Metallothionein prolongs survival and antagonizes senescence-associated cardiomyocyte diastolic dysfunction: Role of oxidative stress

FASEB Journal

Volumn 20, Issue 7, 2006, Pages

  Yang, Xiaoping ^a   Doser, Thomas A ^a   Fang, Cindy X ^a   Nunn, Jennifer M ^a   Janardhanan, Rajiv ^a   Zhu, Meijun ^a   Sreejayan, Nair ^c   Quinn, Mark T ^b   Ren, Jun ^a  

^a UNIVERSITY OF WYOMING   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

^c NONE

Author keywords

Antioxidant; Contraction; Longevity; Oxidative stress

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACONITATE HYDRATASE; CALCIUM; CYTOCHROME C; METALLOTHIONEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SUPEROXIDE; 3 NITROTYROSINE; 3-NITROTYROSINE; DRUG DERIVATIVE; PYROGALLOL; TYROSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CELL AGING; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; ENZYME ACTIVITY; HEART MUSCLE CELL; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SENESCENCE; AGING; ANIMAL; APOPTOSIS; CYTOLOGY; DIASTOLE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HEART CONTRACTION; HEART VENTRICLE; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

MUS MUSCULUS;

ACONITATE HYDRATASE; AGING; ANIMALS; APOPTOSIS; CALCIUM; CYTOCHROMES C; DIASTOLE; GENE EXPRESSION REGULATION; HEART VENTRICLES; METALLOTHIONEIN; MICE; MICE, TRANSGENIC; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; OXIDATIVE STRESS; PYROGALLOL; RHOA GTP-BINDING PROTEIN; SUPEROXIDES; TYROSINE;

EID: 33744456501     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-5288fje     Document Type: Article

References (47)

