Ubiquitin proteasome pathway-mediated degradation of proteins: Effects due to site-specific substrate deamidation

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 8, 2010, Pages 4164-4173

  Dudek, Edward J ^a   Lampi, Kirsten J ^a   Lampi, Jason A ^a   Shang, Fu ^a   King, Jonathan ^b   Wang, Yongting ^a   Taylor, Allen ^a  

^a TUFTS UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BETA CRYSTALLIN; BETA1 CRYSTALLIN; BETA2 CRYSTALLIN; CRYSTALLIN; GAMMA CRYSTALLIN; IODINE 125; PROTEASOME; UBIQUITIN; UNCLASSIFIED DRUG; BETA CRYSTALLIN B2; BETA-CRYSTALLIN B2; CRYBB1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

AGING; ANIMAL CELL; ARTICLE; CATARACT; CATARACTOGENESIS; CELL LYSATE; CIRCULAR DICHROISM; CONTROLLED STUDY; COW; DEAMINATION; HYDROPHOBICITY; ISOTOPE LABELING; LENS EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RETICULOCYTE; THERMOSTABILITY; UBIQUITINATION; WILD TYPE; AMINO ACID SEQUENCE; CHEMISTRY; ENZYME SPECIFICITY; EPITHELIUM CELL; HUMAN; LENS; METABOLISM; MOLECULAR GENETICS; OXIDATIVE STRESS; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; BETA-CRYSTALLIN B CHAIN; DEAMINATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPITHELIAL CELLS; HUMANS; LENS, CRYSTALLINE; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; SUBSTRATE SPECIFICITY; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES; UBIQUITINATION;

EID: 77955866089     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4087     Document Type: Article

References (84)

