Impact of myocardial inflammation on cytosolic and mitochondrial creatine kinase activity and expression

Basic Research in Cardiology

Volumn 104, Issue 3, 2009, Pages 247-257

  Ebermann, Linda ^a   Piper, Cornelia ^b   Kühl, Uwe ^b   Klingel, Karin ^c   Schlattner, Uwe ^d   Siafarikas, Nikias ^a   Zeichhardt, Heinz ^a   Schultheiss, Heinz Peter ^a   Dörner, Andrea ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

^c UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^d Domaine Universitaire   (France)

Author keywords

Coxsackievirus B3; Creatine kinase; Inflammatory heart disease

Indexed keywords

CATALASE; CREATINE KINASE; CYTOSOL RECEPTOR; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; COXSACKIE VIRUS B3; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE PREDISPOSITION; ENERGY METABOLISM; ENZYME ACTIVITY; FEMALE; HEART FUNCTION; HEART MUSCLE BIOPSY; HUMAN; HUMAN TISSUE; MACROPHAGE MIGRATION; MALE; MOUSE; MYOCARDITIS; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR DOWN REGULATION; VIRUS INFECTION; VIRUS REPLICATION;

ADULT; ANIMALS; BLOTTING, WESTERN; COXSACKIEVIRUS INFECTIONS; CREATINE KINASE, MB FORM; CREATINE KINASE, MITOCHONDRIAL FORM; CYTOPLASM; ENTEROVIRUS B, HUMAN; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; MICE; MIDDLE AGED; MYOCARDITIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 64949137030     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-008-0773-5     Document Type: Article

References (54)

