Glutaredoxin regulates apoptosis in cardiomyocytes via NFκb targets Bcl-2 and Bcl-xl: Implications for cardiac aging

Antioxidants and Redox Signaling

Volumn 12, Issue 12, 2010, Pages 1339-1353

  Gallogly, Molly M ^a   Shelton, Melissa D ^a   Qanungo, Suparna ^a   Pai, Harish V ^a   Starke, David W ^a   Hoppel, Charles L ^a   Lesnefsky, Edward J ^a,b   Mieyal, John J ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAREDOXIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN BCL 2; PROTEIN BCL XL;

AGED; AGING; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL LEVEL; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HEART MUSCLE CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RAT; REGULATORY MECHANISM;

AGING; ANIMALS; APOPTOSIS; BCL-X PROTEIN; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, BCL-2; GLUTAREDOXINS; HYDROGEN PEROXIDE; MALE; MYOCARDIUM; MYOCYTES, CARDIAC; NF-KAPPA B; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, INBRED F344; RNA, MESSENGER; RNA, SMALL INTERFERING;

ANIMALIA; RATTUS;

EID: 77951953059     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2009.2791     Document Type: Article

References (57)

1. Arner ES, Zhong L, and Holmgren A. Preparation and assay of mammalian thioredoxin and thioredoxin reductase. Methods Enzymol 300: 226-239, 1999.
2. Bergmann MW, Loser P, Dietz R, and von HR. Effect of NF-kappa B Inhibition on TNF-alpha-induced apoptosis and downstream pathways in cardiomyocytes. J Mol Cell Cardiol 33: 1223-1232, 2001.
3. Bonavita F, Stefanelli C, Giordano E, Columbaro M, Facchini A, Bonafe F, Caldarera CM, and Guarnieri C. H9c2 cardiac myoblasts undergo apoptosis in a model of ischemia consisting of serum deprivation and hypoxia: Inhibition by PMA. FEBS Lett 536: 85-91, 2003.
4. Brocheriou V, Hagege AA, Oubenaissa A, Lambert M, Mallet VO, Duriez M, Wassef M, Kahn A, Menasche P, and Gilgenkrantz H. Cardiac functional improvement by a human Bcl-2 transgene in a mouse model of ischemia= reperfusion injury. J Gene Med 2: 326-333, 2000.
5. Burke JR, Pattoli MA, Gregor KR, Brassil PJ, MacMaster JF, McIntyre KW, Yang X, Iotzova VS, Clarke W, Strand J, Qiu Y, and Zusi FC. BMS-345541 is a highly selective inhibitor of I kappa B kinase that binds at an allosteric site of the enzyme and blocks NF-kappa B-dependent transcription in mice. J Biol Chem 278: 1450-1456, 2003.
6. Chen YR, Chen CL, Pfeiffer DR, and Zweier JL. Mitochon-drial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem 282: 32640-32654, 2007.
7. Chrestensen CA, Starke DW, and Mieyal JJ. Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed dis-ulfides, and initiates apoptosis. J Biol Chem 275: 26556-26565, 2000.
8. Eaton P, Wright N, Hearse DJ, and Shattock MJ. Glycer-aldehyde phosphate dehydrogenase oxidation during cardiac ischemia and reperfusion. J Mol Cell Cardiol 34: 1549-1560, 2002.
9. Fiebig AA, Zhu W, Hollerbach C, Leber B, and Andrews DW. Bcl-XL is qualitatively different from and ten times more effective than Bcl-2 when expressed in a breast cancer cell line. BMC Cancer 6: 213, 2006.
10. Gallogly MM, Starke DW, and Mieyal JJ. Mechanistic and kinetic details of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 11: 1059-1081, 2009.
