Proteasome overload is a common stress factor in multiple forms of inherited retinal degeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 24, 2013, Pages 9986-9991

  Lobanova, Ekaterina S ^a   Finkelstein, Stella ^a   Skiba, Nikolai P ^a   Arshavsky, Vadim Y ^a  

^a DUKE UNIVERSITY EYE CENTER   (United States)

Author keywords

Neurodegenerative diseases; Protein degradation

Indexed keywords

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; PROTEASOME; TRANSDUCIN; TRANSDUCIN GAMMA SUBUNIT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; GENE MUTATION; GENETIC DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; RETINA DEGENERATION; RETINA ROD;

NEURODEGENERATIVE DISEASES; PROTEIN DEGRADATION;

ANIMALS; BLOTTING, WESTERN; GREEN FLUORESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; RETINA; RETINAL DEGENERATION; RETINAL ROD PHOTORECEPTOR CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRESS, PHYSIOLOGICAL; TRANSDUCIN;

ANIMALIA; MUS;

EID: 84878999228     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305521110     Document Type: Article

References (42)

1. Kosmaoglou M, Schwarz N, Bett JS, Cheetham ME (2008) Molecular chaperones and photoreceptor function. Prog Retin Eye Res 27(4):434-449.
2. Mao HY, et al. (2011) AAV delivery of wild-type rhodopsin preserves retinal function in a mouse model of autosomal dominant retinitis pigmentosa. Hum Gene Ther 22(5):567-575.
3. Dryja TP, et al. (1990) A point mutation of the rhodopsin gene in one form of retinitis pigmentosa. Nature 343(6256):364-366.
4. 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.
5. Saliba RS, Munro PMG, Luthert PJ, Cheetham ME (2002) The cellular fate of mutant rhodopsin: Quality control, degradation and aggresome formation. J Cell Sci 115(Pt 14):2907-2918.
6. Lin JH, et al. (2007) IRE1 signaling affects cell fate during the unfolded protein response. Science 318(5852):944-949. (Pubitemid 350098984)
7. Gorbatyuk MS, et al. (2010) Restoration of visual function in P23H rhodopsin transgenic rats by gene delivery of BiP/Grp78. Proc Natl Acad Sci USA 107(13):5961-5966.
8. Mockel A, et al. (2012) Pharmacological modulation of the retinal unfolded protein response in Bardet-Biedl syndrome reduces apoptosis and preserves light detection ability. J Biol Chem 287(44):37483-37494.
9. Clemson CM, et al. (2011) Therapeutic potential of valproic acid for retinitis pigmentosa. Br J Ophthalmol 95(1):89-93.
10. Lobanova ES, et al. (2008) Transducin γ-subunit sets expression levels of α- and β -subunits and is crucial for rod viability. J Neurosci 28(13):3510-3520. (Pubitemid 351469314)
11. Kolesnikov AV, et al. (2011) G-protein betagamma-complex is crucial for efficient signal amplification in vision. J Neurosci 31(22):8067-8077.
12. Okae H, Iwakura Y (2010) Neural tube defects and impaired neural progenitor cell proliferation in Gbeta1-deficient mice. Dev Dyn 239(4):1089-1101.
13. Willardson BM, Howlett AC (2007) Function of phosducin-like proteins in G protein signaling and chaperone-assisted protein folding. Cell Signal 19(12):2417-2427. (Pubitemid 47542295)
14. Kubota S, Kubota H, Nagata K (2006) Cytosolic chaperonin protects folding intermediates of Gbeta from aggregation by recognizing hydrophobic beta-strands. Proc Natl Acad Sci USA 103(22):8360-8365. (Pubitemid 43838460)
15. Wells CA, Dingus J, Hildebrandt JD (2006) Role of the chaperonin CCT/TRiC complex in G protein betagamma-dimer assembly. J Biol Chem 281(29):20221-20232. (Pubitemid 44065797)
16. Marrari Y, Crouthamel M, Irannejad R, Wedegaertner PB (2007) Assembly and trafficking of heterotrimeric G proteins. Biochemistry 46(26):7665-7677. (Pubitemid 47016052)
17. Dingus J, Hildebrandt JD (2012) Synthesis and assembly of G protein βγ dimers: Comparison of in vitro and in vivo studies. Subcell Biochem 63:155-180.
18. Kabir MA, et al. (2011) Functional subunits of eukaryotic chaperonin CCT/TRiC in protein folding. J Amino Acids 2011:843206.
19. Posokhova E, et al. (2011) Disruption of the chaperonin containing TCP-1 function affects protein networks essential for rod outer segment morphogenesis and survival. Mol Cell Proteomics 10(1):M110.000570.
