Degradation of C-terminal truncated αA-crystallins by the ubiquitin-proteasome pathway

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 9, 2007, Pages 4200-4208

  Zhang, Xinyu ^a   Dudek, Edward J ^a   Liu, Bingfen ^b   Ding, Linlin ^c   Fernandes, Alexandre F ^a   Liang, Jack J ^b   Horwitz, Joseph ^c   Taylor, Allen ^a   Shang, Fu ^a  

^a TUFTS UNIVERSITY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA CRYSTALLIN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; IODINE 125; OLIGOMER; PROTEASOME; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME 4; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE INHIBITOR; RECOMBINANT PROTEIN; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ESCHERICHIA COLI; FLUORESCENCE; HYDROPHOBICITY; LENS FIBER; LIGHT SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; RETICULOCYTE LYSATE; SPECTROSCOPY; THERMOSTABILITY; UBIQUITINATION; ULTRAVIOLET RADIATION; AMINO ACID SEQUENCE; ANIMAL; CATTLE; CHEMISTRY; GENE EXPRESSION; LENS; METABOLISM; PHYSIOLOGY; PROTEIN CONFORMATION;

ALPHA-CRYSTALLIN A CHAIN; AMINO ACID SEQUENCE; ANIMALS; CATTLE; CIRCULAR DICHROISM; CYSTEINE PROTEINASE INHIBITORS; GENE EXPRESSION; LENS, CRYSTALLINE; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 35148857088     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.07-0196     Document Type: Article

References (69)