1. Schoneich C. Protein modification in aging: an update. Exp Gerontol. 2006;41(9):807- 812.
2. Gregersen N, Bolund L, Bross P. Protein misfolding, aggregation, and degradation in disease. Mol Biotechnol. 2005;31(2):141-150.
3. Tofaris GK, Razzaq A, Ghetti B, Lilley KS, Spillantini MG. Ubiquitination of alpha-synuclein in Lewy bodies is a pathological event not associated with impairment of proteasome function. J Biol Chem. 2003;278(45):44405-44411.
4. Reynolds MR, Berry RW, Binder LI. Nitration in neurodegeneration: deciphering the "Hows" "nYs". Biochemistry. 2007;46(25):7325-7336.
5. Hernandez F, Avila J. Tauopathies. Cell Mol Life Sci. 2007;64(17):2219-2233.
6. Hains PG, Truscott RJ. Post-translational modifications in the nuclear region of young, aged, and cataract human lenses. J Proteome Res. 2007;6(10):3935-3943.
7. Zhang X, Dudek EJ, Liu B, et al. Degradation of C-terminal truncated alpha A-crystallins by the ubiquitin-proteasome pathway. Invest Ophthalmol Vis Sci. 2007;48(9):4200-4208.
8. Huang LL, Shang F. Nowell TR Jr, Taylor A. Degradation of differentially oxidized alpha-crystallins in bovine lens epithelial cells. Exp Eye Res. 1995;61(1):45-54.
9. Zetterberg M, Zhang X, Taylor A, Liu B, Liang JJ, Shang F. Glutathiolation enhances the degradation of γC-crystallin in lens and reticulocyte lysates, partially via the ubiquitin-proteasome pathway. Invest Ophthalmol Vis Sci. 2006;47(8):3467-3473.
10. Takemoto L, Boyle D. Increased deamidation of asparagine during human senile cataractogenesis. Mol Vis. 2000;6:164-168.
11. Groenen PJ, van Dongen MJ, Voorter CE, Bloemendal H, de Jong WW. Age-dependent deamidation of alpha B-crystallin. FEBS Lett. 1993;322(1):69-72.
12. Linetsky M, Shipova E, Cheng R, Ortwerth BJ. Glycation by ascorbic acid oxidation products leads to the aggregation of lens proteins. Biochim Biophys Acta. 2008;1782(1):22-34.
13. Wang J, Maldonado MA. The ubiquitin-proteasome system and its role in inflammatory and autoimmune diseases. Cell Mol Immunol. 2006;3(4):255-261.
14. Santhoshkumar P, Udupa P, Murugesan R, Sharma KK. Significance of interactions of LMW crystallin fragments in lens aging and cataract formation. J Biol Chem. 2008;283(13):8477-8485.
15. Shearer TR, Shih M, Azuma M, David LL. Precipitation of crystallins from young rat lens by endogenous calpain. Exp Eye Res. 1995; 61(2):141-150.
16. Shang F, Taylor A. Function of the ubiquitin proteolytic pathway in the eye. Exp Eye Res. 2004;78(1):1-14.
17. Rattner A, Nathans J. Macular degeneration: recent advances and therapeutic opportunities. Nat Rev Neurosci. 2006;7(11):860-872.
18. Surguchev A, Surguchov A. Conformational diseases: looking into the eyes. Brain Res Bull. 2010;81(1):12-24.
19. Harrington V, McCall S, Huynh S, Srivastava K, Srivastava OP. Crystallins in water soluble-HMW protein fractions and water insoluble protein fractions in aging and cataractous human lenses. Mol Vis. 2004;10:476-489.
20. Baumeister W, Walz J, Zühl F, Seemüller E. The proteasome: paradigm of a self-compartmentalizing protease. Cell. 1998;92(3): 367-380.
21. Eytan E, Ganoth D, Armon T, Hershko A. ATP-dependent incorporation of 20S protease into the 26S complex that degrades proteins conjugated to ubiquitin. Proc Natl Acad Sci U S A. 1989;86(20): 7751-7755.
22. Nakatsukasa K, Brodsky JL. The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum. Traffic. 2008;9:861-870.
23. Carvalho P, Goder V, Rapoport TA. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell. 2006;126(2):361-373.
24. Park SH, Bolender N, Eisele F, et al. The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitinproteasome system. Mol Biol Cell. 2007;18(1):153-165.
25. Rosser MF, Washburn E, Muchowski PJ, Patterson C, Cyr DM. Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem. 2007;282(31):22267-22277.
26. Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. CHIPmediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature. 2006;440(7083):551-555.
27. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev. 2002;82(2):373-428.
28. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425-479.
29. Hershko A, Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761-807.
30. Pickart CM, Targeting of substrates to the 26S proteasome. FASEB J. 1997;11(13):1055-1066.
31. Waxman L, Fagan JM, Goldberg AL. Demonstration of two distinct HMW proteases in rabbit reticulocytes, one of which degrade subiquitin conjugates. J Biol Chem. 1987;262(6):2451-2457.
