Synergistic protection of MLC 1 against cardiac ischemia/reperfusion-induced degradation: a novel therapeutic concept for the future

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References

• 1  Antman EM, Anbe DT, Armstrong PW et al. ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Revise the 1999 Guidelines for the Management of Patients with Acute Myocardial Infarction). Circulation110(9),e82–e292 (2004).
  MedlineGoogle Scholar
• 2  Cadete VJ, Sawicka J, Jaswal JS et al. Ischemia/reperfusion-induced myosin light chain 1 phosphorylation increases its degradation by matrix metalloproteinase 2. FEBS J.279(13),2444–2454 (2012).▪▪ First report demonstrating phosphorylation of MLC1 increase its degradation by MMP-2.
  Medline CASGoogle Scholar
• 3  Doroszko A, Polewicz D, Cadete VJ et al. Neonatal asphyxia induces the nitration of cardiac myosin light chain 2 that is associated with cardiac systolic dysfunction. Shock34(6),592–600 (2010).▪ First evidence that MLC2 can be degraded by MMP-2.
  Medline CASGoogle Scholar
• 4  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.104(6),669–679 (2009).▪ First indication of possible regulatory role of MLC1 levels in physiological conditions.
  Medline CASGoogle Scholar
• 5  Arrell DK, Neverova I, Fraser H, Marban E, Van Eyk JE. Proteomic analysis of pharmacologically preconditioned cardiomyocytes reveals novel phosphorylation of myosin light chain 1. Circ. Res.89(6),480–487 (2001).
  Medline CASGoogle Scholar
• 6  Nilsson L, Hallen J, Atar D, Jonasson L, Swahn E. Early measurements of plasma matrix metalloproteinase-2 predict infarct size and ventricular dysfunction in ST-elevation myocardial infarction. Heart98(1),31–36 (2012).
  Medline CASGoogle Scholar
• 7  Moore PB, Huxley HE, Derosier DJ. Three-dimensional reconstruction of F-actin, thin filaments and decorated thin filaments. J. Mol. Biol.50(2),279–295 (1970).
  Medline CASGoogle Scholar
• 8  Taylor EW. Molecular muscle. Science261(5117),35–36 (1993).
  Medline CASGoogle Scholar
• 9  Margossian SS, Lowey S. Substructure of the myosin molecule. IV. Interactions of myosin and its subfragments with adenosine triphosphate and F-actin. J. Mol. Biol.74(3),313–330 (1973).
  Medline CASGoogle Scholar
• 10  Rayment I, Holden HM, Whittaker M et al. Structure of the actin-myosin complex and its implications for muscle contraction. Science261(5117),58–65 (1993).
  Medline CASGoogle Scholar
• 11  Huxley AF, Niedergerke R. Structural changes in muscle during contraction; interference microscopy of living muscle fibers. Nature173(4412),971–973 (1954).
  Medline CASGoogle Scholar
• 12  Holmes KC, Geeves MA. The structural basis of muscle contraction. Philos. Trans. R. Soc. Lond. B Biol. Sci.355(1396),419–431 (2000).
  Medline CASGoogle Scholar
• 13  Margossian SS, Lowey S. Substructure of the myosin molecule. 3. Preparation of single-headed derivatives of myosin. J. Mol. Biol.74(3),301–311 (1973).
  Medline CASGoogle Scholar
• 14  Mornet D, Pantel P, Audemard E, Kassab R. The limited tryptic cleavage of chymotryptic S-1: an approach to the characterization of the actin site in myosin heads. Biochem. Biophys. Res. Commun.89(3),925–932 (1979).
  Medline CASGoogle Scholar
• 15  Rayment I, Rypniewski WR, Schmidt-Base K et al. Three-dimensional structure of myosin subfragment-1: a molecular motor. Science261(5117),50–58 (1993).
  Medline CASGoogle Scholar
• 16  Tonomura Y, Oosawa F. Molecular mechanism of contraction. Annu. Rev. Biophys. Bioeng.1,159–190 (1972).
  Medline CASGoogle Scholar
• 17  White MY, Cordwell SJ, Mccarron HC et al. Proteomics of ischemia/reperfusion injury in rabbit myocardium reveals alterations to proteins of essential functional systems. Proteomics5(5),1395–1410 (2005).
  Medline CASGoogle Scholar
• 18  Polewicz D, Cadete VJ, Doroszko A et al. Ischemia induced peroxynitrite dependent modifications of cardiomyocyte MLC1 increases its degradation by MMP-2 leading to contractile dysfunction. J. Cell. Mol. Med.15(5),1136–1147 (2011).▪ First report of intracellular action of MMP-2 using isolated cardiac myocytes. Reactive oxygen species dependent modifications of MLC1 increases its degradation by MMP-2.
