaushal S, Khorana HG (1994). Structure and function in rhodopsin. 7. Point mutations associated with autosomal dominant retinitis pigmentosa. Biochemistry 33, 6121-6128. (Pubitemid 24190763)
30. Kawaguchi S, Ng DT (2007). SnapShot: ER-associated protein degradation pathways. Cell 129, 1230.
31. Kosmaoglou M, Cheetham ME (2008). Calnexin is not essential for mammalian rod opsin biogenesis. Mol Vis 14, 2466-2474.
32. Kosmaoglou M, Kanuga N, Aguila M, Garriga P, Cheetham ME (2009). A dual role for EDEM1 in the processing of rod opsin. J Cell Sci 122, 4465-4472.
33. Kosmaoglou M, Schwarz N, Bett JS, Cheetham ME (2008). Molecular chaperones and photoreceptor function. Prog Retin Eye Res 27, 434-449.
34. LaVail MM, Yasumura D, Matthes MT, Drenser KA, Flannery JG, Lewin AS, Hauswirth WW (2000). Ribozyme rescue of photoreceptor cells in P23H transgenic rats: long-term survival and late-stage therapy. Proc Natl Acad Sci USA 97, 11488-11493.
35. 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, 7448-7459. (Pubitemid 37271447)
36. Lewin AS, Drenser KA, Hauswirth WW, Nishikawa S, Yasumura D, Flannery JG, LaVail MM (1998). Ribozyme rescue of photoreceptor cells in a transgenic rat model of autosomal dominant retinitis pigmentosa. Nat Med 4, 967-971. (Pubitemid 28364040)
37. Li H, Korennykh AV, Behrman SL, Walter P (2010). Mammalian endoplasmic reticulum stress sensor IRE1 signals by dynamic clustering. Proc Natl Acad Sci USA 107, 16113-16118.
38. Li T, Sandberg MA, Pawlyk BS, Rosner B, Hayes KC, Dryja TP, Berson EL (1998). Effect of vitamin A supplementation on rhodopsin mutants threonine- 17 -> methionine and proline-347 -> serine in transgenic mice and in cell cultures. Proc Natl Acad Sci USA 95, 11933-11938. (Pubitemid 28460517)
39. 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, 944-949. (Pubitemid 350098984)
40. Lin JH, Li H, Zhang Y, Ron D, Walter P (2009). Divergent effects of PERK and IRE1 signaling on cell viability. PLoS ONE 4, e4170.
41. Liu H, Wang M, Xia CH, Du X, Flannery JG, Ridge KD, Beutler B, Gong X (2010). Severe retinal degeneration caused by a novel rhodopsin mutation. Invest Ophthalmol Vis Sci 51, 1059-1065.
42. McGowan EB, Becker E, Detwiler TC (1989). Inhibition of calpain in intact platelets by the thiol protease inhibitor E-64d. Biochem Biophys Res Commun 158, 432-435. (Pubitemid 19053947)
43. Mendes HF, Cheetham ME (2008). Pharmacological manipulation of gain-of- function and dominant-negative mechanisms in rhodopsin retinitis pigmentosa. Hum Mol Genet 17, 3043-3054.
44. Mizushima N, Yoshimori T (2007). How to interpret LC3 immunoblotting. Autophagy 3, 542-545. (Pubitemid 350060049)
45. Noorwez SM, Kuksa V, Imanishi Y, Zhu L, Filipek S, Palczewski K, Kaushal S (2003). Pharmacological chaperone-mediated in vivo folding and stabilization of the P23H-opsin mutant associated with autosomal dominant retinitis pigmentosa. J Biol Chem 278, 14442-14450. (Pubitemid 36799997)
46. Noorwez SM, Malhotra R, McDowell JH, Smith KA, Krebs MP, Kaushal S (2004). Retinoids assist the cellular folding of the autosomal dominant retinitis pigmentosa opsin mutant P23H. J Biol Chem 279, 16278-16284. (Pubitemid 38509322)
47. Noorwez SM, Sama RR, Kaushal S (2009). Calnexin improves the folding efficiency of mutant rhodopsin in the presence of pharmacological chaperone 11-cis-retinal. J Biol Chem 284, 33333-33342.
48. Oikawa D, Tokuda M, Iwawaki T (2007). Site-specific cleavage of CD59 mRNA by endoplasmic reticulum-localized ribonuclease, IRE1. Biochem Biophys Res Commun 360, 122-127. (Pubitemid 46990332)
49. Olivari S, Galli C, Alanen H, Ruddock L, Molinari M (2005). A novel stress-induced EDEM variant regulating endoplasmic reticulum-associated glycoprotein degradation. J Biol Chem 280, 2424-2428. (Pubitemid 40189341)
50. 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, 815-830.
51. Ron D, Walter P (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8, 519-529. (Pubitemid 46985379)
52. Rosenbaum EE, Hardie RC, Colley NJ (2006). Calnexin is essential for rhodopsin maturation, Ca2+ regulation, and photoreceptor cell survival. Neuron 49, 229-241. (Pubitemid 43089640)
53. Rubinsztein DC (2006). The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780-786.
54. 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, 10551-10567.
55. Saliba RS, Munro PM, Luthert PJ, Cheetham ME (2002). The cellular fate of mutant rhodopsin: quality control, degradation and aggresome formation. J Cell Sci 115, 2907-2918.
56. Sun F, Zhang R, Gong X, Geng X, Drain PF, Frizzell RA (2006). Derlin-1 promotes the efficient degradation of the cystic fibrosis transmembrane conductance regulator (CFTR) and CFTR folding mutants. J Biol Chem 281, 36856-36863. (Pubitemid 46042153)
57. 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 USA 88, 8840-8844. (Pubitemid 21915451)
58. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, Ron D (2000). Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666. (Pubitemid 30070916)
59. Ward CL, Kopito RR (1994). Intracellular turnover of cystic fibrosis transmembrane conductance regulatorInefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 269, 25710-25718.
60. Winslow AR, Rubinsztein DC (2008). Autophagy in neurodegeneration and development. Biochim Biophys Acta 1782, 723-729.
61. Wong E, Cuervo AM (2010). Autophagy gone awry in neurodegenerative diseases. Nat Neurosci 13, 805-811.
62. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y (1998). Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23, 33-42. (Pubitemid 28223394)
63. Yoshida H, Matsui T, Hosokawa N, Kaufman RJ, Nagata K, Mori K (2003). A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 4, 265-271. (Pubitemid 36221802)
64. 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, 881-891. (Pubitemid 34084979)
65. Younger JM, Chen L, Ren HY, Rosser MF, Turnbull EL, Fan CY, Patterson C, Cyr DM (2006). Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126, 571-582. (Pubitemid 44163603)
66. Zhang K et al. (2011). The unfolded protein response transducer IRE- 1alpha prevents ER stress-induced hepatic steatosis. EMBO J 30, 1357-1375.
67. Zhang K, Wong HN, Song B, Miller CN, Scheuner D, Kaufman RJ (2005). The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J Clin Invest 115, 268-281. (Pubitemid 40385469)