1. Li, S. Y., Du, M., Dolence, E. K., Fang, C. X., Mayer, G. E., Ceylan-Isik, A. F., LaCour, K. H., Yang, X., Wilbert, C. J., Sreejayan, N., and Ren, J. (2005) Aging induces cardiac diastolic dysfunction, oxidative stress, accumulation of advanced glycation endproducts and protein modification. Aging Cell 4, 57-64
2. Harman, D. (1981) The aging process. Proc. Natl. Acad. Sci. U. S. A. 78, 7124-7128
3. Stadtman, E. R., Starke-Reed, P. E., Oliver, C. N., Carney, J. M., and Floyd, R. A. (1992) Protein modification in aging. EXS. 62, 64-72
4. Sohal, R. S., and Weindruch, R. (1996) Oxidative stress, caloric restriction, and aging. Science 273, 59-63
5. Dhalla, N. S., Temsah, R. M., and Netticadan, T. (2000) Role of oxidative stress in cardiovascular diseases. J. Hypertens. 18, 655-673
6. Dhalla, N. S., and Temsah, R. M. (2001) Sarcoplasmic reticulum and cardiac oxidative stress: an emerging target for heart disease. Expert Opin. Ther. Targets 5, 205-217
7. Harman, D. (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11, 298-300
8. Alexeyev, M. F., Ledoux, S. P., and Wilson, G. L. (2004) Mitochondrial DNA and aging. Clin. Sci. (Lond) 107, 355-364
9. Monahan, K. D., Eskurza, I., and Seals, D. R. (2004) Ascorbic acid increases cardiovagal baroreflex sensitivity in healthy older men. Am. J. Physiol. Heart Circ. Physiol. 286, H2113-2117
10. Yang, X., Sreejayan, N., and Ren, J. (2005) Views from within and beyond: narratives of cardiac contractile dysfunction under senescence. Endocrine 26, 127-137
11. Lakatta, E. G., and Levy, D. (2003) Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: Part II: the aging heart in health: links to heart disease. Circulation 107, 346-354
12. Cai, L., Wang, J., Li, Y., Sun, X., Wang, L., Zhou, Z., and Kang, Y. J. (2005) Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 54, 1829-1837
13. Ye, G., Metreveli, N. S., Ren, J., and Epstein, P. N. (2003) Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting ROS production. Diabetes 52, 777-783
14. Kang, Y. J., Chen, Y., Yu, A., Voss-McCowan, M., and Epstein, P. N. (1997) Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J. Clin. Invest. 100, 1501-1506
15. Duan, J., Zhang, H. Y., Adkins, S. D., Ren, B. H., Norby, F. L., Zhang, X., Benoit, J. N., Epstein, P. N., and Ren, J. (2003) Impaired cardiac function and insulin-like growth factor-I response in myocytes from calmodulin-diabetic mice: role of Akt and RhoA. Am. J. Physiol. Endocrinol. Metab. 284, E366-376
16. Hool, L. C., Di Maria, C. A., Viola, H. M., and Arthur, P. G. (2005) Role of NAD(P)H oxidase in the regulation of cardiac L-type Ca2+ channel function during acute hypoxia. Cardiovasc Res. 67, 624-635
17. Esberg, L. B., and Ren, J. (2004) The oxygen radical generator pyrogallol impairs cardiomyocyte contractile function via a superoxide and p38 MAP kinase-dependent pathway: protection by anisodamine and tetramethylpyrazine. Cardiovasc Toxicol. 4, 375-384
18. Dong, F., Zhang, X., Culver, B., Chew, H. G., Kelley, R. O., and Ren, J. (2005) Dietary iron deficiency induces ventricular dilation, mitochondrial ultrastructural aberrations and cytochrome c release: involvement of nitric oxide synthase and protein tyrosine nitration. Clin. Sci. (Lond) 109, 277-286
19. DeLeo, F. R., Nauseef, W. M., Jesaitis, A. J., Burritt, J. B., Clark, R. A., and Quinn, M. T. (1995) A domain of p47phox that interacts with human neutrophil flavocytochrome b558. J. Biol. Chem. 270, 26246-26251
20. Song, Y., Wang, J., Li, Y., Du, Y., Arteel, G. E., Saari, J. T., Kang, Y. J., and Cai, L. (2005) Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am. J. Pathol. 167, 17-26
21. Dong, F., Zhang, X., Wold, L. E., Ren, Q., Zhang, Z., and Ren, J. (2005) Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1. Br. J. Pharmacol. 145, 323-333
22. Yarian, C. S., Rebrin, I., and Sohal, R. S. (2005) Aconitase and ATP synthase are targets of malondialdehyde modification and undergo an age-related decrease in activity in mouse heart mitochondria. Biochem. Biophys. Res. Commun. 330, 151-156
23. Kawamura, H., Yokote, K., Asaumi, S., Kobayashi, K., Fujimoto, M., Maezawa, Y., Saito, Y., and Mori, S. (2004) High Glc-induced upregulation of osteopontin is mediated via Rho/Rho kinase pathway in cultured rat aortic smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 276-281