32. Pickart CM, Fushman D. Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol. 2004;8(6):610-616.
33. Shimeld SM, Purkiss AG, Dirks RP, Bateman OA, Slingsby C, Lubsen NH. Urochordate βγ-crystallin and the evolutionary origin of the vertebrate eye lens. Curr Biol. 2005;15(18):1684-1689.
34. Harding JJ, Dilley KJ. Structural proteins of the mammalian lens: a review with emphasis on changes in development, aging and cataract. Exp Eye Res. 1976;22(1):1-73.
35. Cobb BA, Petrash JM. Structural and functional changes in the alpha A-crystallin R116C mutant in hereditary cataracts. Biochemistry. 2000;39(51):15791-15798.
36. Xia JZ, Wang Q, Tatarkova S, Aerts T, Clauwaert J. Structural basis of eye lens transparency: light scattering by concentrated solutions of bovine alpha-crystallin proteins. Biophys J. 1996;71(5):2815-2822.
37. Veretout F, Delaye M, Tardieu A. Molecular basis of eye lens transparency: osmotic pressure and X-ray analysis of alpha-crystallin solutions. J Mol Biol. 1989;205(4):713-728.
38. Hatters DM, Lindner RA, Carver JA, Howlett GJ. The molecular chaperone, alpha-crystallin, inhibits amyloid formation by apolipoprotein C-II. J Biol Chem. 2001;276(36):33755-33761.
39. Horwitz J. Alpha-crystallin can function as a molecular chaperone. Proc Natl Acad Sci U S A. 1992;89(21):10449-10453.
40. Kashlan OB, Mueller GM, Qamar MZ, et al. Small heat shock protein _A-crystallin regulates epithelial sodium channel expression. J Biol Chem. 2007;282(38):28149-28156.
41. Doran P, Gannon J, O'Connell K, Ohlendieck K. Aging skeletal muscle shows a drastic increase in the small heat shock proteins β-crystallin/HspB5 and cvHsp/HspB7. Eur J Cell Biol. 2007; 86(10):629-640.
42. Lee FY, Kast-Woelbern HR, Chang J, et al. Alpha-crystallin is a target gene of the farnesoid X-activated receptor in human livers. J Biol Chem. 2005;280(36):31792-312800.
43. Xi J, Farjo R, Yoshida S, Kern TS, Swaroop A, Andley UP. A comprehensive analysis of the expression of crystallins in mouse retina. Mol Vis. 2003;9:410-419.
44. Dirks RP, Van Genesen ST, Kruse JJ, Jorissen L, Lubsen NH. Extralenticular expression of the rodent β2-crystallin gene. Exp Eye Res. 1998;66(2):267-269.
45. Wilmarth PA, Tanner S, Dasari S, et al. Age-related changes in human crystallins determined from comparative analysis of posttranslational modifications in young and aged lens: does deamidation contribute to crystallin insolubility? J Proteome Res. 2006; 5(10):2554-2566.
46. Lapko VN, Purkiss AG, Smith DL, Smith JB. Deamidation in human γS-crystallin from cataractous lenses is influenced by surface exposure. Biochemistry. 2002;41(27):8638-8648.
47. Lapko VN, Cerny RL, Smith DL, Smith JB. Modifications of human βA1/βA3-crystallins include S-methylation, glutathiolation, and truncation. Protein Sci. 2005;14(1):45-54.
48. Flaugh SL, Mills IA, King J. Glutamine deamidation destabilizes human γD-crystallin and lowers the kinetic barrier to unfolding. J Biol Chem. 2006;281(41):30782-30793.
49. Hanson SR, Hasan A, Smith DL, Smith JB. The major in vivo modifications of the human water-insoluble lens crystallins are disulfide bonds, deamidation, methionine oxidation and backbone cleavage. Exp Eye Res. 2000;71(2):195-207.
50. Wagner BJ, Margolis JW, Singh I. Bovine lens multicatalytic proteinase complex. Enzyme Protein. 1993;47(4-6):202-209.
51. Lampi KJ, Oxford JT, Bachinger HP, Shearer TR, David LL, Kapfer DM. Deamidation of human β1 alters the elongated structure of the dimer. Exp Eye Res. 2001;72(3):279-288.
52. Lampi KJ, Amyx KK, Ahmann P, Steel EA. Deamidation in human lens β2-crystallin destabilizes the dimer. Biochemistry. 2006; 45(10):3146-3153.
53. Harms MJ, Wilmarth PA, Kapfer DM, et al. Laser light-scattering evidence for an altered association of β1-crystallin deamidated in the connecting peptide. Protein Sci. 2004;13(3):678-686.
54. Jahngen JH, Haas AL, Ciechanover A, Blondin J, Eisenhauer D, Taylor A. The eye lens has an active ubiquitin-protein conjugation system. J Biol Chem. 1986;261(29):13760-13767.
55. Chau V, Tobias JW, Bachmair A, et al. A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science. 1989;243(4898):1576-1583.
56. Hershko A, Heller H. Occurrence of a polyubiquitin structure in ubiquitin-protein conjugates. Biochem Biophys Res Commun. 1985;128(3):1079-1086.
57. Taylor A, Peltier CZ, Torre FJ, Hakamian N. Inhibition of bovine lens leucine aminopeptidase by bestatin: number of binding sites and slow binding of this inhibitor. Biochemistry. 1993;32(3):784-790.
