Abstract
Matrix metalloproteinases (MMPs) are central to the development and progression of dysfunctional ventricular remodeling after tissue injury. We studied 6 month old heterozygous mice with cardiac-specific transgenic expression of active MMP-2 (MMP-2 Tg). MMP-2 Tg hearts showed no substantial gross alteration of cardiac phenotype compared to age-matched wild-type littermates. However, buffer perfused MMP-2 Tg hearts subjected to 30 min of global ischemia followed by 30 min of reperfusion had a larger infarct size and greater depression in contractile performance compared to wild-type hearts. Importantly, cardioprotection mediated by ischemic preconditioning (IPC) was completely abolished in MMP-2 Tg hearts, as shown by abnormalities in mitochondrial ultrastructure and impaired respiration, increased lipid peroxidation, cell necrosis and persistently reduced recovery of contractile performance during post-ischemic reperfusion. We conclude that MMP-2 functions not only as a proteolytic enzyme but also as a previously unrecognized active negative regulator of mitochondrial function during superimposed oxidative stress.
MeSH Terms
Animals
Creatine Kinase/metabolism
Heterozygote
Ischemic Preconditioning, Myocardial
Lipid Peroxidation
Matrix Metalloproteinase 2/biosynthesis,genetics
Mice
Mice, Transgenic
Mitochondria, Heart/enzymology,physiology
Myocardial Contraction
Myocardial Infarction/enzymology,pathology,physiopathology
Myocardial Reperfusion Injury/enzymology,pathology,physiopathology
Myocardium/enzymology,pathology,ultrastructure
Necrosis
Chemicals
Creatine Kinase
Matrix Metalloproteinase 2
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zhou Hui-Zhong
Cardiology Section, Department of Medicine, UCSF, VA Medical Center, 4150 Clement Street, 111C-5, San Francisco, CA 94121, USA.
Ma Xiaokui
Gray Mary O
Zhu Bo-qing
Nguyen Anita P
Baker Anthony J
Simonis Ursula
Cecchini Gary
Lovett David H
Karliner Joel S
References (29)
29 references, click to expand
-
Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart.
Circulation. 2000 Apr 18;101(15):1833-9
PMID: 10769285
-
Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction.
Am J Physiol Heart Circ Physiol. 2007 Apr;292(4):H1847-60
PMID: 17158653
-
Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury.
Circulation. 2002 Sep 17;106(12):1543-9
PMID: 12234962
-
Duration of ischaemia determines matrix metalloproteinase-2 activation in the reperfused rabbit heart.
Proteomics. 2002 Sep;2(9):1204-10
PMID: 12362337
-
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. 2003 Feb 1;369(Pt 3):485-96
PMID: 12371906
-
Left ventricular remodeling and ventricular arrhythmias after myocardial infarction.
Circulation. 2003 May 27;107(20):2577-82
PMID: 12732606
-
Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase C epsilon.
J Biol Chem. 2004 Jan 30;279(5):3596-604
PMID: 14600145
-
Circulating matrix metalloproteinase-2 is elevated in patients with congestive heart failure.
Eur J Heart Fail. 2004 Jan;6(1):41-5
PMID: 15012917
-
Matrix metalloproteinase-2 (MMP-2) is present in the nucleus of cardiac myocytes and is capable of cleaving poly (ADP-ribose) polymerase (PARP) in vitro.
FASEB J. 2004 Apr;18(6):690-2
PMID: 14766804
-
Increased circulating matrix metalloproteinase-2 in patients with hypertrophic cardiomyopathy with systolic dysfunction.
Circ J. 2004 Apr;68(4):355-60
PMID: 15056834
-
Ultrastructural evidence of increased tolerance of hibernating myocardium to cardioplegic ischemia-reperfusion injury.
J Am Coll Cardiol. 2004 Jun 16;43(12):2329-36
PMID: 15193702
-
Mitochondrial redox control of matrix metalloproteinases.
Free Radic Biol Med. 2004 Sep 15;37(6):768-84
PMID: 15304253
-
Sphingosine kinase activation mediates ischemic preconditioning in murine heart.
Circulation. 2004 Oct 5;110(14):1980-9
PMID: 15451787
-
Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction.
Anal Biochem. 1979 Jun;95(2):351-8
PMID: 36810
-
Ischaemia-reperfusion injury activates matrix metalloproteinases in the human heart.
Eur Heart J. 2005 Jan;26(1):27-35
PMID: 15615796
-
Targeted deletion or pharmacological inhibition of MMP-2 prevents cardiac rupture after myocardial infarction in mice.
J Clin Invest. 2005 Mar;115(3):599-609
PMID: 15711638
-
Underlying mechanism of hypoxic preconditioning decreasing apoptosis induced by anoxia in cultured hippocampal neurons.
Neurosignals. 2005;14(3):109-16
PMID: 16088225
-
Mitochondria and ischemia/reperfusion injury.
Ann N Y Acad Sci. 2005 Jun;1047:248-58
PMID: 16093501
-
Circulating matrix metalloproteinase-2 but not matrix metalloproteinase-3, matrix metalloproteinase-9, or tissue inhibitor of metalloproteinase-1 predicts outcome in patients with congestive heart failure.
Am Heart J. 2005 Sep;150(3):484-7
PMID: 16169329
-
Selective disruption of MMP-2 gene exacerbates myocardial inflammation and dysfunction in mice with cytokine-induced cardiomyopathy.
Am J Physiol Heart Circ Physiol. 2005 Nov;289(5):H1858-64
PMID: 15937097
-
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. 2006 Jan;290(1):C254-61
PMID: 16148033
-
Hyperlipidemia attenuates the infarct size-limiting effect of ischemic preconditioning: role of matrix metalloproteinase-2 inhibition.
J Pharmacol Exp Ther. 2006 Jan;316(1):154-61
PMID: 16166272
-
Cardiac transgenic matrix metalloproteinase-2 expression directly induces impaired contractility.
Cardiovasc Res. 2006 Feb 15;69(3):688-96
PMID: 16183043
-
Structure and function of matrix metalloproteinases and TIMPs.
Cardiovasc Res. 2006 Feb 15;69(3):562-73
PMID: 16405877
-
Poly(ADP-ribose) polymerase-1 hyperactivation and impairment of mitochondrial respiratory chain complex I function in reperfused mouse hearts.
Am J Physiol Heart Circ Physiol. 2006 Aug;291(2):H714-23
PMID: 16582021
-
Comparison of pyrroloquinoline quinone and/or metoprolol on myocardial infarct size and mitochondrial damage in a rat model of ischemia/reperfusion injury.
J Cardiovasc Pharmacol Ther. 2006 Jun;11(2):119-28
PMID: 16891289
-
Cardiac ischemia-reperfusion injury induces matrix metalloproteinase-2 expression through the AP-1 components FosB and JunB.
Am J Physiol Heart Circ Physiol. 2006 Oct;291(4):H1838-46
PMID: 16699069
-
Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches.
Annu Rev Pharmacol Toxicol. 2007;47:211-42
PMID: 17129183
-
Preconditioning decreases ischemia/reperfusion-induced release and activation of matrix metalloproteinase-2.
Biochem Biophys Res Commun. 2002 Aug 30;296(4):937-41
PMID: 12200138