11. Gao ZQ, Yang C, Wang YY, Wang P, Chen HL, Zhang XD, Liu R, Li WL, Qin XJ, Liang X, and Hai CX. RAGE upre-gulation and nuclear factor-kappaB activation associated with ageing rat cardiomyocyte dysfunction. Gen Physiol Biophys 27: 152-158, 2008.
12. Gustafsson AB and Gottlieb RA. Bcl-2 family members and apoptosis, taken to heart. Am J Physiol Cell Physiol 292: C45-C51, 2007.
13. Han H, Long H, Wang H, Wang J, Zhang Y, and Wang Z. Progressive apoptotic cell death triggered by transient oxi-dative insult in H9c2 rat ventricular cells: A novel pattern of apoptosis and the mechanisms. Am J Physiol Heart Circ Physiol 286: H2169-H2182, 2004.
14. Hirota K, Matsui M, Murata M, Takashima Y, Cheng FS, Itoh T, Fukuda K, and Yodoi J. Nucleoredoxin, glutaredoxin, and thioredoxin differentially regulate NF-kappaB, AP-1, and CREB activation in HEK293 cells. Biochem Biophys Res Commun 274: 177-182, 2000.
15. Huang J, Ito Y, Morikawa M, Uchida H, Kobune M, Sasaki K, Abe T, and Hamada H. Bcl-xL gene transfer protects the heart against ischemia=reperfusion injury. Biochem Biophys Res Commun 311: 64-70, 2003.
16. Imahashi K, Schneider MD, Steenbergen C, and Murphy E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia=reperfusion injury. Circ Res 95: 734-741, 2004.
17. Jao SC, English Ospina SM, Berdis AJ, Starke DW, Post CB, and Mieyal JJ. Computational and mutational analysis of human glutaredoxin (thioltransferase): probing the molecular basis of the low pKa of cysteine 22 and its role in catalysis. Biochemistry 45: 4785-4796, 2006.
18. Jones WK, Brown M, Wilhide M, He S, and Ren X. NF-kappaB in cardiovascular disease: Diverse and specific effects of a "general" transcription factor? Cardiovasc Toxicol 5: 183-202, 2005.
19. Kajstura J, Cheng W, Sarangarajan R, Li P, Li B, Nitahara JA, Chapnick S, Reiss K, Olivetti G, and Anversa P. Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am J Physiol 271: H1215-H1228, 1996.
20. Kalogeropoulos A, Georgiopoulou V, Kritchevsky SB, Psaty BM, Smith NL, Newman AB, Rodondi N, Satterfield S, Bauer DC, Bibbins-Domingo K, Smith AL, Wilson PW, Vasan RS, Harris TB, and Butler J. Epidemiology of incident heart failure in a contemporary elderly cohort: The health, aging, and body composition study. Arch Intern Med 169: 708-715, 2009.
21. Kim JS, Jin Y, and Lemasters JJ. Reactive oxygen species, but not Ca2\+overloading, trigger pH-and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. Am J Physiol Heart Circ Physiol 290: H2024-H2034, 2006.
22. Lazou A, Iliodromitis EK, Cieslak D, Voskarides K, Mousikos S, Bofilis E, and Kremastinos DT. Ischemic but not mechanical preconditioning attenuates ischemia=reperfusion induced myocardial apoptosis in anaesthetized rabbits: The role of Bcl-2 family proteins and ERK1=2. Apoptosis 11: 2195-2204, 2006.
23. Lee Y and Gustafsson AB. Role of apoptosis in cardiovascular disease. Apoptosis 14: 536-548, 2009.
24. Lesnefsky EJ, Lundergan CF, Hodgson JM, Nair R, Reiner JS, Greenhouse SW, Califf RM, and Ross AM. Increased left ventricular dysfunction in elderly patients despite successful thrombolysis: The GUSTO-I angiographic experience. J Am Coll Cardiol 28: 331-337, 1996.
