Ataxia telangiectasia mutated kinase plays a protective role in β-adrenergic receptor-stimulated cardiac myocyte apoptosis and myocardial remodeling

Molecular and Cellular Biochemistry

Volumn 353, Issue 1-2, 2011, Pages 13-22

  Foster, Cerrone R ^a   Singh, Mahipal ^a   Subramanian, Venkateswaran ^a   Singh, Krishna ^a  

^a East Tennessee State University   (United States)

Author keywords

1 Integrin; Apoptosis; ATM; Cardiac remodeling; p53

Indexed keywords

ATM PROTEIN; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; BETA1 INTEGRIN; COMPLEMENTARY DNA; GELATINASE A; GELATINASE B; PROTEIN BAX; PROTEIN P53; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA ADRENERGIC STIMULATION; BODY WEIGHT; CONTROLLED STUDY; FEMALE; HEART; HEART EJECTION FRACTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE FUNCTION; HEART WEIGHT; IN VITRO STUDY; M MODE ECHOCARDIOGRAPHY; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SHAM PROCEDURE; WILD TYPE;

ADRENERGIC BETA-AGONISTS; ANIMALS; ANTIGENS, CD29; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; HEART; ISOPROTERENOL; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MYOCARDIUM; MYOCYTES, CARDIAC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, ADRENERGIC, BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; VENTRICULAR REMODELING;

ATAXIA TELANGIECTASIA; MUS;

EID: 79959218250     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-011-0769-6     Document Type: Article

References (68)

1. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, Shiloh Y, Crawley JN, Ried T, Tagle D, Wynshaw-Boris A (1996) ATM-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171 (Pubitemid 26259926)
2. Ball LG, Xiao W (2005) Molecular basis of ataxia telangiectasia and related diseases. Acta Pharmacol Sin 26:897-907 (Pubitemid 41153209)
3. McKinnon PJ (2004) ATM and ataxia telangiectasia. EMBO Rep 5:772-776
4. Su Y, Swift M (2000) Mortality rates among carriers of ataxia-telangiectasia mutant alleles. Ann Intern Med 133:770-778
5. Rotman G, Shiloh Y (1998) ATM: from gene to function. Hum Mol Genet 7:1555-1563 (Pubitemid 28464032)
6. Khanna KK, Lavin MF, Jackson SP, Mulhern TD (2001) ATM, a central controller of cellular responses to DNA damage. Cell Death Differ 8:1052-1065 (Pubitemid 33061823)
7. Rotman G, Shiloh Y (1999) ATM: a mediator of multiple responses to genotoxic stress. Oncogene 18:6135-6144
8. Watters D, Kedar P, Spring K, Bjorkman J, Chen P, Gatei M, Birrell G, Garrone B, Srinivasa P, Crane DI, Lavin MF (1999) Localization of a portion of extranuclear ATM to peroxisomes. J Biol Chem 274:34277-34282 (Pubitemid 129511769)
9. Yang DQ, Kastan MB (2000) Participation of ATM in insulin signalling through phosphorylation of eIF-4E-binding protein 1. Nat Cell Biol 2:893-898
10. Barlow C, Ribaut-Barassin C, Zwingman TA, Pope AJ, Brown KD, Owens JW, Larson D, Harrington EA, Haeberle AM, Mariani J, Eckhaus M, Herrup K, Bailly Y, Wynshaw-Boris A (2000) ATM is a cytoplasmic protein in mouse brain required to prevent lysosomal accumulation. Proc Natl Acad Sci USA 97:871-876 (Pubitemid 30070402)
11. Oka A, Takashima S (1998) Expression of the ataxia-telangiectasia gene (ATM) product in human cerebellar neurons during development. Neurosci Lett 252:195-198 (Pubitemid 28400341)
12. Boehrs JK, He J, Halaby MJ, Yang DQ (2007) Constitutive expression and cytoplasmic compartmentalization of ATM protein in differentiated human neuron-like SH-SY5Y cells. J Neurochem 100:337-345 (Pubitemid 46010995)
13. Carlsson L, Abrahamsson T, Almgren O (1985) Local release of myocardial norepinephrine during acute ischemia: an experimental study in the isolated perfused rat heart. J Cardiovasc Pharmacol 7:791-798 (Pubitemid 15070355)
14. Behonick GS, Novak MJ, Nealley EW, Baskin SI (2001) Toxicology update: the cardiotoxicity of the oxidative stress metabolites of catecholamines (aminochromes). J Appl Toxicol 21(Suppl 1):S15-S22
15. Downing SE, Chen V (1985) Myocardial injury following endogenous catecholamine release in rabbits. J Mol Cell Cardiol 17:377-387 (Pubitemid 15030727)
16. Bos R, Mougenot N, Findji L, Mediani O, Vanhoutte PM, Lechat P (2005) Inhibition of catecholamine-induced cardiac fibrosis by an aldosterone antagonist. J Cardiovasc Pharmacol 45:8-13 (Pubitemid 40039749)
17. Colucci WS, Sawyer DB, Singh K, Communal C (2000) Adrenergic overload and apoptosis in heart failure: implications for therapy. J Card Fail 6:1-7 (Pubitemid 30439432)
18. Shizukuda Y, Buttrick PM, Geenen DL, Borczuk AC, Kitsis RN, Sonnenblick EH (1998) Beta-adrenergic stimulation causes cardiocyte apoptosis: influence of tachycardia and hypertrophy. Am J Physiol 275:H961-H968
19. Singh K, Xiao L, Remondino A, Sawyer DB, Colucci WS (2001) Adrenergic regulation of cardiac myocyte apoptosis. J Cell Physiol 189:257-265 (Pubitemid 33063293)
20. Krishnamurthy P, Subramanian V, Singh M, Singh K (2007) Beta1 integrins modulate beta-adrenergic receptor-stimulated cardiac myocyte apoptosis and myocardial remodeling. Hypertension 49:865-872 (Pubitemid 351664231)
21. Singh K, Communal C, Sawyer DB, Colucci WS (2000) Adrenergic regulation of myocardial apoptosis. Cardiovasc Res 45:713-719 (Pubitemid 30047138)
22. Haunstetter A, Izumo S (2000) Future perspectives and potential implications of cardiac myocyte apoptosis. Cardiovasc Res 45: 795-801 (Pubitemid 30047148)
23. Kajstura J, Bolli R, Sonnenblick EH, Anversa P, Leri A (2006) Cause of death: suicide. J Mol Cell Cardiol 40:425-437
24. Nadal-Ginard B, Kajstura J, Leri A, Anversa P (2003) Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ Res 92:139-150 (Pubitemid 36254270)
25. Stupack DG, Cheresh DA (2002) Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 115:3729-3738 (Pubitemid 35203599)
26. Ross RS, Borg TK (2001) Integrins and the myocardium. Circ Res 88:1112-1119 (Pubitemid 34132510)
