Glutaredoxin 2 (Grx2) gene deletion induces early onset of age-dependent cataracts in mice

Journal of Biological Chemistry

Volumn 289, Issue 52, 2014, Pages 36125-36139

  Wu, Hongli ^a,b   Yu, Yibo ^a,c   David, Larry ^d   Ho, Ye Shih ^e   Lou, Marjorie F ^a,f  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e WAYNE STATE UNIVERSITY   (United States)

^f UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; GENES; MAMMALS; MASS SPECTROMETRY; MITOCHONDRIA; OPACITY; PLANTS (BOTANY);

AGE-MATCHED CONTROLS; BIOCHEMICAL CHANGES; CATARACT FORMATION; DISULFIDE REDUCTASE; GLUTATHIONYLATION; MITOCHONDRIAL FUNCTION; PEROXIDASE ACTIVITIES; STRUCTURAL PROTEINS;

PROTEINS;

ACTIN; ADENOSINE TRIPHOSPHATE; ALPHA CRYSTALLIN; BETA B2 CRYSTALLIN; COAT PROTEIN COMPLEX I; CYTOCHROME C OXIDASE; GLOBULIN; GLUTAREDOXIN; GLUTAREDOXIN 2; GLUTATHIONE; STRUCTURAL PROTEIN; THIOL PROTEINASE; THIOREDOXIN 1; THIOREDOXIN 2; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL; CYSTINE; EYE PROTEIN; GLRX2 PROTEIN, MOUSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATARACT; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENZYME SYNTHESIS; EYE EXAMINATION; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GRX2 GENE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; SLIT LAMP; TISSUE LEVEL; WESTERN BLOTTING; WILD TYPE; 129 MOUSE; ANIMAL; GENETICS; LENS CAPSULE; METABOLISM; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CATARACT; CYSTINE; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX IV; EYE PROTEINS; GENE DELETION; GLUTAREDOXINS; GLUTATHIONE; LENS CAPSULE, CRYSTALLINE; MALE; MICE, 129 STRAIN; MICE, KNOCKOUT;

EID: 84919797503     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.620047     Document Type: Article

References (60)