24. Chung, L., and Ng, Y. C. (2005) Age-related alterations in expression of apoptosis regulatory proteins and heat shock proteins in rat skeletal muscle. Biochim. Biophys. Acta 1762, 103-109
25. Kurosu, H., Yamamoto, M., Clark, J. D., Pastor, J. V., Nandi, A., Gurnani, P., McGuinness, O. P., Chikuda, H., Yamaguchi, M., Kawaguchi, H., Shimomura, I., Takayama, Y., Herz, J., Kahn, C. R., Rosenblatt, K. P., and Kuro-o, M. (2005) Suppression of aging in mice by the hormone Klotho. Science 309, 1829-1833
26. Bindokas, V. P., Jordan, J., Lee, C. C., and Miller, R. J. (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16, 1324-1336
27. Cai, H., Griendling, K. K., and Harrison, D. G. (2003) The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol. Sci. 24, 471-478
28. Wang, G. W., Schuschke, D. A., and Kang, Y. J. (1999) Metallothionein-overexpressing neonatal mouse cardiomyocytes are resistant to H2O2 toxicity. Am. J. Physiol. 276, H167-175
29. Cai, L., and Kang, Y. J. (2001) Oxidative stress and diabetic cardiomyopathy: a brief review. Cardiovasc Toxicol. 1, 181-193
30. Jin, L., Ying, Z., and Webb, R. C. (2004) Activation of Rho/Rho kinase signaling pathway by ROS in rat aorta. Am. J. Physiol. Heart Circ. Physiol. 287, H1495-1500
31. Rikitake, Y., and Liao, J. K. (2005) Rho-kinase mediates hyperglycemia-induced plasminogen activator inhibitor-1 expression in vascular endothelial cells. Circulation 111, 3261-3268
32. Luo, J. D., and Chen, A. F. (2003) Perspectives on the cardioprotective effects of statins. Curr. Med. Chem. 10, 1593-1601
33. Ren, J., and Fang, C. X. (2005) Small guanine nucleotide-binding protein Rho and myocardial function. Acta Pharmacol. Sin. 26, 279-285
34. Matsuoka, Y., Picciano, M., La Francois, J., and Duff, K. (2001) Fibrillar beta-amyloid evokes oxidative damage in a transgenic mouse model of Alzheimer's disease. Neuroscience 104, 609-613
35. Yan, L. J., Levine, R. L., and Sohal, R. S. (1997) Oxidative damage during aging targets mitochondrial aconitase. Proc. Natl. Acad. Sci. U. S. A. 94, 11168-11172
36. Schriner, S. E., Linford, N. J., Martin, G. M., Treuting, P., Ogburn, C. E., Emond, M., Coskun, P. E., Ladiges, W., Wolf, N., Van Remmen, H., Wallace, D. C., and Rabinovitch, P. S. (2005) Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308, 1909-1911
37. Gardner, P. R., and Fridovich, I. (1992) Inactivation-reactivation of aconitase in Escherichia coli. A sensitive measure of superoxide radical. J. Biol. Chem. 267, 8757-8763
38. Kanda, T., Wakino, S., Homma, K., Yoshioka, K., Tatematsu, S., Hasegawa, K., Takamatsu, I., Sugano, N., Hayashi, K., and Saruta, T. (2005) Rho-kinase as a molecular target for insulin resistance and hypertension. FASEB J. In press
39. Fridovich, I. (2004) Mitochondria: are they the seat of senescence? Aging Cell 3, 13-16
40. Benderdour, M., Charron, G., Comte, B., Ayoub, R., Beaudry, D., Foisy, S., Deblois, D., and Des Rosiers, C. (2004) Decreased cardiac mitochondrial NADP+-isocitrate dehydrogenase activity and expression: a marker of oxidative stress in hypertrophy development. Am. J. Physiol. Heart Circ. Physiol. 287, H2122-2131
41. Benderdour, M., Charron, G., DeBlois, D., Comte, B., and Des Rosiers, C. (2003) Cardiac mitochondrial NADP+-isocitrate dehydrogenase is inactivated through 4-hydroxynonenal adduct formation: an event that precedes hypertrophy development. J. Biol. Chem. 278, 45154-45159
42. Ceconi, C., Boraso, A., Cargnoni, A., and Ferrari, R. (2003) Oxidative stress in cardiovascular disease: myth or fact? Arch Biochem. Biophys. 420, 217-221
43. Xu, Y., Armstrong, S. J., Arenas, I. A., Pehowich, D. J., and Davidge, S. T. (2004) Cardioprotection by chronic estrogen or superoxide dismutase mimetic treatment in the aged female rat. Am. J. Physiol. Heart Circ. Physiol. 287, H165-171
44. Kasapoglu, M., and Ozben, T. (2001) Alterations of antioxidant enzymes and oxidative stress markers in aging. Exp. Gerontol. 36, 209-220
45. Fang, C. X., Dong, F., Ren, B. H., Epstein, P. N., and Ren, J. (2005) Metallothionein alleviates cardiac contractile dysfunction induced by insulin resistance: role of Akt phosphorylation, PTB1B, PPARgamma and c-Jun. Diabetologia 48, 2412-2421
46. Sowers, J. R. (2004) Insulin resistance and hypertension. Am. J. Physiol. Heart Circ. Physiol 286, H1597-1602
47. Miao, L., Calvert, J. W., Tang, J., Parent, A. D., and Zhang, J. H. (2001) Age-related RhoA expression in blood vessels of rats. Mech. Ageing Dev. 122, 1757-1770