25. Lieber SC, Aubry N, Pain J, Diaz G, Kim SJ, and Vatner SF. Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. Am J Physiol Heart Circ Physiol 287: H645-H651, 2004.
26. Liu P, Xu B, Cavalieri TA, and Hock CE. Age-related difference in myocardial function and inflammation in a rat model of myocardial ischemia-reperfusion. Cardiovasc Res 56: 443-453, 2002.
27. Malik G, Nagy N, Ho YS, Maulik N, and Das DK. Role of glutaredoxin-1 in cardioprotection: An insight with Glrx1 transgenic and knockout animals. J Mol Cell Cardiol 44: 261-269, 2008.
28. Mani K. Programmed cell death in cardiac myocytes: Strategies to maximize post-ischemic salvage. Heart Fail Rev 13: 193-209, 2008.
29. Maulik N, Engelman RM, Rousou JA, Flack JE, III, Deaton D, and Das DK. Ischemic preconditioning reduces apoptosis by upregulating anti-death gene Bcl-2. Circulation 100: II369-II375, 1999.
30. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, and Shelton MD. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941-1988, 2008.
31. Moorjani N, Catarino P, Trabzuni D, Saleh S, Moorji A, Dzimiri N, Al-Mohanna F, Westaby S, and Ahmad M. Upregulation of Bcl-2 proteins during the transition to pressure overload-induced heart failure. Int J Cardiol 116: 27-33, 2007.
32. Murata H, Ihara Y, Nakamura H, Yodoi J, Sumikawa K, and Kondo T. Glutaredoxin exerts an antiapoptotic effect by regulating the redox state of Akt. J Biol Chem 278: 50226-50233, 2003.
33. Mustapha S, Kirshner A, De MD, and Kirshenbaum LA. A direct requirement of nuclear factor-kappa B for suppression of apoptosis in ventricular myocytes. Am J Physiol Heart Circ Physiol 279: H939-H945, 2000.
34. Nitahara JA, Cheng W, Liu Y, Li B, Leri A, Li P, Mogul D, Gambert SR, Kajstura J, and Anversa P. Intracellular calcium, DNase activity and myocyte apoptosis in aging Fischer 344 rats. J Mol Cell Cardiol 30: 519-535, 1998.
35. Okaya T, Blanchard J, Schuster R, Kuboki S, Husted T, Caldwell CC, Zingarelli B, Wong H, Solomkin JS, and Lentsch AB. Age-dependent responses to hepatic ischemia= reperfusion injury. Shock 24: 421-427, 2005.
36. Pan S and Berk BC. Glutathiolation regulates tumor necrosis factor-alpha-induced caspase-3 cleavage and apoptosis: Key role for glutaredoxin in the death pathway. Circ Res 100: 213-219, 2007.
37. Patel HH, Head BP, Petersen HN, Niesman IR, Huang D, Gross GJ, Insel PA, and Roth DM. Protection of adult rat cardiac myocytes from ischemic cell death: Role of caveolar microdomains and delta-opioid receptors. Am J Physiol Heart Circ Physiol 291: H344-H350, 2006.
38. Patel JR and Brewer GJ. Age-related differences in NFkap-paB translocation and Bcl-2=Bax ratio caused by TNFalpha and Abeta42 promote survival in middle-age neurons and death in old neurons. Exp Neurol 213: 93-100, 2008.
39. Qanungo S, Starke DW, Pai HV, Mieyal JJ, and Nieminen AL. Glutathione supplementation potentiates hypoxic apo-ptosis by S-glutathionylation of p65-NFkappaB. J Biol Chem 282: 18427-18436, 2007.
40. Rebrin I and Sohal RS. Pro-oxidant shift in glutathione redox state during aging. Adv Drug Deliv Rev 60: 1545-1552, 2008.