1. Horwitz J. Alpha-crystallin. Exp Eye Res. 2003;76:145-153.
2. McDevitt DS, Hawkins JW, Jaworski CJ, Piatigorsky J. Isolation and partial characterization of the human alpha a-crystallin gene. Exp Eye Res. 1986;43:285-291.
3. Dubin RA, Ally AH, Chung S, Piatigorsky J. Human alpha b-crystallin gene and preferential promoter function in lens. Genomics. 1990;7:594-601.
4. Piatigorsky J. Molecular biology: recent studies on enzyme/crystallins and alpha-crystallin gene expression. Exp Eye Res. 1990;50:725-728.
5. Horwitz J. A-crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA. 1992;89:10449-10453.
6. Reddy GB, Das KP, Petrash JM, Surewicz WK. Temperature-dependent chaperone activity and structural properties of human alphaA- and alphaB-crystallins. J Biol Chem. 2000;275:4565-4570.
7. Boyle DL, Takemoto L, Brady JP, Wawrousek EF. Morphological characterization of the alpha A- and alpha B-crystallin double knockout mouse lens. BMC Ophthalmol. 2003;3:3.
8. Azuma M, David LL, Shearer TR. Cysteine protease inhibitor e64 reduces the rate of formation of selenite cataract in the whole animal. Curr Eye Res. 1991;10:657-666.
9. Azuma M, Fukiage C, David LL, Shearer TR. Activation of calpain in lens: a review and proposed mechanism. Exp Eye Res. 1997;64:529-538.
10. Qian W, Shichi H. Cataract formation by a semiquinone metabolite of acetaminophen in mice: possible involvement of ca(2+) and calpain activation. Exp Eye Res. 2000;71:567-574.
11. Nakamura Y, Fukiage C, Shih M, et al. Contribution of calpain lp82-induced proteolysis to experimental cataractogenesis in mice. Invest Ophthalmol Vis Sci. 2000;41:1460-1466.
12. David LL, Dickey BM, Shearer TR. Origin of urea soluble protein in the selenite cataract: role of β-crystallin proteolysis and calpain ii. Invest Ophthalmol Vis Sci. 1987;28:1148-1156.
13. Yoshida H, Murachi T, Tsukahara I. Degradation of actin and vimentin by calpain II, a ca2+-dependent cysteine proteinase, in bovine lens. FEBS Lett. 1984;170:259-262.
14. Shih M, David LL, Lampi KJ, et al. Proteolysis by m-calpain enhances in vitro light scattering by crystalline from human and bovine lenses. Curr Eye Res. 2001;22:458-469.
15. Kelley MJ, David LL, Iwasaki N, Wright J, Shearer TR. A-crystallin chaperone activity is reduced by calpain II in vitro and in selenite cataract. J Biol Chem. 1993;268:18844-18849.
16. Croall DE, DeMartino GN. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol Rev. 1991;71:813-847.
17. Biswas S, Harris F, Dennison S, Singh J, Phoenix DA. Calpains: targets of cataract prevention? Trends Mol Med. 2004;10:78-84.
18. Sorimachi H, Ishiura S, Suzuki K. Structure and physiological function of calpains. Biochem J. 1997;328:721-732.
19. Sorimachi H, Imajoh-Ohmi S, Emori Y, et al. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types: specific expression of the mRNA in skeletal muscle. J Biol Chem. 1989;264:20106-20111.
20. Fukiage C, Nakajima E, Ma H, Azuma M, Shearer TR. Characterization and regulation of lens-specific calpain lp82. J Biol Chem. 2002;277:20678-20685.
21. Shih M, Ma H, Nakajima E, et al. Biochemical properties of lens-specific calpain lp85. Exp Eye Res. 2006;82:146-152.
22. Azuma M, Shearer TR. Involvement of calpain in diamide induced cataract in cultured lenses. FEBS Lett. 1992;307:313-317.
23. Hightower KR, David LL, Shearer TR. Regional distribution of free calcium in selenite cataract: relation to calpain II. Invest Ophthalmol Vis Sci. 1987;28:1433-1436.
24. David LL, Wright JW, Shearer TR. Calpain II induced insolublization of lens β-crystallin polypeptides may induce cataract. Biochim Biophys Acta. 1992;1139:210-216.
25. Sakamoto-Mizutani K, Fukiage C, Tamada Y, Azuma M, Shearer TR. Contribution of ubiquitous calpains to cataractogenesis in the spontaneous diabetic wbn/kob rat. Exp Eye Res. 2002;75:611-617.
26. Shearer TR, Shih M, Azuma M, David LL. Precipitation of crystallins from young rat lens by endogenous calpain. Exp Eye Res. 1995;61:141-150.
27. Shearer TR, Shih M, Mizuno T, David LL. Crystallins from rat lens are especially susceptible to calpain-induced light scattering compared to other species. Curr Eye Res. 1996;15:860-868.
28. Tamada Y, Fukiage C, Mizutani K, et al. Calpain inhibitor, sja6017, reduces the rate of formation of selenite cataract in rats. Curr Eye Res. 2001;22:280-285.
29. David LL, Shearer TR. Purification of calpain ii from rat lens and determination of endogenous substrates. Exp Eye Res. 1986;42:227-238.
30. Ueda Y, Fukiage C, Shih M, Shearer TR, David LL. Mass measurements of c-terminally truncated alpha-crystallins from two-dimensional gels identify lp82 as a major endopeptidase in rat lens. Mol Cell Proteomics. 2002;1:357-365.
31. David LL, Shearer TR, Shih M. Sequence analysis of lens beta-crystallins suggests involvement of calpain in cataract formation. J Biol Chem. 1993;268:1937-1940.
32. Thampi P, Hassan A, Smith JB, Abraham EC. Enhanced c-terminal truncation of αA- and αB-crystallins in diabetic lenses. Invest Ophthalmol Vis Sci. 2002;43:3265-3272.
33. Shang F, Deng G, Obin M, et al. Ubiquitin-activating enzyme (e1) isoforms in lens epithelial cells: origin of translation, e2 specificity and cellular localization determined with novel site-specific antibodies. Exp Eye Res. 2001;73:827-836.
34. Shang F, Gong X, McAvoy JW, et al. Ubiquitin-dependent pathway is up-regulated in differentiating lens cells. Exp Eye Res. 1999;68:179-192.
35. Shang F, Gong X, Palmer HJ, Nowell TR, Taylor A. Age-related decline in ubiquitin conjugation in response to oxidative stress in the lens. Exp Eye Res. 1997;64:21-30.