20. Wan Y, et al. (2012) Misfolded Gβ is recruited to cytoplasmic dynein by Nudel for efficient clearance. Cell Res 22(7):1140-1154.
21. Moulédous L, et al. (2005) Long-term morphine treatment enhances proteasome-dependent degradation of G beta in human neuroblastoma SH-SY5Y cells: Correlation with onset of adenylate cyclase sensitization. Mol Pharmacol 68(2):467-476. (Pubitemid 41058310)
22. Wójcik C (2007) Role of ubiquitin- and proteasome system in neuronal apoptosis. The Ubiquitin Proteasome System in the Central Nervous System: From Physiology to Pathology, eds Di Napoli M, Wójcik C (Nova Biomedical Books, New York), pp 513-536.
23. Lindsten K, Menéndez-Benito V, Masucci MG, Dantuma NP (2003) A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol 21(8):897-902. (Pubitemid 36936195)
24. Dantuma NP, Lindsten K, Glas R, Jellne M, Masucci MG (2000) Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat Biotechnol 18(5):538-543. (Pubitemid 30313959)
25. Kisselev AF, Goldberg AL (2005) Monitoring activity and inhibition of 26S proteasomes with fluorogenic peptide substrates. Methods Enzymol 398:364-378. (Pubitemid 41578898)
26. Pickering AM, Linder RA, Zhang H, Forman HJ, Davies KJ (2012) Nrf2-dependent induction of proteasome and Pa28αβ regulator are required for adaptation to oxidative stress. J Biol Chem 287(13):10021-10031.
27. Travis GH, Brennan MB, Danielson PE, Kozak CA, Sutcliffe JG (1989) Identification of a photoreceptor-specific mRNA encoded by the gene responsible for retinal degeneration slow (rds). Nature 338(6210):70-73. (Pubitemid 19076785)
28. Sanyal S, Jansen HG (1981) Absence of receptor outer segments in the retina of rds mutant mice. Neurosci Lett 21(1):23-26. (Pubitemid 11178780)
29. Lem J, et al. (1999) Morphological, physiological, and biochemical changes in rhodopsin knockout mice. Proc Natl Acad Sci USA 96(2):736-741. (Pubitemid 29061278)
30. Lee ES, Burnside B, Flannery JG (2006) Characterization of peripherin/rds and rom-1 transport in rod photoreceptors of transgenic and knockout animals. Invest Ophthalmol Vis Sci 47(5):2150-2160. (Pubitemid 46768300)
31. Chiang WC, Messah C, Lin JH (2012) IRE1 directs proteasomal and lysosomal degradation of misfolded rhodopsin. Mol Biol Cell 23(5):758-770.
32. Menéndez-Benito V, Verhoef LG, Masucci MG, Dantuma NP (2005) Endoplasmic reticulum stress compromises the ubiquitin-proteasome system. Hum Mol Genet 14(19):2787-2799. (Pubitemid 41418785)
33. Redmond TM, et al. (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat Genet 20(4):344-351. (Pubitemid 28541631)
34. Cremers FP, van den Hurk JA, den Hollander AI (2002) Molecular genetics of Leber congenital amaurosis. Hum Mol Genet 11(10):1169-1176. (Pubitemid 34567497)
35. Woodruff ML, et al. (2003) Spontaneous activity of opsin apoprotein is a cause of Leber congenital amaurosis. Nat Genet 35(2):158-164. (Pubitemid 37187634)
36. Fain GL (2006) Why photoreceptors die (and why they don't). Bioessays 28(4):344-354.
37. Schwartz AL, Ciechanover A (2009) Targeting proteins for destruction by the ubiquitin system: Implications for human pathobiology. Annu Rev Pharmacol Toxicol 49:73-96.
38. Dantuma NP, Lindsten K (2010) Stressing the ubiquitin-proteasome system. Cardiovasc Res 85(2):263-271.
39. Ortega Z, et al. (2010) Acute polyglutamine expression in inducible mouse model unravels ubiquitin/proteasome system impairment and permanent recovery attributable to aggregate formation. J Neurosci 30(10):3675-3688.
40. Cheroni C, et al. (2009) Functional alterations of the ubiquitin-proteasome system in motor neurons of a mouse model of familial amyotrophic lateral sclerosis. Hum Mol Genet 18(1):82-96.
41. Huang QA, Figueiredo-Pereira ME (2010) Ubiquitin/proteasome pathway impairment in neurodegeneration: Therapeutic implications. Apoptosis 15(11):1292-1311.
42. Gerber SA, Rush J, Stemman O, Kirschner MW, Gygi SP (2003) Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 100(12):6940-6945. (Pubitemid 36706372)