Inhibition of the cardiomyocyte-specific kinase TNNI3K limits oxidative stress, injury, and adverse remodeling in the ischemic heart

Science Translational Medicine

Volumn 5, Issue 207, 2013, Pages

  Vagnozzi, Ronald J ^a,b   Gatto Jr , Gregory J ^c   Kallander, Lara S ^c   Hoffman, Nicholas E ^b   Mallilankaraman, Karthik ^b   Ballard, Victoria L T ^c   Lawhorn, Brian G ^c   Stoy, Patrick ^c   Philp, Joanne ^c   Graves, Alan P ^c   Naito, Yoshiro ^d   Lepore, John J ^c   Gao, Erhe ^b   Madesh, Muniswamy ^b   Force, Thomas ^b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GLAXOSMITHKLINE   (United States)

^d HYOGO COLLEGE OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; GSK 329; GSK 854; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TROPONIN I INTERACTING KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SYNTHESIS; HEART FUNCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FAILURE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REPERFUSION INJURY;

ACUTE CORONARY SYNDROME; ANIMALS; CELL DEATH; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; ENZYME ACTIVATION; GENE DELETION; HEART FAILURE; HUMANS; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; SMALL MOLECULE LIBRARIES; SUPEROXIDES; UP-REGULATION; VENTRICULAR DYSFUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 84886416217     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006479     Document Type: Article

References (30)