27. Communal C, Singh M, Menon B, Xie Z, Colucci WS, Singh K (2003) Beta1 integrins expression in adult rat ventricular myocytes and its role in the regulation of beta-adrenergic receptor-stimulated apoptosis. J Cell Biochem 89:381-388 (Pubitemid 36547272)
28. Menon B, Singh M, Ross RS, Johnson JN, Singh K (2006) beta-Adrenergic receptor-stimulated apoptosis in adult cardiac myocytes involves MMP-2-mediated disruption of beta1 integrin signaling and mitochondrial pathway. Am J Physiol Cell Physiol 290:C254-C261
29. Menon B, Singh M, Singh K (2005) Matrix metalloproteinases mediate beta-adrenergic receptor-stimulated apoptosis in adult rat ventricular myocytes. Am J Physiol Cell Physiol 289:C168-C176 (Pubitemid 40880837)
30. Yan M, Kuang X, Qiang W, Shen J, Claypool K, Lynn WS, Wong PK (2002) Prevention of thymic lymphoma development in ATM-/-mice by dexamethasone. Cancer Res 62:5153-5157 (Pubitemid 35024585)
31. Communal C, Colucci WS, Singh K (2000) p38 mitogen-activated protein kinase pathway protects adult rat ventricular myocytes against beta -adrenergic receptor-stimulated apoptosis. Evidence for Gi-dependent activation. J Biol Chem 275:19395-19400 (Pubitemid 30422915)
32. Hoit BD, Khoury SF, Kranias EG, Ball N, Walsh RA (1995) In vivo echocardiographic detection of enhanced left ventricular function in gene-targeted mice with phospholamban deficiency. Circ Res 77:632-637
33. Diwan A, Krenz M, Syed FM, Wansapura J, Ren X, Koesters AG, Li H, Kirshenbaum LA, Hahn HS, Robbins J, Jones WK, Dorn GW (2007) Inhibition of ischemic cardiomyocyte apoptosis through targeted ablation of Bnip3 restrains postinfarction remodeling in mice. J Clin Invest 117:2825-2833 (Pubitemid 47529613)
34. Galvez AS, Brunskill EW, Marreez Y, Benner BJ, Regula KM, Kirschenbaum LA, Dorn GW (2006) Distinct pathways regulate proapoptotic Nix and BNip3 in cardiac stress. J Biol Chem 281: 1442-1448
35. Hamacher-Brady A, Brady NR, Logue SE, Sayen MR, Jinno M, Kirshenbaum LA, Gottlieb RA, Gustafsson AB (2007) Response to myocardial ischemia/reperfusion injury involves Bnip3 and autophagy. Cell Death Differ 14:146-157 (Pubitemid 44911902)
36. Kubli DA, Quinsay MN, Huang C, Lee Y, Gustafsson AB (2008) Bnip3 functions as a mitochondrial sensor of oxidative stress during myocardial ischemia and reperfusion. Am J Physiol Heart Circ Physiol 295:H2025-H2031
37. Lozano G, Zambetti GP (2005) What have animal models taught us about the p53 pathway? J Pathol 205:206-220
38. Pusapati RV, Rounbehler RJ, Hong S, Powers JT, Yan M, Kiguchi K, McArthur MJ, Wong PK, Johnson DG (2006) ATM promotes apoptosis and suppresses tumorigenesis in response to Myc. Proc Natl Acad Sci USA 103:1446-1451 (Pubitemid 43191185)
39. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B, Reed JC (1994) Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805 (Pubitemid 24163411)
40. Krishnamurthy P, Subramanian V, Singh M, Singh K (2006) Deficiency of beta1 integrins results in increased myocardial dysfunction after myocardial infarction. Heart 92:1309-1315 (Pubitemid 44298891)
41. Goldsmith EC, Carver W, McFadden A, Goldsmith JG, Price RL, Sussman M, Lorell BH, Cooper G, Borg TK (2003) Integrin shedding as a mechanism of cellular adaptation during cardiac growth. Am J Physiol Heart Circ Physiol 284:H2227-H2234 (Pubitemid 36622435)
42. Li YY, McTiernan CF, Feldman AM (2000) Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiacmatrix remodeling. Cardiovasc Res 46:214-224 (Pubitemid 30204593)
43. Greene J, Wang M, Liu YE, Raymond LA, Rosen C, Shi YE (1996) Molecular cloning and characterization of human tissue inhibitor of metalloproteinase 4. J Biol Chem 271:30375-30380 (Pubitemid 26404039)
44. Halaby MJ, Hibma JC, He J, Yang DQ (2008) ATM protein kinase mediates full activation of Akt and regulates glucose transporter 4 translocation by insulin in muscle cells. Cell Signal 20:1555-1563
45. Schneider JG, Finck BN, Ren J, Standley KN, Takagi M, Maclean KH, Bernal-Mizrachi C, Muslin AJ, Kastan MB, Semenkovich CF (2006) ATM-dependent suppression of stress signaling reduces vascular disease in metabolic syndrome. Cell Metab 4:377-389 (Pubitemid 44645067)
46. Fukao T, Kaneko H, Birrell G, Gatei M, Tashita H, Yoshida T, Cross S, Kedar P, Watters D, Khana KK, Misko I, Kondo N, Lavin MF (1999) ATM is upregulated during the mitogenic response in peripheral blood mononuclear cells. Blood 94:1998-2006 (Pubitemid 29430416)