  Medline CASGoogle Scholar
• 19  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. Circulation112(4),544–552 (2005).▪ First report of increased degradation of myocardial MLC1 by MMP-2 in ischemia reperfusion hearts
  Medline CASGoogle Scholar
• 20  Holmes KC. Muscle proteins-their actions and interactions. Curr. Opin. Struct. Biol.6(6),781–789 (1996).
  Medline CASGoogle Scholar
• 21  Ebashi S, Kodama A. A new protein factor promoting aggregation of tropomyosin. J. Biochem.58(1),107–108 (1965).
  Medline CASGoogle Scholar
• 22  Murakami K, Yumoto F, Ohki SY et al. Structural basis for calcium-regulated relaxation of striated muscles at interaction sites of troponin with actin and tropomyosin. Adv. Exp. Med. Biol.592,71–86 (2007).
  MedlineGoogle Scholar
• 23  Greaser ML, Gergely J. Reconstitution of troponin activity from three protein components. J. Biol. Chem.246(13),4226–4233 (1971).
  Medline CASGoogle Scholar
• 24  Boussouf SE, Geeves MA. Tropomyosin and troponin cooperativity on the thin filament. Adv. Exp. Med. Biol.592,99–109 (2007).
  MedlineGoogle Scholar
• 25  Scruggs SB, Walker LA, Lyu T et al. Partial replacement of cardiac troponin I with a non-phosphorylatable mutant at serines 43/45 attenuates the contractile dysfunction associated with PKCepsilon phosphorylation. J. Mol. Cell. Cardiol.40(4),465–473 (2006).
  Medline CASGoogle Scholar
• 26  Gao CQ, Sawicki G, Suarez-Pinzon WL et al. Matrix metalloproteinase-2 mediates cytokine-induced myocardial contractile dysfunction. Cardiovasc. Res.57(2),426–433 (2003).
  Medline CASGoogle Scholar
• 27  Wang W, Schulze CJ, Suarez-Pinzon WL et al. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation106(12),1543–1549 (2002).
  Medline CASGoogle Scholar
• 28  Gomes AV, Potter JD. Cellular and molecular aspects of familial hypertrophic cardiomyopathy caused by mutations in the cardiac troponin I gene. Mol. Cell. Biochem.263(1–2),99–114 (2004).
  Medline CASGoogle Scholar
• 29  Granzier HL, Labeit S. The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ. Res.94(3),284–295 (2004).
  Medline CASGoogle Scholar
• 30  Gregorio CC, Granzier H, Sorimachi H, Labeit S. Muscle assembly: a titanic achievement? Curr. Opin. Cell Biol.11(1),18–25 (1999).
  Medline CASGoogle Scholar
• 31  Fukuda N, Granzier HL, Ishiwata S, Kurihara S. Physiological functions of the giant elastic protein titin in mammalian striated muscle. J. Physiol. Sci.58(3),151–159 (2008).
  Medline CASGoogle Scholar
• 32  Stansfield WE, Moss NC, Willis MS, Tang R, Selzman CH. Proteasome inhibition attenuates infarct size and preserves cardiac function in a murine model of myocardial ischemia-reperfusion injury. Ann. Thorac. Surg.84(1),120–125 (2007).
  MedlineGoogle Scholar
• 33  Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol. Rev.79(2),609–634 (1999).
  Medline CASGoogle Scholar
• 34  Ali MA, Cho WJ, Hudson B et al. Titin is a target of matrix metalloproteinase-2: implications in myocardial ischemia/reperfusion injury. Circulation122(20),2039–2047 (2010).
  Medline CASGoogle Scholar
• 35  Wong HY, Tan JY, Lim CC. Abnormal liver function tests in the symptomatic pregnant patient: the local experience in Singapore. Ann. Acad. Med. Singap.33(2),204–208 (2004).
  Medline CASGoogle Scholar
• 36  Tinsley JH, Hunter FA, Childs EW. PKC and MLCK-dependent, cytokine-induced rat coronary endothelial dysfunction. J. Surg. Res.152(1),76–83 (2009).
  Medline CASGoogle Scholar
• 37  Gao Y, Ye LH, Kishi H et al. Myosin light chain kinase as a multifunctional regulatory protein of smooth muscle contraction. IUBMB Life51(6),337–344 (2001).
  Medline CASGoogle Scholar
• 38  Liu X, Shao Q, Dhalla NS. Myosin light chain phosphorylation in cardiac hypertrophy and failure due to myocardial infarction. J. Mol. Cell. Cardiol.27(12),2613–2621 (1995).