1. D. J. Hausenloy, D. M. Yellon, Myocardial ischemia-reperfusion injury: A neglected therapeutic target. J. Clin. Invest. 123, 92-100 (2013).
2. D. M. Yellon, D. J. Hausenloy, Myocardial reperfusion injury. N. Engl. J. Med. 357, 1121-1135 (2007).
3. A. T. Turer, J. A. Hill, Pathogenesis of myocardial ischemia-reperfusion injury and rationale for therapy. Am. J. Cardiol. 106, 360-368 (2010).
4. E. Murphy, C. Steenbergen, Mechanisms underlying acute protection from cardiac ischemiareperfusion injury. Physiol. Rev. 88, 581-609 (2008).
5. C. P. Baines, How and when do myocytes die during ischemia and reperfusion: The late phase. J. Cardiovasc. Pharmacol. Ther. 16, 239-243 (2011).
6. Y. Zhao, X. M. Meng, Y. J. Wei, X. W. Zhao, D. Q. Liu, H. Q. Cao, C. C. Liew, J. F. Ding, Cloning and characterization of a novel cardiac-specific kinase that interacts specifically with cardiac troponin I. J. Mol. Med. 81, 297-304 (2003).
7. Y. Feng, H. Q. Cao, Z. Liu, J. F. Ding, X. M. Meng, Identification of the dual specificity and the functional domains of the cardiac-specific protein kinase TNNI3K. Gen. Physiol. Biophys. 26, 104-109 (2007).
8. L. Wang, H. Wang, J. Ye, R. X. Xu, L. Song, N. Shi, Y. W. Zhang, X. Chen, X. M. Meng, Adenovirus-mediated overexpression of cardiac troponin I-interacting kinase promotes cardiomyocyte hypertrophy. Clin. Exp. Pharmacol. Physiol. 38, 278-284 (2011).
9. F. C. Wheeler, H. Tang, O. A. Marks, T. N. Hadnott, P. L. Chu, L. Mao, H. A. Rockman, D. A. Marchuk, Tnni3k modifies disease progression in murine models of cardiomyopathy. PLoS Genet. 5, e1000647 (2009).
10. H. Tang, K. Xiao, L. Mao, H. A. Rockman, D. A. Marchuk, Overexpression of TNNI3K, a cardiac-specific MAPKKK, promotes cardiac dysfunction. J. Mol. Cell. Cardiol. 54, 101-111 (2013).
11. X. Wang, J. Wang, M. Su, C. Wang, J. Chen, H. Wang, L. Song, Y. Zou, L. Zhang, Y. Zhang, R. Hui, TNNI3K, a cardiac-specific kinase, promotes physiological cardiac hypertrophy in transgenic mice. PLoS One 8, e58570 (2013).
12. Z. F. Lai, Y. Z. Chen, L. P. Feng, X. M. Meng, J. F. Ding, L. Y. Wang, J. Ye, P. Li, X. S. Cheng, Y. Kitamoto, K. Monzen, I. Komuro, N. Sakaguchi, S. Kim-Mitsuyama, Overexpression of TNNI3K, a cardiac-specific MAP kinase, promotes P19CL6-derived cardiac myogenesis and prevents myocardial infarction-induced injury. Am. J. Physiol. Heart Circ. Physiol. 295, H708-H716 (2008).
13. E. Gao, Y. H. Lei, X. Shang, Z. M. Huang, L. Zuo, M. Boucher, Q. Fan, J. K. Chuprun, X. L. Ma, W. J. Koch, A novel and efficient model of coronary artery ligation and myocardial infarction in the mouse. Circ. Res. 107, 1445-1453 (2010).
14. D. J. Lefer, D. N. Granger, Oxidative stress and cardiac disease. Am. J. Med. 109, 315-323 (2000).
15. L. B. Becker, New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc. Res. 61, 461-470 (2004).
16. Z. Cheng, X. Jiang, W. D. Kruger, D. Praticò, S. Gupta, K. Mallilankaraman, M. Madesh, A. I. Schafer, W. Durante, X. Yang, H. Wang, Hyperhomocysteinemia impairs endothelium-derived hyperpolarizing factor-mediated vasorelaxation in transgenic cystathionine β synthase-deficient mice. Blood 118, 1998-2006 (2011).
17. T. L. Vanden Hoek, C. Li, Z. Shao, P. T. Schumacker, L. B. Becker, Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J. Mol. Cell. Cardiol. 29, 2571-2583 (1997).
18. J. N. Weiss, P. Korge, H. M. Honda, P. Ping, Role of the mitochondrial permeability transition in myocardial disease. Circ. Res. 93, 292-301 (2003).
19. C. P. Baines, The mitochondrial permeability transition pore and ischemia-reperfusion injury. Basic Res. Cardiol. 104, 181-188 (2009).
20. D. G. Johns, Z. Ao, R. N. Willette, C. H. Macphee, S. A. Douglas, Role of p38 MAP kinase in postcapillary venule leukocyte adhesion induced by ischemia/reperfusion injury. Pharmacol. Res. 51, 463-471 (2005).
21. T. M. Behr, S. S. Nerurkar, A. H. Nelson, R. W. Coatney, T. N. Woods, A. Sulpizio, S. Chandra, D. P. Brooks, S. Kumar, J. C. Lee, E. H. Ohlstein, C. E. Angermann, J. L. Adams, J. Sisko, J. D. Sackner-Bernstein, R. N. Willette, Hypertensive end-organ damage and premature mortality are p38 mitogen-activated protein kinase-dependent in a ratmodel of cardiac hypertrophy and dysfunction. Circulation 104, 1292-1298 (2001).
22. Z. Shao, K. Bhattacharya, E. Hsich, L. Park, B. Walters, U. Germann, Y. M. Wang, J. Kyriakis, R. Mohanlal, K. Kuida, M. Namchuk, F. Salituro, Y. M. Yao, W. M. Hou, X. Chen, M. Aronovitz, P. N. Tsichlis, S. Bhattacharya, T. Force, H. Kilter, c-Jun N-terminal kinases mediate reactivation of Akt and cardiomyocyte survival after hypoxic injury in vitro and in vivo. Circ. Res. 98, 111-118 (2006).
23. N. Koitabashi, D. Bedja, A. L. Zaiman, Y. M. Pinto, M. Zhang, K. L. Gabrielson, E. Takimoto, D. A. Kass, Avoidance of transient cardiomyopathy in cardiomyocyte-targeted tamoxifen-induced MerCreMer gene deletion models. Circ. Res. 105, 12-15 (2009).
24. L. Schwartz Longacre, R. A. Kloner, A. E. Arai, C. P. Baines, R. Bolli, E. Braunwald, J. Downey, R. J. Gibbons, R. A. Gottlieb, G. Heusch, R. B. Jennings, D. J. Lefer, R. M. Mentzer, E. Murphy, M. Ovize, P. Ping, K. Przyklenk, M. N. Sack, R. S. Vander Heide, J. Vinten-Johansen, D. M. Yellon; National Heart, Lung, and Blood Institute, National Institutes of Health, New horizons in cardioprotection: Recommendations from the 2010 National Heart, Lung, and Blood Institute Workshop. Circulation 124, 1172-1179 (2011).
25. B. A. Rose, T. Force, Y. Wang, Mitogen-activated protein kinase signaling in the heart: Angels versus demons in a heart-breaking tale. Physiol. Rev. 90, 1507-1546 (2010).
26. A. Clerk, S. J. Fuller, A. Michael, P. H. Sugden, Stimulation of "stress-regulated " mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J. Biol. Chem. 273, 7228-7234 (1998).
27. A. Kulisz, N. Chen, N. S. Chandel, Z. Shao, P. T. Schumacker, Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes. Am. J. Physiol. Lung Cell Mol. Physiol. 282, L1324-L1329 (2002).
28. E. Denise Martin, G. F. De Nicola, M. S. Marber, New therapeutic targets in cardiology: p38 α mitogen-activated protein kinase for ischemic heart disease. Circulation 126, 357-368 (2012).
29. M. S. Marber, J. D. Molkentin, T. Force, Developing small molecules to inhibit kinases unkind to the heart: p38 MAPK as a case in point. Drug Discov. Today Dis. Mech. 7, e123-e127 (2010).
30. S. R. Houser, K. B. Margulies, A. M. Murphy, F. G. Spinale, G. S. Francis, S. D. Prabhu, H. A. Rockman, D. A. Kass, J. D. Molkentin, M. A. Sussman, W. J. Koch; American Heart Association Council on Basic Cardiovascular Sciences, Council on Clinical Cardiology, and Council on Functional Genomics and Translational Biology, Animal models of heart failure: A scientific statement from the American Heart Association. Circ. Res. 111, 131-150 (2012).