58. Shang F, Huang L, Taylor A. Degradation of native and oxidized β- and γ-crystallin using bovine lens epithelial cell and rabbit reticulocyte extracts. Curr Eye Res. 1994;13(6):423-431.
59. Bax B, Lapatto R, Nalini V, et al. X-ray analysis of β2-crystallin and evolution of oligomeric lens proteins. Nature. 1990;347(6295): 776-780.
60. Rechsteiner M, Chin D, Hough R, et al. What determines the degradation rate of an injected protein? CIBA Found Symp. 1984; 103:181-201.
61. Jahngen-Hodge J, Cyr D, Laxman E, Taylor A. Ubiquitin and ubiquitin conjugates in human lens. Exp Eye Res. 1992;55(6):897-902.
62. Seufert W, Jentsch S. Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J. 1990;9(2):543-550.
63. Midelfort CF, Mehler AH. Deamidation in vivo of an asparagines residue of rabbit muscle aldolase. Proc Natl Acad Sci U S A. 1972;69(7):1816-1819.
64. Voorter CE, de Haard-Hoekman WA, van den Oetelaar PJ, Bloemendal H, de Jong WW. Spontaneous peptide bond cleavage in aging α-crystallin through a succinimide intermediate. J Biol Chem. 1988;263(35):19020-19023.
65. Van Kleef FSM, DeJong WW, Hoenders HJ. Stepwise degradation and deamidations of the eye lens protein alpha crystallin in aging. Nature. 1975;258(2333):262-264.
66. Boros S, Wilmarth PA, Kamps B, et al. Tissue transglutaminase catalyzes the deamidation of glutamines in lens β(2)- and β(3)-crystallins. Exp Eye Res. 2008;86(2):383-393.
67. Dunten RL, Cohen RE. Recognition of modified forms of ribonuclease A by the ubiquitin system. J Biol Chem. 1989;264(28): 16739-16747.
68. Huebscher KJ, Lee J, Rovelli G, et al. Protein isoaspartyl methyltransferase protects from Bax-induced apoptosis. Gene. 1999; 240(2):333-341.
69. Santa-Maria I, Perez M, Hernandez F, Munoz V, Moreno FJ, Avila J. In vitro tau fibrillization: mapping protein regions. Biochim Biophys Acta. 2006;1762(7):683-692.
70. Miyasaka T, Watanabe A, Saito Y, et al. Visualization of newly deposited tau in neurofibrillary tangles and neuropil threads. J Neuropathol Exp Neurol. 2005;64(8):665-674.
71. Zetterberg M, Petersen A, Sjöstrand J, Karlsson J. Proteasome activity in human lens nuclei and correlation with age, gender and severity of cataract. Curr Eye Res. 2003;27(1):45-53.
72. Zhang T, Liu Y, Wu M, Luo L, Jiang Y, Yuan Z. [Compare the proteasome activity in the epithelium of human age-related cataract and normal lens]. Yan Ke Xue Bao. 2006;22(2):89-91, 102.
73. Jahngen JH, Lipman RD, Eisenhauer DA, Jahngen EG Jr, Taylor A. Aging and cellular maturation cause changes in ubiquitin-eye lens protein conjugates. Arch Biochem Biophys. 1990;276(1):32-37.
74. Pereira P, Shang F, Hobbs M, Girão H, Taylor A. Lens fibers have a fully functional ubiquitin-proteasome pathway. Exp Eye Res. 2003; 76(5):623-631.
75. Girão H, Pereira P, Taylor A, Shang F. Subcellular redistribution of components of the ubiquitin-proteasome pathway during lens differentiation and maturation. Invest Ophthalmol Vis Sci. 2005; 46(4):1386-1392.
76. Varshavsky A. The N-end rule pathway of protein degradation. Genes Cells. 1997;2(1):13-28.
77. Baker RT, Varshavsky A. Yeast N-terminal amidase: a new enzyme and component of the N-end rule pathway. J Biol Chem. 1995; 270(20):12065-12074.
78. Doye A, Mettouchi A, Bossis G, et al. CNF1 exploits the ubiquitinproteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell. 2002;111(4):553-564.
79. Kim YH, Kapfer DM, Boekhorst J, et al. Deamidation, but not truncation, decreases the urea stability of a lens structural protein, β1-crystallin. Biochemistry. 2002;41(47):14076-14084.
80. Lampi KJ, Kim YH, Bächinger HP, et al. Decreased heat stability and increased chaperone requirement of modified human betaβ1-crystallins. Mol Vis. 2002;8:359-366.
81. Van Montfort RL, Bateman OA, Lubsen NH, Slingsby C. Crystal structure of truncated human β1-crystallin. Protein Sci. 2003; 12(11):2606-2612.
82. Lapatto R, Nalini V, Bax B, et al. High resolution structure of an oligomeric eye lens β -crystallin: loops, arches, linkers and interfaces in β2 dimer compared to a monomeric β -crystallin. J Mol Biol. 1991;222(4):1067-1083.
83. Nalini V, Bax B, Driessen H, Moss DS, Lindley PF, Slingsby C. Close packing of an oligomeric eye lens β -crystallin induces loss of symmetry and ordering of sequence extensions. J Mol Biol. 1994; 236(4):1250-1258.
84. Sergeev YV, Hejtmancik JF, Wingfield PT. Energetics of domaindomain interactions and entropy driven association of β -crystallins. Biochemistry. 2004;43(2):415-424.