1. Finkel, T., and Holbrook, N. J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247
2. Barnham, K. J., Masters, C. L., and Bush, A. I. (2004) Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov. 3, 205-214
3. Jenner, P. (2003) Oxidative stress in Parkinson's disease. Ann. Neurol. 53, S26-S38
4. Bhat, H. K., Calaf, G., Hei, T. K., Loya, T., and Vadgama, J. V. (2003) Critical role of oxidative stress in estrogen-induced carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 3913-3918
5. Beatty, S., Koh, H., Phil, M., Henson, D., and Boulton, M. (2000) The role of oxidative stress in the pathogenesis of age-related macular degeneration. Surv. Ophthalmol. 45, 115-134
6. Spector, A. (1995) Oxidative stress-induced cataract: mechanism of action. FASEB J. 9, 1173-1182
7. Lou, M. F. (2003) Redox regulation in the lens. Prog. Retin. Eye Res. 22, 657-682
8. Grek, C. L., Zhang, J., Manevich, Y., Townsend, D. M., and Tew, K. D. (2013) Causes and consequences of cysteine S-glutathionylation. J. Biol. Chem. 288, 26497-26504
9. Mieyal, J. J., Gallogly, M. M., Qanungo, S., Sabens, E. A., and Shelton, M. D. (2008) Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid. Redox Signal. 10, 1941-1988
10. Gallogly, M. M., and Mieyal, J. J. (2007) Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress. Curr. Opin. Pharmacol. 7, 381-391
11. st century perspective. Br. J. Ophthalmol. 85, 261-266
12. Harding, J. J., Crabbe, M. J. (1984) in The Lens: Development, Proteins, Metabolism and Cataract (Davson, H., ed) Vol. 1, pp. 207-492, Academic Press, Orlando
13. Lou, M. F., and Dickerson, J. E., Jr. (1992) Protein-thiol mixed disulfides in human lens. Exp. Eye Res. 55, 889-896
14. Lou, M. F., Huang, Q. L., and Zigler, J. S., Jr. (1989) Effect of opacification and pigmentation on human lens protein thiol/disulfide and solubility. Curr. Eye Res. 8, 883-890
15. Lou, M. F., Dickerson, J. E., Jr., Tung, W. H., Wolfe, J. K., and Chylack, L. T., Jr. (1999) Correlation of nuclear color and opalescence with protein Sthiolation in human lenses. Exp. Eye Res. 68, 547-552
16. Lou, M. (2004) in Redox-Genome Interactions in Health and Disease (Fuchs, J., Podda, M., and Packer, L., eds) pp. 325-350, Marcel Dekker, Inc., New York
17. Fecondo, J. V., and Augusteyn, R. C. (1983) Superoxide dismutase, catalase and glutathione peroxidase in the human cataractous lens. Exp. Eye Res. 36, 15-23
18. Raghavachari, N., and Lou, M. F. (1996) Evidence for the presence of thioltransferase in the lens. Exp. Eye Res. 63, 433-441
19. Qiao, F., Xing, K., and Lou, M. F. (2000) Modulation of lens glycolytic pathway by thioltransferase. Exp. Eye Res. 70, 745-753
20. Xing, K. Y., and Lou, M. F. (2002) Effect of H2O2 on human lens epithelial cells and the possible mechanism for oxidative damage repair by thioltransferase. Exp. Eye Res. 74, 113-122
21. Yegorova, S., Liu, A., and Lou, M. F. (2003) Human lens thioredoxin: molecular cloning and functional characterization. Invest. Ophthalmol. Vis. Sci. 44, 3263-3271
22. Fernando, M. R., Satake, M., Monnier, V. M., and Lou, M. F. (2004) Thioltransferase mediated ascorbate recycling in human lens epithelial cells. Invest. Ophthalmol. Vis. Sci. 45, 230-237
23. Mannervik, B., and Axelsson, K. (1980) Role of cytoplasmic thioltransferase in cellular regulation by thiol-disulphide interchange. Biochem. J. 190, 125-130
24. Axelsson, K., and Mannervik, B. (1983) An essential role of cytosolic thioltransferase in protection of pyruvate kinase from rabbit liver against oxidative inactivation. FEBS Lett. 152, 114-118
25. Holmgren, A. (1989) Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264, 13963-13966
26. Shelton, M. D., Chock, P. B., and Mieyal, J. J. (2005) Glutaredoxin: role in reversible protein S-glutathionylation and regulation of redox signal transduction and protein translocation. Antioxid. Redox Signal. 7, 348-366
27. Gladyshev, V. N., Liu, A., Novoselov, S. V., Krysan, K., Sun, Q. A., Kryukov, V. M., Kryukov, G. V., and Lou, M. F. (2001) Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J. Biol. Chem. 276, 30374-30380
28. Lundberg, M., Johansson, C., Chandra, J., Enoksson, M., Jacobsson, G., Ljung, J., Johansson, M., and Holmgren, A. (2001) Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J. Biol. Chem. 276, 26269-26275
29. Lillig, C. H., Berndt, C., Vergnolle, O., Lönn, M. E., Hudemann, C., Bill, E., and Holmgren, A. (2005) Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc. Natl. Acad. Sci. U.S.A. 102, 8168-8173
30. Tian, X. L., Upadhyaya, B., Wu, H. L., and Lou, M. F. (2013) Expression and distribution of thiol-regulating enzyme glutaredoxin 2 (Grx2) in porcine ocular tissues. Invest. Ophthalmol. Vis. Sci. 54, (Abstr. 4936)
31. Fernando, M. R., Lechner, J. M., Löfgren, S., Gladyshev, V. N., and Lou, M. F. (2006) Mitochondrial thioltransferase (glutaredoxin 2) has GSH-dependent and thioredoxin reductase-dependent peroxidase activities in vitro and in lens epithelial cells. FASEB J. 20, 2645-2647
32. Wu, H. L., Xing, K. Y., and Lou, M. F. (2009) Mitochondrial glutaredoxin (Grx2) protects human lens epithelial cells from H2O2-induced apoptosis via defending complex I from oxidation damage ARVO Meeting Abstracts (Abstr. 2541)
33. Moon, S., Fernando, M. R., and Lou, M. F. (2005) Induction of thioltransferase and thioredoxin/thioredoxin reductase systems in cultured porcine lenses under oxidative stress. Invest. Ophthalmol. Vis. Sci. 46, 3783-3789