  Medline CASGoogle Scholar
• 39  Yuan SY, Wu MH, Ustinova EE et al. Myosin light chain phosphorylation in neutrophil-stimulated coronary microvascular leakage. Circ. Res.90(11),1214–1221 (2002).
  Medline CASGoogle Scholar
• 40  Lin HB, Cadete VJ, Sawicka J, Wozniak M, Sawicki G. Effect of the myosin light chain kinase inhibitor ML-7 on the proteome of hearts subjected to ischemia-reperfusion injury. J. Proteomics75(17),5386–5395 (2012).
  Medline CASGoogle Scholar
• 41  Nakanishi S, Yamada K, Kase H, Nakamura S, Nonomura Y. K-252a, a novel microbial product, inhibits smooth muscle myosin light chain kinase. J. Biol. Chem.263(13),6215–6219 (1988).
  Medline CASGoogle Scholar
• 42  Kelley SJ, Thomas R, Dunham PB. Candidate inhibitor of the volume-sensitive kinase regulating K-Cl cotransport: the myosin light chain kinase inhibitor ML-7. J. Membr. Biol.178(1),31–41 (2000).
  Medline CASGoogle Scholar
• 43  Isemura M, Mita T, Satoh K, Narumi K, Motomiya M. Myosin light chain kinase inhibitors ML-7 and ML-9 inhibit mouse lung carcinoma cell attachment to the fibronectin substratum. Cell Biol. Int. Rep.15(10),965–972 (1991).
  Medline CASGoogle Scholar
• 44  Deng M, Williams CJ, Schultz RM. Role of MAP kinase and myosin light chain kinase in chromosome-induced development of mouse egg polarity. Dev. Biol.278(2),358–366 (2005).
  Medline CASGoogle Scholar
• 45  Luh C, Kuhlmann CR, Ackermann B et al. Inhibition of myosin light chain kinase reduces brain edema formation after traumatic brain injury. J. Neurochem.112(4),1015–1025 (2010).
  Medline CASGoogle Scholar
• 46  Rosenthal R, Choritz L, Schlott S et al. Effects of ML-7 and Y-27632 on carbachol- and endothelin-1-induced contraction of bovine trabecular meshwork. Exp. Eye Res.80(6),837–845 (2005).
  Medline CASGoogle Scholar
• 47  Nagase H, Woessner JF Jr. Matrix metalloproteinases. J. Biol. Chem.274(31),21491–21494 (1999).
  Medline CASGoogle Scholar
• 48  Salo T, Makela M, Kylmaniemi M, Autio-Harmainen H, Larjava H. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab Invest.70(2),176–182 (1994).
  Medline CASGoogle Scholar
• 49  Mosig RA, Dowling O, Difeo A et al. Loss of MMP-2 disrupts skeletal and craniofacial development and results in decreased bone mineralization, joint erosion and defects in osteoblast and osteoclast growth. Hum. Mol. Genet.16(9),1113–1123 (2007).
  Medline CASGoogle Scholar
• 50  Stetler-Stevenson WG. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J. Clin. Invest.103(9),1237–1241 (1999).
  Medline CASGoogle Scholar
• 51  Chang YH, Lin IL, Tsay GJ et al. Elevated circulatory MMP-2 and MMP-9 levels and activities in patients with rheumatoid arthritis and systemic lupus erythematosus. Clin. Biochem.41(12),955–959 (2008).
  Medline CASGoogle Scholar
• 52  Benesova Y, Vasku A, Novotna H et al. Matrix metalloproteinase-9 and matrix metalloproteinase-2 as biomarkers of various courses in multiple sclerosis. Mult. Scler.15(3),316–322 (2009).
  Medline CASGoogle Scholar
• 53  Gokaslan ZL, Chintala SK, York JE et al. Expression and role of matrix metalloproteinases MMP-2 and MMP-9 in human spinal column tumors. Clin. Exp. Metastasis16(8),721–728 (1998).
  Medline CASGoogle Scholar
• 54  Creemers EE, Cleutjens JP, Smits JF, Daemen MJ. Matrix metalloproteinase inhibition after myocardial infarction: a new approach to prevent heart failure? Circ. Res.89(3),201–210 (2001).
  Medline CASGoogle Scholar
• 55  Dollery CM, Mcewan JR, Henney AM. Matrix metalloproteinases and cardiovascular disease. Circ. Res.77(5),863–868 (1995).
  Medline CASGoogle Scholar
• 56  Spinale FG, Coker ML, Bond BR, Zellner JL. Myocardial matrix degradation and metalloproteinase activation in the failing heart: a potential therapeutic target. Cardiovasc. Res.46(2),225–238 (2000).
