Thioredoxin glycation: A novel posttranslational modification that inhibits its antioxidant and organ protective actions

Free Radical Biology and Medicine

Volumn 49, Issue 3, 2010, Pages 332-338

  Yuan, Yuexing ^a   Jiao, Xiangying ^a   Lau, Wayne Bond ^a   Wang, Yajing ^a   Christopher, Theodore A ^a   Lopez, Bernard L ^a   RamachandraRao, Satish P ^a   Tao, Ling ^a   Ma, Xin Liang ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Organ injury; Posttranslational protein modification; Sepsis

Indexed keywords

AMINOGUANIDINE; FRUCTOSAMINE; LIPID A; LIPOPOLYSACCHARIDE; RIBOSE; THIOREDOXIN 1; ANTIOXIDANT; GUANIDINE DERIVATIVE; THIOREDOXIN;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG DETERMINATION; GLYCATION; IN VITRO STUDY; INCUBATION TIME; LIVER INJURY; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PERIODIC ACID SCHIFF STAIN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PROCESSING; ANIMAL; ANTAGONISTS AND INHIBITORS; GLYCOSYLATION; METABOLISM;

ANIMALS; ANTIOXIDANTS; GLYCOSYLATION; GUANIDINES; LIPOPOLYSACCHARIDES; MALE; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; THIOREDOXINS;

EID: 77954142597     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.04.017     Document Type: Article

References (39)

