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PMID: 17475219 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Transgenic MMP-2 expression induces latent cardiac mitochondrial dysfunction.

Biochemical and biophysical research communications ·Vol. 358 ·No. 1 ·2007-06-22 ·Pages 189-95

Zhou HZ, Ma X, Gray MO, Zhu BQ, Nguyen AP, Baker AJ, Simonis U, Cecchini G, Lovett DH, Karliner JS

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
  1. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart.
    Circulation. 2000 Apr 18;101(15):1833-9 PMID: 10769285
  2. 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
  3. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury.
    Circulation. 2002 Sep 17;106(12):1543-9 PMID: 12234962
  4. Duration of ischaemia determines matrix metalloproteinase-2 activation in the reperfused rabbit heart.
    Proteomics. 2002 Sep;2(9):1204-10 PMID: 12362337
  5. 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
  6. Left ventricular remodeling and ventricular arrhythmias after myocardial infarction.
    Circulation. 2003 May 27;107(20):2577-82 PMID: 12732606
  7. 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
  8. Circulating matrix metalloproteinase-2 is elevated in patients with congestive heart failure.
    Eur J Heart Fail. 2004 Jan;6(1):41-5 PMID: 15012917
  9. 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
  10. Increased circulating matrix metalloproteinase-2 in patients with hypertrophic cardiomyopathy with systolic dysfunction.
    Circ J. 2004 Apr;68(4):355-60 PMID: 15056834
  11. 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
  12. Mitochondrial redox control of matrix metalloproteinases.
    Free Radic Biol Med. 2004 Sep 15;37(6):768-84 PMID: 15304253
  13. Sphingosine kinase activation mediates ischemic preconditioning in murine heart.
    Circulation. 2004 Oct 5;110(14):1980-9 PMID: 15451787
  14. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction.
    Anal Biochem. 1979 Jun;95(2):351-8 PMID: 36810
  15. Ischaemia-reperfusion injury activates matrix metalloproteinases in the human heart.
    Eur Heart J. 2005 Jan;26(1):27-35 PMID: 15615796
  16. 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
  17. Underlying mechanism of hypoxic preconditioning decreasing apoptosis induced by anoxia in cultured hippocampal neurons.
    Neurosignals. 2005;14(3):109-16 PMID: 16088225
  18. Mitochondria and ischemia/reperfusion injury.
    Ann N Y Acad Sci. 2005 Jun;1047:248-58 PMID: 16093501
  19. 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
  20. 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
  21. 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
  22. 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
  23. Cardiac transgenic matrix metalloproteinase-2 expression directly induces impaired contractility.
    Cardiovasc Res. 2006 Feb 15;69(3):688-96 PMID: 16183043
  24. Structure and function of matrix metalloproteinases and TIMPs.
    Cardiovasc Res. 2006 Feb 15;69(3):562-73 PMID: 16405877
  25. 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
  26. 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
  27. 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
  28. Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches.
    Annu Rev Pharmacol Toxicol. 2007;47:211-42 PMID: 17129183
  29. 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
Article Info
Journal
Biochemical and biophysical research communications
Abbr.
Biochem Biophys Res Commun
ISSN
0006-291X
Published
2007-06-22
Epub
2007-00-23
Pages
189-95
Language
English
Region
United States
NLM ID
0372516
PMCID
PMC3423089
Subset
IM
Grants
NHLBI NIH HHS · P01 HL068738 · United States
NHLBI NIH HHS · P01HL068738-01A1 · United States
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