  Medline CASGoogle Scholar
• 57  Lee RT. Matrix metalloproteinase inhibition and the prevention of heart failure. Trends Cardiovasc. Med.11(5),202–205 (2001).
  Medline CASGoogle Scholar
• 58  Cauwe B, Opdenakker G. Intracellular substrate cleavage: a novel dimension in the biochemistry, biology and pathology of matrix metalloproteinases. Crit. Rev. Biochem. Mol. Biol.45(5),351–423 (2010).
  Medline CASGoogle Scholar
• 59  Sung MM, Schulz CG, Wang W et al. Matrix metalloproteinase-2 degrades the cytoskeletal protein alpha-actinin in peroxynitrite mediated myocardial injury. J. Mol. Cell. Cardiol.43(4),429–436 (2007).
  Medline CASGoogle Scholar
• 60  Corbel M, Boichot E, Lagente V. Role of gelatinases MMP-2 and MMP-9 in tissue remodeling following acute lung injury. Braz J. Med. Biol. Res.33(7),749–754 (2000).
  Medline CASGoogle Scholar
• 61  Han B, Zhao X, Huang X, Xie L. Vaporized perfluorocarbon confers protection against acute lung injury by inhibiting MMP-9 expression without protective effects in other organs. J. Int. Med. Res.40(1),115–125 (2012).
  Medline CASGoogle Scholar
• 62  Doroszko A, Hurst TS, Polewicz D et al. Effects of MMP-9 inhibition by doxycycline on proteome of lungs in high tidal volume mechanical ventilation-induced acute lung injury. Proteome Sci.8,3 (2010).
  MedlineGoogle Scholar
• 63  St-Pierre Y, Couillard J, Van Themsche C. Regulation of MMP-9 gene expression for the development of novel molecular targets against cancer and inflammatory diseases. Expert Opin. Ther. Targets8(5),473–489 (2004).
  Medline CASGoogle Scholar
• 64  Martens E, Leyssen A, Van Aelst I et al. A monoclonal antibody inhibits gelatinase B/MMP-9 by selective binding to part of the catalytic domain and not to the fibronectin or zinc binding domains. Biochim. Biophys. Acta1770(2),178–186 (2007).
  Medline CASGoogle Scholar
• 65  Saglam F, Cavdar Z, Sarioglu S et al. Pioglitazone reduces peritoneal fibrosis via inhibition of TGF-beta, MMP-2, and MMP-9 in a model of encapsulating peritoneal sclerosis. Ren. Fail.34(1),95–102 (2012).
  Medline CASGoogle Scholar
• 66  Marchesi C, Dentali F, Nicolini E et al. Plasma levels of matrix metalloproteinases and their inhibitors in hypertension: a systematic review and meta-analysis. J. Hypertens.30(1),3–16 (2012).
  Medline CASGoogle Scholar
• 67  Zhao S, Choksuchat C, Zhao Y et al. Effects of doxycycline on serum and endometrial levels of MMP-2, MMP-9 and TIMP-1 in women using a levonorgestrel-releasing subcutaneous implant. Contraception79(6),469–478 (2009).
  Medline CASGoogle Scholar
• 68  Overall CM. Dilating the degradome: matrix metalloproteinase 2 (MMP-2) cuts to the heart of the matter. Biochem J.383(Pt 3),e5–e7 (2004).
  Medline CASGoogle Scholar
• 69  St-Pierre Y, Couillard J, Van Themsche C. Regulation of MMP-9 gene expression for the development of novel molecular targets against cancer and inflammatory diseases. Expert Opin. Ther. Targets8(5),473–489 (2004).
  Medline CASGoogle Scholar
• 70  Ali MA, Schulz R. Activation of MMP-2 as a key event in oxidative stress injury to the heart. Front. Biosci.14,699–716 (2009).
  Medline CASGoogle Scholar
• 71  Viappiani S, Nicolescu AC, Holt A et al. Activation and modulation of 72 kDa matrix metalloproteinase-2 by peroxynitrite and glutathione. Biochem. Pharmacol.77(5),826–834 (2009).
  Medline CASGoogle Scholar
• 72  Wang W, Sawicki G, Schulz R. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc. Res.53(1),165–174 (2002).
  Medline CASGoogle Scholar
• 73  Sariahmetoglu M, Crawford BD, Leon H et al. Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation. FASEB J.21(10),2486–2495 (2007).
  Medline CASGoogle Scholar
• 74  Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim. Biophys. Acta1803(1),55–71 (2010).