34. Beer, S. M., Taylor, E. R., Brown, S. E., Dahm, C. C., Costa, N. J., Runswick, M. J., and Murphy, M. P. (2004) Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol proteins: implications for mitochondrial redox regulation and antioxidant defence. J. Biol. Chem. 279, 47939-47951
35. Enoksson, M., Fernandes, A. P., Prast, S., Lillig, C. H., Holmgren, A., and Orrenius, S. (2005) Overexpression of glutaredoxin 2 attenuates apoptosis by preventing cytochrome c release. Biochem. Biophys. Res. Commun. 327, 774-779
36. Wu, H., Xing, K., and Lou, M. F. (2010) Glutaredoxin 2 prevents H2O2-induced cell apoptosis by protecting complex I activity in the mitochondria. Biochim. Biophys. Acta 1797, 1705-1715
37. Mailloux, R. J., Xuan, J. Y., Beauchamp, B., Jui, L., Lou, M., and Harper, M. E. (2013) Glutaredoxin-2 is required to control proton leak through uncoupling protein-3. J. Biol. Chem. 288, 8365-8379
38. Wu, H., Lin, L., Giblin, F., Ho, Y. S., and Lou, M. F. (2011) Glutaredoxin 2 knockout increases sensitivity to oxidative stress in mouse lens epithelial cells. Free Radic. Biol. Med. 51, 2108-2117
39. Tybulewicz, V. L., Crawford, C. E., Jackson, P. K., Bronson, R. T., and Mulligan, R. C. (1991) Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163
40. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J. C. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 90, 8424-8428
41. Bradley, A. (1987) in Tetratocarcinomas and Embryonic Stem Cells: A Practical Approach (Roberston, E. J., ed) pp. 113-151, IRL Press at Oxford University Press, Oxford
42. Ho, Y. S., Xiong, Y., Ho, D. S., Gao, J., Chua, B. H., Pai, H., and Mieyal, J. J. (2007) Targeted disruption of the glutaredoxin 1 gene does not sensitize adult mice to tissue injury induced by ischemia/reperfusion and hyperoxia. Free Radic. Biol. Med. 43, 1299-1312
43. Chylack, L. T., Jr., Leske, M. C., McCarthy, D., Khu, P., Kashiwagi, T., and Sperduto, R. (1989) Lens opacities classification system II (LOCS II). Arch. Ophthalmol. 107, 991-997
44. Rehncrona, S., Mela, L., and Siesjö, B. K. (1979) Recovery of brain mitochondrial function in the rat after complete and incomplete cerebral ischemia. Stroke 10, 437-446
45. Lou, M. F., Dickerson, J. E., Jr., Garadi, R., and York, B. M., Jr. (1988) Glutathione depletion in the lens of galactosemic and diabetic rats. Exp. Eye Res. 46, 517-530
46. Lou, M. F., McKellar, R., and Chyan, O. (1986) Quantitation of lens protein mixed disulfides by ion-exchange chromatography. Exp. Eye Res. 42, 607-616
47. Yan, F. F., Pratt, E. B., Chen, P. C., Wang, F., Skach, W. R., David, L. L., and Shyng, S. L. (2010) Role of Hsp90 in biogenesis of the beta-cell ATPsensitive potassium channel complex. Mol. Biol. Cell 21, 1945-1954
48. Wilmarth, P. A., Riviere, M. A., and David, L. L. (2009) Techniques for accurate protein identification in shotgun proteomic studies of human, mouse, bovine, and chicken lenses. J. Ocul. Biol. Dis. Infor. 2, 223-234
49. Janssen, A. J., Trijbels, F. J., Sengers, R. C., Smeitink, J. A., van den Heuvel, L. P., Wintjes, L. T., Stoltenborg-Hogenkamp, B. J., and Rodenburg, R. J. (2007) Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin. Chem. 53, 729-734
50. Maquat, L. E., and Carmichael, G. G. (2001) Quality control of mRNA function. Cell 104, 173-176
51. Spector, A., and Roy, D. (1978) Disulfide-linked high molecular weight protein associated with human cataract. Proc. Natl. Acad. Sci. U.S.A. 75, 3244-3248
52. Augusteyn, R. (1981) in Mechanisms of Cataract Formation in the Human Lens (Duncan, G., ed) pp. 72-115, Academic Press, New York
53. Wolf, N., Penn, P., Pendergrass, W., Van Remmen, H., Bartke, A., Rabinovitch, P., and Martin, G. M. (2005) Age-related cataract progression in five mouse models for anti-oxidant protection or hormonal influence. Exp. Eye Res. 81, 276-285
54. Cherian, M., Smith, J. B., Jiang, X. Y., and Abraham, E. C. (1997) Influence of protein-glutathione mixed disulfide on the chaperone-like function of α-crystallin. J. Biol. Chem. 272, 29099-29103
55. Hanson, S. R., Chen, A. A., Smith, J. B., and Lou, M. F. (1999) Thiolation of the γB-crystallins in intact bovine lens exposed to hydrogen peroxide. J. Biol. Chem. 274, 4735-4742
56. Liang, J. N., and Pelletier, M. R. (1988) Destabilization of lens protein conformation by glutathione mixed disulfide. Exp. Eye Res. 47, 17-25
57. Kono, M., Sen, A. C., and Chakrabarti, B. (1990) Thermodynamics of thermal and athermal denaturation of γ-crystallins: changes in conformational stability upon glutathione reaction. Biochemistry 29, 464-470
58. Truscott, R. J., and Augusteyn, R. C. (1977) The state of sulphydryl groups in normal and cataractous human lenses. Exp. Eye Res. 25, 139-148
59. Pai, H. V., Starke, D. W., Lesnefsky, E. J., Hoppel, C. L., and Mieyal, J. J. (2007) What is the functional significance of the unique location of glutaredoxin 1 (GRx1) in the intermembrane space of mitochondria? Antioxid. Redox Signal. 9, 2027-2033
60. Löfgren, S., Fernando, M. R., Xing, K. Y., Wang, Y., Kuszynski, C. A., Ho, Y. S., and Lou, M. F. (2008) Effect of thioltransferase (glutaredoxin) deletion on cellular sensitivity to oxidative stress and cell proliferation in lens epithelial cells of thioltransferase knockout mouse. Invest. Ophthalmol. Vis. Sci. 49, 4497-4505