Ischemia induced peroxynitrite dependent modifications of cardiomyocyte MLC1 increases its degradation by MMP-2 leading to contractile dysfunction

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 5, 2011, Pages 1136-1147

  Polewicz, Dorota ^a   Cadete, Virgilio J J ^a   Doroszko, Adrian ^a,d   Hunter, Beth E ^b   Sawicka, Jolanta ^a   Szczesna Cordary, Danuta ^c   Light, Peter E ^b   Sawicki, Grzegorz ^a,d  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d WROCLAW MEDICAL UNIVERSITY   (Poland)

Author keywords

Cardiomyocytes; Ischemia; MLC1; MMP 2; Nitration; Nitrosylation; Nitrotyrosine; Peroxynitrite

Indexed keywords

GELATINASE A; MEMBRANE PROTEIN; MLC1 PROTEIN, HUMAN; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN I; PEROXYNITROUS ACID; REACTIVE OXYGEN METABOLITE;

ANIMAL; ARTICLE; DRUG ANTAGONISM; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; METABOLISM; PATHOPHYSIOLOGY; RAT; REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

ANIMALS; HUMANS; MATRIX METALLOPROTEINASE 2; MEMBRANE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; MYOSIN LIGHT CHAINS; PEROXYNITROUS ACID; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES;

RATTUS;

EID: 79957598460     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01094.x     Document Type: Article

References (41)

1. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007; 357: 1121-35.
2. Yasmin W, Strynadka KD, Schulz R. Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc Res. 1997; 33: 422-32.
3. Zweier JL, Wang P, Kuppusamy P. Direct measurement of nitric oxide generation in the ischemic heart using electron paramagnetic resonance spectroscopy. J Biol Chem. 1995; 270: 304-7.
4. Yao Z, Tong J, Tan X, et al Role of reactive oxygen species in acetylcholine-induced preconditioning in cardiomyocytes. Am J Physiol. 1999; 277: H2504-9.
5. Schulz R, Wambolt R. Inhibition of nitric oxide synthesis protects the isolated working rabbit heart from ischaemia-reperfusion injury. Cardiovasc Res. 1995; 30: 432-9.
6. Lopez BL, Liu GL, Christopher TA, et al Peroxynitrite, the product of nitric oxide and superoxide, causes myocardial injury in the isolated perfused rat heart. Coron Artery Dis. 1997; 8: 149-53.
7. Ferdinandy P, Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br J Pharmacol. 2003; 138: 532-43.
8. Jugdutt BI. Nitric oxide and cardioprotection during ischemia-reperfusion. Heart Fail Rev. 2002; 7: 391-405.
9. Schulz R, Dodge KL, Lopaschuk GD, et al Peroxynitrite impairs cardiac contractile function by decreasing cardiac efficiency. Am J Physiol. 1997; 272: H1212-9.
10. Digerness SB, Harris KD, Kirklin JW, et al Peroxynitrite irreversibly decreases diastolic and systolic function in cardiac muscle. Free Radic Biol Med. 1999; 27: 1386-92.
11. Vescovo G, Ravara B, Dalla Libera L. Skeletal muscle myofibrillar protein oxidation and exercise capacity in heart failure. Basic Res Cardiol. 2008; 103: 285-90.
12. Hess DT, Matsumoto A, Kim SO, et al Protein S-nitrosylation: purview and parameters. Nature reviews. 2005; 6: 150-66.
13. Kanski J, Behring A, Pelling J, et al Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging. Am J Physiol. 2005; 288: H371-81.
14. Hong SJ, Gokulrangan G, Schoneich C. Proteomic analysis of age dependent nitration of rat cardiac proteins by solution isoelectric focusing coupled to nanoHPLC tandem mass spectrometry. Exp Gerontol. 2007; 42: 639-51.
15. Snook JH, Li J, Helmke BP, et al Peroxynitrite inhibits myofibrillar protein function in anin vitroassay of motility. Free Radic Biol Med. 2008; 44: 14-23.
16. Van Eyk JE, Powers F, Law W, et al Breakdown and release of myofilament proteins during ischemia and ischemia/reperfusion in rat hearts: identification of degradation products and effects on the pCa-force relation. Circ Res. 1998; 82: 261-71.
17. Kanski J, Hong SJ, Schoneich C. Proteomic analysis of protein nitration in aging skeletal muscle and identification of nitrotyrosine-containing sequencesin vivoby nanoelectrospray ionization tandem mass spectrometry. J Biol Chem. 2005; 280: 24261-6.
18. Sawicki G, Leon H, Sawicka J, et al Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation. 2005; 112: 544-52.
19. Doroszko A, Polewicz D, Sawicka J, et al Cardiac dysfunction in an animal model of neonatal asphyxia is associated with increased degradation of MLC1 by MMP-2. Basic Res Cardiol. 2009; 104: 669-79.
20. Wang W, Schulze CJ, Suarez-Pinzon WL, et al Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation. 2002; 106: 1543-9.
21. Wang W, Sawicki G, Schulz R. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc Res. 2002; 53: 165-74.
22. Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev. 2007; 87: 1285-342.
23. Chow AK, Cena J, Schulz R. Acute actions and novel targets of matrix metalloproteinases in the heart and vasculature. Br J Pharmacol. 2007; 152: 189-205.
24. Schulz R. Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches. Annu Rev Pharmacol Toxicol. 2007; 47: 211-42.
25. Gallagher G, Menzie S, Huang Y, et al Regional cardiac dysfunction is associated with specific alterations in inflammatory cytokines and matrix metalloproteinases after acute myocardial infarction in sheep. Basic Res Cardiol. 2007; 102: 63-72.
26. Light P, Shimoni Y, Harbison S, et al Hypothyroidism decreases the ATP sensitivity of KATP channels from rat heart. J Membr Biol. 1998; 162: 217-23.
27. Bouchard RA, Clark RB, Giles WR. Role of sodium-calcium exchange in activation of contraction in rat ventricle. J Physiol. 1993; 472: 391-413.
28. Watanabe T, Delbridge LM, Bustamante JO, et al Heterogeneity of the action potential in isolated rat ventricular myocytes and tissue. Circ Res. 1983; 52: 280-90.
29. Diaz RJ, Wilson GJ. Studying ischemic preconditioning in isolated cardiomyocyte models. Cardiovasc Res. 2006; 70: 286-96.
30. Diaz RJ, Zobel C, Cho HC, et al Selective inhibition of inward rectifier K+ channels (Kir2.1 or Kir2.2) abolishes protection by ischemic preconditioning in rabbit ventricular cardiomyocytes. Circ Res. 2004; 95: 325-32.
31. Diaz RJ, Losito VA, Mao GD, et al Chloride channel inhibition blocks the protection of ischemic preconditioning and hypo-osmotic stress in rabbit ventricular myocardium. Circ Res. 1999; 84: 763-75.
32. Ferdinandy P, Danial H, Ambrus I, et al Peroxynitrite is a major contributor to cytokine-induced myocardial contractile failure. Circ Res. 2000; 87: 241-7.
33. Sawicki G, Jugdutt BI. Detection of regional changes in protein levels in thein vivocanine model of acute heart failure following ischemia-reperfusion injury: functional proteomics studies. Proteomics. 2004; 4: 2195-202.
34. Sawicki G, Dakour J, Morrish DW. Functional proteomics of neurokinin B in the placenta indicates a novel role in regulating cytotrophoblast antioxidant defences. Proteomics. 2003; 3: 2044-51.
35. Perkins DN, Pappin DJ, Creasy DM, et al Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 1999; 20: 3551-67.
36. Cheung PY, Sawicki G, Wozniak M, et al Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation. 2000; 101: 1833-9.
37. Zhang WZ, Lang C, Kaye DM. Determination of plasma free 3-nitrotyrosine and tyrosine by reversed-phase liquid chromatography with 4-fluoro-7-nitrobenzofurazan derivatization. Biomed Chromatogr. 2007; 21: 273-8.
38. Mathews CE, Suarez-Pinzon WL, Baust JJ, et al Mechanisms underlying resistance of pancreatic islets from ALR/Lt mice to cytokine-induced destruction. J Immunol. 2005; 175: 1248-56.
39. Hensley K, Maidt ML, Pye QN et al Quantitation of protein-bound 3-nitrotyrosine and 3, 4-dihydroxyphenylalanine by high-performance liquid chromatography with electrochemical array detection. Anal Biochem. 1997; 251: 187-95.
40. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227: 680-5.
41. Fert-Bober J, Basran RS, Sawicka J, et al Effect of duration of ischemia on myocardial proteome in ischemia/reperfusion injury. Proteomics. 2008; 8: 2543-55.