1. Nakamura H., Nakamura K., Yodoi J. Redox regulation of cellular activation. Annu. Rev. Immunol. 1997, 15:351-369.
2. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998, 17:2596-2606.
3. Nishiyama A., Matsui M., Iwata S., Hirota K., Masutani H., Nakamura H., Takagi Y., Sono H., Gon Y., Yodoi J. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J. Biol. Chem. 1999, 274:21645-21650.
4. Kondo N., Ishii Y., Kwon Y.W., Tanito M., Horita H., Nishinaka Y., Nakamura H., Yodoi J. Redox-sensing release of human thioredoxin from T lymphocytes with negative feedback loops. J. Immunol. 2004, 172:442-448.
5. Tsutsui T., Koide H., Fukahori H., Isoda K., Higashiyama S., Maeda I., Tashiro F., Yamato E., Miyazaki J.I., Yodoi J., Kawase M., Yagi K. Adenoviral transfection of hepatocytes with the thioredoxin gene confers protection against apoptosis and necrosis. Biochem. Biophys. Res. Commun. 2003, 307:765-770.
6. Sano H., Sata T., Nanri H., Ikeda M., Shigematsu A. Thioredoxin is associated with endotoxin tolerance in mice. Crit. Care Med. 2002, 30:190-194.
7. Casagrande S., Bonetto V., Fratelli M., Gianazza E., Eberini I., Massignan T., Salmona M., Chang G., Holmgren A., Ghezzi P. Glutathionylation of human thioredoxin: a possible crosstalk between the glutathione and thioredoxin systems. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9745-9749.
8. Haendeler J., Hoffmann J., Tischler V., Berk B.C., Zeiher A.M., Dimmeler S. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 2002, 4:743-749.
9. Haendeler J., Hoffmann J., Zeiher A.M., Dimmeler S. Antioxidant effects of statins via S-nitrosylation and activation of thioredoxin in endothelial cells. A novel vasculoprotective function of statins. Circulation 2004, 110:856-861.
10. Tao L., Gao E., Bryan N.S., Qu Y., Liu H.R., Hu A., Christopher T.A., Lopez B.L., Yodoi J., Koch W.J., Feelisch M., Ma X.L. Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: role of S-nitrosation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11471-11476.
11. Tao L., Jiao X., Gao E., Lau W.B., Yuan Y., Lopez B., Christopher T., Ramachandrarao S.P., Williams W., Southan G., Sharma K., Koch W., Ma X.L. Nitrative inactivation of thioredoxin-1 and its role in postischemic myocardial apoptosis. Circulation 2006, 114:1395-1402.
12. Martin G.S., Mannino D.M., Eaton S., Moss M. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 2003, 348:1546-1554.
13. Opal S.M. The clinical relevance of endotoxin in human sepsis: a critical analysis. J. Endotoxin Res. 2002, 8:473-476.
14. Okuyama H., Nakamura H., Shimahara Y., Uyama N., Kwon Y.W., Kawada N., Yamaoka Y., Yodoi J. Overexpression of thioredoxin prevents thioacetamide-induced hepatic fibrosis in mice. J. Hepatol. 2005, 42:117-123.
15. Okuyama H., Nakamura H., Shimahara Y., Araya S., Kawada N., Yamaoka Y., Yodoi J. Overexpression of thioredoxin prevents acute hepatitis caused by thioacetamide or lipopolysaccharide in mice. Hepatology 2003, 37:1015-1025.
16. Yamamoto M., Yang G., Hong C., Liu J., Holle E., Yu X., Wagner T., Vatner S.F., Sadoshima J. Inhibition of endogenous thioredoxin in the heart increases oxidative stress and cardiac hypertrophy. J. Clin. Invest. 2003, 112:1395-1406.
17. Kouzuma T., Usami T., Yamakoshi M., Takahashi M., Imamura S. An enzymatic method for the measurement of glycated albumin in biological samples. Clin. Chim. Acta 2002, 324:61-71.
18. Misenheimer T.M., Hahr A.J., Harms A.C., Annis D.S., Mosher D.F. Disulfide connectivity of recombinant C-terminal region of human thrombospondin 2. J. Biol. Chem. 2001, 276:45882-45887.
19. Pio R., Martinez A., Unsworth E.J., Kowalak J.A., Bengoechea J.A., Zipfel P.F., Elsasser T.H., Cuttitta F. Complement factor H is a serum-binding protein for adrenomedullin, and the resulting complex modulates the bioactivities of both partners. J. Biol. Chem. 2001, 276:12292-12300.
20. Tao L., Gao E., Hu A., Coletti C., Wang Y., Christopher T.A., Lopez B.L., Koch W., Ma X.L. Thioredoxin reduces post-ischemic myocardial apoptosis by reducing oxidative/nitrative stress. Br. J. Pharmacol. 2006, 149:311-318.
21. Ota K., Nakamura J., Li W., Kozakae M., Watarai A., Nakamura N., Yasuda Y., Nakashima E., Naruse K., Watabe K., Kato K., Oiso Y., Hamada Y. Metformin prevents methylglyoxal-induced apoptosis of mouse Schwann cells. Biochem. Biophys. Res. Commun. 2007, 357:270-275.
22. McCarthy A.D., Cortizo A.M., Gimenez S.G., Bruzzone L., Etcheverry S.B. Non-enzymatic glycosylation of alkaline phosphatase alters its biological properties. Mol. Cell. Biochem. 1998, 181:63-69.
23. Deutschman C.S., Andrejko K.M., Haber B.A., Bellin L., Elenko E., Harrison R., Taub R. Sepsis-induced depression of rat glucose-6-phosphatase gene expression and activity. Am. J. Physiol. 1997, 273:R1709-R1718.
24. Thorpe S.R., Baynes J.W. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 2003, 25:275-281.
25. Lapolla A., Traldi P., Fedele D. Importance of measuring products of non-enzymatic glycation of proteins. Clin. Biochem. 2005, 38:103-115.
26. Ahmed N., Thornalley P.J. Advanced glycation endproducts: what is their relevance to diabetic complications?. Diab. Obes. Metab. 2007, 9:233-245.
27. Furber J.D. Extracellular glycation crosslinks: prospects for removal. Rejuvenation Res. 2006, 9:274-278.
28. Wolffenbuttel B.H., Boulanger C.M., Crijns F.R., Huijberts M.S., Poitevin P., Swennen G.N., Vasan S., Egan J.J., Ulrich P., Cerami A., Levy B.I. Breakers of advanced glycation end products restore large artery properties in experimental diabetes. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:4630-4634.
29. Kang J.H. Modification and inactivation of human Cu,Zn-superoxide dismutase by methylglyoxal. Mol. Cells 2003, 15:194-199.
30. Sen S., Bose T., Roy A., Chakraborti A.S. Effect of non-enzymatic glycation on esterase activities of hemoglobin and myoglobin. Mol. Cell. Biochem. 2007, 301:251-257.
31. Monnier V.M. Intervention against the Maillard reaction in vivo. Arch. Biochem. Biophys. 2003, 419:1-15.
32. Brownlee M., Vlassara H., Kooney A., Ulrich P., Cerami A. Aminoguanidine prevents diabetes-induced arterial wall protein cross-linking. Science 1986, 232:1629-1632.
33. Tsuji G., Koshiba M., Nakamura H., Kosaka H., Hatachi S., Kurimoto C., Kurosaka M., Hayashi Y., Yodoi J., Kumagai S. Thioredoxin protects against joint destruction in a murine arthritis model. Free Radic. Biol. Med. 2006, 40:1721-1731.
34. Yoshida T., Oka S.I., Masutani H., Nakamura H., Yodoi J. The role of thioredoxin in the aging process: involvement of oxidative stress. Antioxid. Redox Signal. 2003, 5:563-570.
35. Ramasamy R., Yan S.F., Schmidt A.M. Methylglyoxal comes of AGE. Cell 2006, 124:258-260.
36. Asif M., Egan J., Vasan S., Jyothirmayi G.N., Masurekar M.R., Lopez S., Williams C., Torres R.L., Wagle D., Ulrich P., Cerami A., Brines M., Regan T.J. An advanced glycation endproduct cross-link breaker can reverse age-related increases in myocardial stiffness. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:2809-2813.
37. Xu S.Z., Sukumar P., Zeng F., Li J., Jairaman A., English A., Naylor J., Ciurtin C., Majeed Y., Milligan C.J., Bahnasi Y.M., Al-Shawaf E., Porter K.E., Jiang L.H., Emery P., Sivaprasadarao A., Beech D.J. TRPC channel activation by extracellular thioredoxin. Nature 2008, 451:69-72.
38. Nakamura H., Masutani H., Yodoi J. Extracellular thioredoxin and thioredoxin-binding protein 2 in control of cancer. Semin. Cancer Biol. 2006, 16:444-451.
39. Cowan D.B., Noria S., Stamm C., Garcia L.M., Poutias D.N., del Nido P.J., McGowan F.X. Lipopolysaccharide internalization activates endotoxin-dependent signal transduction in cardiomyocytes. Circ. Res. 2001, 88:491-498.