41. Reynaert NL, van der Vliet A, Guala AS, McGovern T, Hristova M, Pantano C, Heintz NH, Heim J, Ho YS, Matthews DE, Wouters EF, and Janssen-Heininger YM. Dynamic redox control of NF-kappaB through glutaredoxin-regulated S-glutathionylation of inhibitory kappaB kinase beta. Proc Natl Acad Sci USA 103: 13086-13091, 2006.
42. Rikans LE and Hornbrook KR. Thiol-disulfide exchange systems in the liver of aging Fischer 344 rats. Gerontology 44: 72-77, 1998.
43. Rong Y and Distelhorst CW. Bcl-2 protein family members: Versatile regulators of calcium signaling in cell survival and apoptosis. Annu Rev Physiol 70: 73-91, 2008.
44. Santa MC and Machado A. Age and sex related differences in some rat renal NADPH-consuming detoxification enzymes. Arch Gerontol Geriatr 5: 235-247, 1986.
45. Shelton MD, Kern TS, and Mieyal JJ. Glutaredoxin regulates nuclear factor kappa-B and intercellular adhesion molecule in Muller cells: Model of diabetic retinopathy. J Biol Chem 282: 12467-12474, 2007.
46. Shelton MD and Mieyal JJ. Regulation by reversible S-glutathionylation: Molecular targets implicated in inflammatory diseases. Mol Cells 25: 332-346, 2008.
47. Sohal RS, Farmer KJ, and Allen RG. Correlates of longevity in two strains of the housefly, Musca domestica. Mech Ageing Dev 40: 171-179, 1987.
48. Song JJ, Rhee JG, Suntharalingam M, Walsh SA, Spitz DR, and Lee YJ. Role of glutaredoxin in metabolic oxidative stress. Glutaredoxin as a sensor of oxidative stress mediated by H2O2. J Biol Chem 277: 46566-46575, 2002.
49. Starke DW, Chen Y, Bapna CP, Lesnefsky EJ, and Mieyal JJ. Sensitivity of protein sulfhydryl repair enzymes to oxidative stress. Free Radic Biol Med 23: 373-384, 1997.
50. Suh JH, Heath SH, and Hagen TM. Two subpopulations of mitochondria in the aging rat heart display heterogenous levels of oxidative stress. Free Radic Biol Med 35: 1064-1072, 2003.
51. Tanaka T, Nakamura H, Nishiyama A, Hosoi F, Masutani H, Wada H, and Yodoi J. Redox regulation by thioredoxin su-perfamily; Protection against oxidative stress and aging. Free Radic Res 33: 851-855, 2000.
52. Tani M, Suganuma Y, Hasegawa H, Shinmura K, Ebihara Y, Hayashi Y, Guo X, and Takayama M. Decrease in ischemic tolerance with aging in isolated perfused Fischer 344 rat hearts: Relation to increases in intracellular Na\+ after ischemia. J Mol Cell Cardiol 29: 3081-3089, 1997.
53. Wang J, Boja ES, Tan W, Tekle E, Fales HM, English S, Mieyal JJ, and Chock PB. Reversible glutathionylation regulates actin polymerization in A431 cells. J Biol Chem 276: 47763-47766, 2001.
54. Wang X, Zhang J, Kim HP, Wang Y, Choi AM, and Ryter SW. Bcl-XL disrupts death-inducing signal complex formation in plasma membrane induced by hypoxia= reoxygenation. FASEB J 18: 1826-1833, 2004.
55. Willems L, Zatta A, Holmgren K, Ashton KJ, and Headrick JP. Age-related changes in ischemic tolerance in male and female mouse hearts. J Mol Cell Cardiol 38: 245-256, 2005.
56. Zhang H, Tao L, Jiao X, Gao E, Lopez BL, Christopher TA, Koch W, and Ma XL. Nitrative thioredoxin inactivation as a cause of enhanced myocardial ischemia=reperfusion injury in the aging heart. Free Radic Biol Med 43: 39-47, 2007.
57. Zidar N, Jera J, Maja J, and Dusan S. Caspases in myocardial infarction. Adv Clin Chem 44: 1-33, 2007.