47. Fang ZM, Lee CS, Sarris M, Kearsley JH, Murrell D, Lavin MF, Keating K, Clarke RA (2001) Rapid radiation-induction of ATM protein levels in situ. Pathology 33:30-36 (Pubitemid 32222507)
48. Gueven N, Keating K, Fukao T, Loeffler H, Kondo N, Rodemann HP, Lavin MF (2003) Site-directed mutagenesis of the ATM promoter: consequences for response to proliferation and ionizing radiation. Genes Chromosomes Cancer 38:157-167 (Pubitemid 37093433)
49. Ghee M, Baker H, Miller JC, Ziff EB (1998) AP-1, CREB and CBP transcription factors differentially regulate the tyrosine hydroxylase gene. Brain Res Mol Brain Res 55:101-114
50. Communal C, Singh K, Pimentel DR, Colucci WS (1998) Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the beta-adrenergic pathway. Circulation 98:1329-1334 (Pubitemid 28443398)
51. Swynghedauw B (1999) Molecular mechanisms of myocardial remodeling. Physiol Rev 79:215-262
52. Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B (1997) A model for p53-induced apoptosis. Nature 389:300-305 (Pubitemid 27406646)
53. Shieh SY, Ikeda M, Taya Y, Prives C (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91:325-334 (Pubitemid 27467963)
54. Meulmeester E, Jochemsen AG (2008) p53: a guide to apoptosis. Curr Cancer Drug Targets 8:87-97 (Pubitemid 351347244)
55. Menon B, Krishnamurthy P, Kaverina E, Johnson JN, Ross RS, Singh M, Singh K (2006) Expression of the cytoplasmic domain of beta1 integrin induces apoptosis in adult rat ventricular myocytes (ARVM) via the involvement of caspase-8 and mitochondrial death pathway. Basic Res Cardiol 101:485-493 (Pubitemid 44637864)
56. Ahmed KM, Li JJ (2008) NF-kappa B-mediated adaptive resistance to ionizing radiation. Free Radic Biol Med 44:1-13
57. Bergman MR, Cheng S, Honbo N, Piacentini L, Karliner JS, Lovett DH (2003) A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers. Biochem J 369:485-496 (Pubitemid 36246232)
58. Xie Z, Singh M, Singh K (2004) Differential regulation of matrix metalloproteinase-2 and -9 expression and activity in adult rat cardiac fibroblasts in response to interleukin-1beta. J Biol Chem 279:39513-39519 (Pubitemid 39258218)
59. Roman J, Ritzenthaler JD, Boles B, Lois M, Roser-Page S (2004) Lipopolysaccharide induces expression of fibronectin alpha 5 beta 1-integrin receptors in human monocytic cells in a protein kinase C-dependent fashion. Am J Physiol Lung Cell Mol Physiol 287:L239-L249 (Pubitemid 38787671)
60. Weber KT, Sun Y, Tyagi SC, Cleutjens JP (1994) Collagen network of the myocardium: function, structural remodeling and regulatory mechanisms. J Mol Cell Cardiol 26:279-292 (Pubitemid 24199288)
61. Creemers EE, Cleutjens JP, Smits JF, Daemen MJ (2001) Matrix metalloproteinase inhibition after myocardial infarction: a new approach to prevent heart failure? Circ Res 89:201-210
62. Chancey AL, Brower GL, Peterson JT, Janicki JS (2002) Effects of matrix metalloproteinase inhibition on ventricular remodeling due to volume overload. Circulation 105:1983-1988 (Pubitemid 34437628)
63. Miura S, Ohno I, Suzuki J, Suzuki K, Okada S, Okuyama A, Nawata J, Ikeda J, Shirato K (2003) Inhibition of matrix metalloproteinases prevents cardiac hypertrophy induced by beta-adrenergic stimulation in rats. J Cardiovasc Pharmacol 42:174-181 (Pubitemid 36899668)
64. Villarreal FJ, Griffin M, Omens J, Dillmann W, Nguyen J, Covell J (2003) Early short-term treatment with doxycycline modulates postinfarction left ventricular remodeling. Circulation 108:1487-1492 (Pubitemid 37176456)
65. Hori Y, Kunihiro S, Sato S, Yoshioka K, Hara Y, Kanai K, Hoshi F, Itoh N, Higuchi S (2009) Doxycycline attenuates isoproterenol-induced myocardial fibrosis and matrix metalloproteinase activity in rats. Biol Pharm Bull 32:1678-1682
66. Bergman MR, Teerlink JR, Mahimkar R, Li L, Zhu BQ, Nguyen A, Dahi S, Karliner JS, Lovett DH (2007) Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction. Am J Physiol Heart Circ Physiol 292:H1847-H1860 (Pubitemid 46572408)
67. Weber KT (2004) From inflammation to fibrosis: a stiff stretch of highway. Hypertension 43:716-719
68. Shahbaz AU, Sun Y, Bhattacharya SK, Ahokas RA, Gerling IC, McGee JE, Weber KT (2010) Fibrosis in hypertensive heart disease: molecular pathways and cardioprotective strategies. J Hypertens 28(Suppl 1):S25-S32