36. Shang F, Gong X, Taylor A. Activity of ubiquitin dependent pathway in response to oxidative stress: ubiquitin activating enzyme (e1) is transiently upregulated. J Biol Chem. 1997;272:23086-23093.
37. Shang F, Nowell TR Jr, Taylor A. Removal of oxidatively damaged proteins from lens cells by the ubiquitin-proteasome pathway. Exp Eye Res. 2001;73:229-238.
38. Pereira P, Shang F, Girão H, Taylor A. Lens fibers have a fully functional ubiquitin-proteasome pathway. Exp Eye Res. 2003;76:623-631.
39. Shang F, Huang L, Taylor A. Degradation of native and oxidized beta- and gamma-crystallins using bovine lens epithelial cell and rabbit reticulocyte extracts. Curr Eye Res. 1994;13:423-431.
40. Dudek EJ, Shang F, Valverde P, et al. Selectivity of the ubiquitin pathway for oxidatively modified proteins: relevance to protein precipitation diseases. FASEB J. 2005;19:1707-1709.
41. Marques C, Guo W, Pereira P, et al. The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones. FASEB J. 2006;20:741-743.
42. Zetterberg M, Zhang X, Taylor A, et al. Glutathiolation enhances the degradation of γC-crystallin in lens and reticulocyte lysates, partially via the ubiquitin-proteasome pathway. Invest Ophthalmol Vis Sci. 2006;47:3467-3473.
43. Sun TX, Das BK, Liang JJ. Conformational and functional differences between recombinant human lens αA- and αB-crystallin. J Biol Chem. 1997;272:6220-6225.
44. Sun TX, Liang JJ. Intermolecular exchange and stabilization of recombinant human alphaA- and alphaB-crystallin. J Biol Chem. 1998;273:286-290.
45. Mach H, Middaugh CR, Lewis RV. Statistical determination of the average values of the extinction coefficients of tryptophan and tyrosine in native proteins. Anal Biochem. 1992;200:74-80.
46. Huang LL, Shang F, Nowell TR Jr, Taylor A. Degradation of differentially oxidized α-crystallins in bovine lens epithelial cells. Exp Eye Res. 1995;61:45-54.
47. Wing SS, Jain P. Molecular cloning, expression and characterization of a ubiquitin conjugation enzyme (e2(17)kb) highly expressed in rat testis. Biochem J. 1995;305(Pt 1):125-132.
48. Shang F, Deng G, Liu Q, et al. Lys6-modified ubiquitin inhibits ubiquitin-dependent protein degradation. J Biol Chem. 2005;280:20365-20374.
49. Yang JT, Wu CS, Martinez HM. Calculation of protein conformation from circular dichroism. Methods Enzymol. 1986;130:208-269.
50. Bloemendal M, Toumadje A, Johnson WC Jr. Bovine lens crystallins do contain helical structure: a circular dichroism study. Biochim Biophys Acta. 1999;1432:234-238.
51. Kosinski-Collins MS, King J. In vitro unfolding, refolding, and polymerization of human γD crystallin, a protein involved in cataract formation. Protein Sci. 2003;12:480-490.
52. Shaeffer JR. Monoubiquitinated alpha globin is an intermediate in the atp-dependent proteolysis of alpha globin. J Biol Chem. 1994;269:22205-22210.
53. Shaeffer JR. Atp-dependent proteolysis of hemoglobin alpha chains in beta-thalassemic hemolysates is ubiquitin-dependent. J Biol Chem. 1988;263:13663-13669.
54. Takeuchi N, Ouchida A, Kamei A. C-terminal truncation of alpha-crystallin in hereditary cataractous rat lens. Biol Pharm Bull. 2004;27:308-314.
55. Robertson LJ, Morton JD, Yamaguchi M, et al. Calpain may contribute to hereditary cataract formation in sheep. Invest Ophthalmol Vis Sci. 2005;46:4634-4640.
56. Thampi P, Abraham EC. Influence of the c-terminal residues on oligomerization of alpha a-crystallin. Biochemistry. 2003;42:11857-11863.
57. Taylor A, Daims M, Lee J, Surgenor T. Identification and quantification of leucine aminopeptidase in aged normal and cataractous human lenses and ability of bovine lens lap to cleave bovine crystallins. Curr Eye Res. 1982;2:41-56.
58. Taylor A. Aminopeptidases: towards a mechanism of action. Trends Biochem Sci. 1993;18:167-172.
59. Taylor A, Sanford D, Nowell T. Structure and function of bovine lens aminopeptidase and comparison with homologous aminopeptidases. In: Taylor A, ed. Aminopeptidases. Austin, TX: RG Landes Company; 1996:21-59.
60. Swaminathan S, Chandrasekher G, Venkataraman A, Pattabiraman TN. Proteases and protease inhibitory activities in normal mammalian lenses and human cataractous lenses. Biochem Med Metab Biol. 1986;35:184-190.
61. Srivastava OP, Ortwerth BJ. The effects of aging and cataract formation on the trypsin inhibitor activity of human lens. Exp Eye Res. 1989;48:25-36.
62. Shang F, Taylor A. Function of the ubiquitin proteolytic pathway in the eye. Exp Eye Res. 2004;78:1-14.
63. Jahngen-Hodge J, Laxman E, Zuliani A, Taylor A. Evidence for atp and ubiquitin degradation of proteins in cultured bovine lens epithelial cells. Exp Eye Res. 1991;52:41-47.
64. Jahngen-Hodge J, Cyr D, Laxman E, Taylor A. Ubiquitin and ubiquitin conjugates in human lens. Exp Eye Res. 1992;55:897-902.
65. Huang LL, Jahngen-Hodge J, Taylor A. Bovine lens epithelial cells have a ubiquitin-dependent proteolysis system. Biochim Biophys Acta. 1993;1175:181-187.
66. Jahngen JH, Haas AL, Ciechanover A, et al. The eye lens has an active ubiquitin-protein conjugation system. J Biol Chem. 1986;261:13760-13767.
67. Marques C, Pereira P, Taylor A, et al. Ubiquitin-dependent lysosomal degradation of the HNE-modified proteins in lens epithelial cells. FASEB J. 2004;18:1424-1426.
68. Shang F, Taylor A. Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem J. 1995;307:297-303.
69. David LL, Lampi KJ, Lund AL, Smith JB. The sequence of human βB1-crystallin cDNA allows mass spectrometric detection of betab1 protein missing portions of its N-terminal extension. J Biol Chem. 1996;271:4273-4279.