  Medline CASGoogle Scholar
• 75  Falk V, Soccal PM, Grunenfelder J et al. Regulation of matrix metalloproteinases and effect of MMP-inhibition in heart transplant related reperfusion injury. Eur. J. Cardiothorac. Surg.22(1),53–58 (2002).
  Medline CASGoogle Scholar
• 76  Peterson JT. The importance of estimating the therapeutic index in the development of matrix metalloproteinase inhibitors. Cardiovasc. Res.69(3),677–687 (2006).
  Medline CASGoogle Scholar
• 77  Agren MS, Mirastschijski U, Karlsmark T, Saarialho-Kere UK. Topical synthetic inhibitor of matrix metalloproteinases delays epidermal regeneration of human wounds. Exp. Dermatol.10(5),337–348 (2001).
  Medline CASGoogle Scholar
• 78  Cheung PY, Sawicki G, Wozniak M et al. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation101(15),1833–1839 (2000).
  Medline CASGoogle Scholar
• 79  Leon H, Baczko I, Sawicki G, Light PE, Schulz R. Inhibition of matrix metalloproteinases prevents peroxynitrite-induced contractile dysfunction in the isolated cardiac myocyte. Br. J. Pharmacol.153(4),676–683 (2008).
  Medline CASGoogle Scholar
• 80  Fert-Bober J, Leon H, Sawicka J et al. Inhibiting matrix metalloproteinase-2 reduces protein release into coronary effluent from isolated rat hearts during ischemia-reperfusion. Basic Res. Cardiol.103(5),431–443 (2008).
  Medline CASGoogle Scholar
• 81  Golub LM, Lee HM, Ryan ME et al. Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv. Dent. Res.12(2),12–26 (1998).
  Medline CASGoogle Scholar
• 82  Tessone A, Feinberg MS, Barbash IM et al. Effect of matrix metalloproteinase inhibition by doxycycline on myocardial healing and remodeling after myocardial infarction. Cardiovasc. Drugs Ther.19(6),383–390 (2005).
  Medline CASGoogle Scholar
• 83  He G. Electron paramagnetic resonance oximetry and redoximetry. Methods Mol. Biol.594,85–105 (2010).
  Medline CASGoogle Scholar
• 84  Sanz-Rosa D, Garcia-Prieto J, Ibanez B. The future: therapy of myocardial protection. Ann. NY Acad. Sci.1254,90–98 (2012).
  Medline CASGoogle Scholar
• 85  Marchant DJ, Boyd JH, Lin DC et al. Inflammation in myocardial diseases. Circ. Res.110(1),126–144 (2012).
  Medline CASGoogle Scholar
• 86  Stanley WC, Recchia FA, Lopaschuk GD. Myocardial substrate metabolism in the normal and failing heart. Physiol. Rev.85(3),1093–1129 (2005).
  Medline CASGoogle Scholar
• 87  Tucka J, Bennett M, Littlewood T. Cell death and survival signaling in the cardiovascular system. Front. Biosci.17,248–261 (2012).
  Medline CASGoogle Scholar
• 88  Baines CP. How and when do myocytes die during ischemia and reperfusion: the late phase. J. Cardiovasc. Pharmacol. Ther.16(3–4),239–243 (2011).
  Medline CASGoogle Scholar
• 89  Rouet-Benzineb P, Buhler JM, Dreyfus P et al. Altered balance between matrix gelatinases (MMP-2 and MMP-9) and their tissue inhibitors in human dilated cardiomyopathy: potential role of MMP-9 in myosin-heavy chain degradation. Eur. J. Heart Fail.1(4),337–352 (1999).
  Medline CASGoogle Scholar
• 90  Sawicki G, Jugdutt BI. Detection of regional changes in protein levels in the in vivo canine model of acute heart failure following ischemia-reperfusion injury: functional proteomics studies. Proteomics4(7),2195–2202 (2004).
  Medline CASGoogle Scholar
• 91  Gu X, Liu X, Xu D et al. Cardiac functional improvement in rats with myocardial infarction by up-regulating cardiac myosin light chain kinase with neuregulin. Cardiovasc. Res.88(2),334–343 (2010).
  Medline CASGoogle Scholar
• 92  Thygesen K, Alpert JS, Jaffe AS et al. Third universal definition of myocardial infarction. Eur. Heart J.33(20),2551–2567 (2012).
  MedlineGoogle Scholar
• 93  Seguchi O, Takashima S, Yamazaki S et al. A cardiac myosin light chain kinase regulates sarcomere assembly in the vertebrate heart. J. Clin. Invest.117(10),2812–2824 (2007).
  Medline CASGoogle Scholar