1. Antoniak S, Boltzen U, Riad A, Kallwellis-Opara A, Rohde M, Dorner A, Tschope C, Noutsias M, Pauschinger M, Schultheiss HP, Rauch U (2008) Viral myocarditis and coagulopathy: Increased tissue factor expression and plasma thrombogenicity. J Mol Cell Cardiol 45:118-126
2. Beck MA, Handy J, Levander OA (2000) The role of oxidative stress in viral infections. Ann N Y Acad Sci 917:906-912
3. Bramos D, Ikonomidis I, Tsirikos N, Kottis G, Kostopoulou V, Pamboucas C, Papadopoulou E, Venetsanou K, Giatrakos N, Yang GZ, Nihoyannopoulos P, Toumanidis S (2008) The association of coronary flow changes and inflammatory indices to ischaemia-reperfusion microvascular damage and left ventricular remodelling. Basic Res Cardiol 103:345-55
4. Bryant D, Becker L, Richardson J, Shelton J, Franco F, Peshock R, Thompson M, Giroir B (1998) Cardiac failure in transgenic mice with myocardial expression of tumor necrosis factor-alpha. Circulation 97:1375-1381
5. Chau DH, Yuan J, Zhang H, Cheung P, Lim T, Liu Z, Sall A, Yang D (2007) Coxsackievirus B3 proteases 2A and 3C induce apoptotic cell death through mitochondrial injury and cleavage of eIF4GI but not DAP5/p97/ NAT1. Apoptosis 12:513-524
6. Dolder M, Walzel B, Speer O, Schlattner U, Wallimann T (2003) Inhibition of the mitochondrial permeability transition by creatine kinase substrates. Requirement for microcompartmentation. J Biol Chem 278:17760-17766
7. Dörge H, Schulz R, Belosjorow S, Post H, van de Sand A, Konietzka I, Frede S, Hartung T, Vinten-Johansen J, Youker KA, Entman ML, Erbel R, Heusch G (2002) Coronary microembolization: The role of TNF-alpha in contractile dysfunction. J Mol Cell Cardiol 34: 51-62
8. Dörner A, Kallwellis-Opara A, Pauschinger M, Kuhl U, Schultheiss HP (2005) Cardiac autoantibodies in viral myocarditis. Heart Fail Clin 1:333-343
9. Freeman GL, Colston JT, Zabalgoitia M, Chandrasekar B (1998) Contractile depression and expression of proinflammatory cytokines and iNOS in viral myocarditis. Am J Physiol 274:H249-H258
10. Gross WL, Bak MI, Ingwall JS, Arstall MA, Smith TW, Balligand JL, Kelly RA (1996) Nitric oxide inhibits creatine kinase and regulates rat heart contractile reserve. Proc Natl Acad Sci USA 93:5604-5609
11. Hiraoka Y, Kishimoto C, Kurokawa M, Ochiai H, Sasayama S (1992) Effects of polyethylene glycol conjugated superoxide dismutase on coxsackievirus B3 myocarditis in mice. Cardiovasc Res 26:956-961
12. Hiraoka Y, Kishimoto C, Takada H, Kurokawa M, Ochiai H, Shiraki K, Sasayama S (1993) Role of oxygen derived free radicals in the pathogenesis of coxsackievirus B3 myocarditis in mice. Cardiovasc Res 27:957-961
13. Ingwall JS, Weiss RG (2004) Is the failing heart energy starved? On using chemical energy to support cardiac function. Circ Res 95:135-145
14. Khatib R, Probert A, Reyes MP, Khatib G, Chason JL (1987) Mouse strain-related variation as a factor in the pathogenesis of coxsackievirus B3 murine myocarditis. J Gen Virol 68:2981-2988
15. Khuchua ZA, Vasiljeva EV, Clark JF, Korchazhkina OV, Branishte T, Kapelko VI, Kuznetsov AV, Ventura-Clapier R, Steinschneider AY, Lakomkin VL (1992) The creatine kinase system and cardiomyopathy. Am J Cardiovasc Pathol 4:223-234
16. Kishimoto C, Shioji K, Kinoshita M, Iwase T, Tamaki S, Fujii M, Murashige A, Maruhashi H, Takeda S, Nonogi H, Hashimoto T (2003) Treatment of acute inflammatory cardiomyopathy with intravenous immunoglobulin ameliorates left ventricular function associated with suppression of inflammatory cytokines and decreased oxidative stress. Int J Cardiol 91:173-178
17. Klingel K, Sauter M, Bock CT, Szalay G, Schnorr JJ, Kandolf R (2004) Molecular pathology of inflammatory cardiomyopathy. Med Microbiol Immunol 193:101-107
18. Koufen P, Ruck A, Brdiczka D, Wendt S, Wallimann T, Stark G (1999) Free radical-induced inactivation of creatine kinase: Influence on the octameric and dimeric states of the mitochondrial enzyme (Mib-CK). Biochem J 344:413-417
19. Kuhl U, Noutsias M, Seeberg B, Schultheiss HP (1996) Immunohistological evidence for a chronic intramyocardial inflammatory process in dilated cardiomyopathy. Heart 75:295-300
20. Kuhl U, Pauschinger M, Noutsias M, Seeberg B, Bock T, Lassner D, Poller W, Kandolf R, Schultheiss HP (2005) High prevalence of viral genomes and multiple viral infections in the myocardium of adults with "idiopathic" left ventricular dysfunction. Circulation 111: 887-893
21. Kuhl U, Pauschinger M, Seeberg B, Lassner D, Noutsias M, Poller W, Schultheiss HP (2005) Viral persistence in the myocardium is associated with progressive cardiac dysfunction. Circulation 112:1965-1970
22. Kyto V, Lapatto R, Lakkisto P, Saraste A, Voipio-Pulkki LM, Vuorinen T, Pulkki K (2004) Glutathione depletion and cardiomyocyte apoptosis in viral myocarditis. Eur J Clin Invest 34:167-175
23. Lane JR, Neumann DA, LaFond-Walker A, Herskowitz A, Rose NR (1993) Role of IL-1 and tumor necrosis factor in coxsackie virus-induced autoimmune myocarditis. J Immunol 151:1682-1690
24. Langen RC, Schols AM, Kelders MC, Wouters EF, Janssen-Heininger YM (2001) Inflammatory cytokines inhibit myogenic differentiation through activation of nuclear factor-kappaB. FASEB J 15:1169-1180
25. Martin U, Jarasch N, Nestler M, Rassmann A, Munder T, Seitz S, Zell R, Wutzler P, Henke A (2007) Antiviral effects of pan-caspase inhibitors on the replication of coxsackievirus B3. Apoptosis 12:525-533
26. Nascimben L, Ingwall JS, Pauletto P, Friedrich J, Gwathmey JK, Saks V, Pessina AC, Allen PD (1996) Creatine kinase system in failing and nonfailing human myocardium. Circulation 94:1894-1901
27. Neubauer S (2007) The failing heart-an engine out of fuel. N Engl J Med 356:1140-1151
28. Nose PS (1993) Cytokines and reperfusion injury. J Card Surg 8:305-308
29. Ozcan C, Bienengraeber M, Hodgson DM, Mann DL, Terzic A (2003) Mitochondrial tolerance to stress impaired in failing heart. J Mol Cell Cardiol 35:1161-1166
30. Pauschinger M, Rutschow S, Chandrasekharan K, Westermann D, Weitz A, Peter SL, Zeichhardt H, Poller W, Noutsias M, Li J, Schultheiss HP, Tschope C (2005) Carvedilol improves left ventricular function in murine coxsackievirus-induced acute myocarditis association with reduced myocardial interleukin-1beta and MMP-8 expression and a modulated immune response. Eur J Heart Fail 7:444-452
31. Qin W, Khuchua Z, Cheng J, Boero J, Payne RM, Strauss AW (1998) Molecular characterization of the creatine kinases and some historical perspectives. Mol Cell Biochem 184:153-167
32. Sakata Y, Chancey AL, Divakaran VG, Sekiguchi K, Sivasubramanian N, Mann DL (2008) Transforming growth factor-beta receptor antagonism attenuates myocardial fibrosis in mice with cardiac-restricted overexpression of tumor necrosis factor. Basic Res Cardiol 103:60-68
33. Saks V, Dzeja P, Schlattner U, Vendelin M, Terzic A, Wallimann T (2006) Cardiac system bioenergetics: Metabolic basis of the Frank-Starling law. J Physiol 571:253-273
34. Schlattner U, Mockli N, Speer O, Werner S, Wallimann T (2002) Creatine kinase and creatine transporter in normal, wounded, and diseased skin. J Invest Dermatol 118:416-423
35. Schlattner U, Tokarska-Schlattner M, Wallimann T (2006) Mitochondrial creatine kinase in human health and disease. Biochim Biophys Acta 1762:164-180
36. Schultheiss HP, Schulze K, Dorner A (1996) Significance of the adenine nucleotide translocator in the pathogenesis of viral heart disease. Mol Cell Biochem 163-164:319-327
37. Schulze K, Schultheiss HP (1995) The role of the ADP/ATP carrier in the pathogenesis of viral heart disease. Eur Heart J 160:64-67
38. Schulze K, Witzenbichler B, Christmann C, Schultheiss HP (1999) Disturbance of myocardial energy metabolism in experimental virus myocarditis by antibodies against the adenine nucleotide translocator. Cardiovasc Res 44:91-100
39. Shen W, Spindler M, Higgins MA, Jin N, Gill RM, Bloem LJ, Ryan TP, Ingwall JS (2005) The fall in creatine levels and creatine kinase isozyme changes in the failing heart are reversible: Complex post-transcriptional regulation of the components of the CK system. J Mol Cell Cardiol 39:537-544
40. Skyschally A, Gres P, Hoffmann S, Haude M, Erbel R, Schulz R, Heusch G. (2007) Bidirectional role of tumor necrosis factor-alpha in coronary microembolization: Progressive contractile dysfunction versus delayed protection against infarction. Circ Res 100:140-146
41. Smith A (1967) Preparation, properties and conditions for assay of mitochondria; slaughterhouse material, small scale. Methods Enzymol 10:81-86
42. Spindler M, Engelhardt S, Niebler R, Wagner H, Hein L, Lohse MJ, Neubauer S (2003) Alterations in the myocardial creatine kinase system precede the development of contractile dysfunction in beta(1)-adrenergic receptor transgenic mice. J Mol Cell Cardiol 35:389-397
43. Stachowiak O, Dolder M, Wallimann T, Richter C (1998) Mitochondrial creatine kinase is a prime target of peroxynitrite-induced modification and inactivation. J Biol Chem 273:16694-16699
44. Thielmann M, Dörge H, Martin C, Belosjorow S, Schwanke U, van de Sand A, Konietzka I, Büchert A, Krüger A, Schulz R, Heusch G (2002) Myocardial dysfunction with coronary microembolization: Signal transduction through a squence of nitric oxide, tumor necrosis factor-α, and sphingosine Circulation Research 90:807-813
45. Tokarska-Schlattner M, Zaugg M, Da SR, Lucchinetti E, Schaub MC, Wallimann T, Schlattner U (2005) Acute toxicity of doxorubicin on isolated perfused heart: Response of kinases regulating energy supply. Am J Physiol Heart Circ Physiol 289:H37-H47
46. Vendelin M, Lemba M, Saks VA (2004) Analysis of functional coupling: mitochondrial creatine kinase and adenine nucleotide translocase. Biophys J 87:696-713
47. Ventura-Clapier R, Garnier A, Veksler V (2004) Energy metabolism in heart failure. J Physiol 555:1-13
48. Vyssokikh MY, Brdiczka D (2003) The function of complexes between the outer mitochondrial membrane pore (VDAC) and the adenine nucleotide translocase in regulation of energy metabolism and apoptosis. Acta Biochim Pol 50:389-404
49. Vyssokikh M, Brdiczka D (2004) VDAC and peripheral channelling complexes in health and disease. Mol Cell Biochem 256-257:117-126
50. Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133-134:193-220
51. Wallimann T, Dolder M, Schlattner U, Eder M, Hornemann T, Kraft T, Stolz M (1998) Creatine kinase: An enzyme with a central role in cellular energy metabolism. MAGMA 6:116-119
52. Wolosker H, Panizzutti R, Engelender S (1996) Inhibition of creatine kinase by S-nitrosoglutathione. FEBS Lett 392: 274-276
53. Zhang C (2008) The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol 103:398-406
54. Zhang HM, Yanagawa B, Cheung P, Luo H, Yuan J, Chau D, Wang A, Bohunek L, Wilson JE, McManus BM, Yang D (2002) Nip21 gene expression reduces coxsackievirus B3 replication by promoting apoptotic cell death via a mitochondria-dependent pathway. Circ Res 90:1251-1258