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Research Article

Long-Term MMP Inhibition by Doxycycline Exerts Divergent Effect on Ventricular Extracellular Matrix Deposition and Systolic Performance in Stroke-Prone Spontaneously Hypertensive Rats

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Pages 316-324 | Received 25 Jun 2010, Accepted 03 Nov 2010, Published online: 07 Jun 2011

REFERENCES

  • Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol 2008;75:346–359.
  • Spinale FG. Myocardial matrix remodeling and the matrix metalloproteinases: influence on cardiac form and function. Physiol Rev 2007;87:1285–1342.
  • Schulz R. Intracellular targets of matrix metalloproteinase-2 in cardiac disease: rationale and therapeutic approaches. Annu Rev Pharmacol Toxicol 2007;47:211–242.
  • Ronco P, Lelongt B, Piedagnel R, Chatziantoniou C. Matrix metalloproteinases in kidney disease progression and repair: a case of flipping the coin. Semin Nephrol 2007;27:352–362.
  • Golub LM, Lee HM, Ryan ME, Giannobile WV, Payne J, Sorsa T. Tetracyclines inhibit connective tissue breakdown by multiple non-antimicrobial mechanisms. Adv Dent Res 1998;12:12–26.
  • Brown DL, Desai KK, Vakili BA, Nouneh C, Lee HM, Golub LM. Clinical and biochemical results of the metalloproteinase inhibition with subantimicrobial doses of doxycycline to prevent acute coronary syndromes (MIDAS) pilot trial. Arterioscler Thromb Vasc Biol 2004;24:733–738.
  • Xiong W, Knispel RA, Dietz HC, Ramirez F, Baxter BT. Doxycycline delays aneurysm rupture in a mouse model of Marfan syndrome. J Vasc Surg 2008;47:166–172; discussion 172.
  • Chung AW, Yang HH, Radomski MW, van Breemen C. Long-term doxycycline is more effective than atenolol to prevent thoracic aortic aneurysm in marfan syndrome through the inhibition of matrix metalloproteinase-2 and -9. Circ Res 2008;102:e73–85.
  • Castro MM, Rizzi E, Figueiredo-Lopes L, Fernandes K, Bendhack LM, Pitol DL, Gerlach RF, Tanus-Santos JE. Metalloproteinase inhibition ameliorates hypertension and prevents vascular dysfunction and remodeling in renovascular hypertensive rats. Atherosclerosis 2008;198:320–331.
  • Axisa B, Loftus IM, Naylor AR, Goodall S, Jones L, Bell PR, Thompson MM. Prospective, randomized, double-blind trial investigating the effect of doxycycline on matrix metalloproteinase expression within atherosclerotic carotid plaques. Stroke 2002;33:2858–2864.
  • Yaras N, Sariahmetoglu M, Bilginoglu A, Aydemir–Koksoy A, Onay–Besikci A, Turan B, Schulz R. Protective action of doxycycline against diabetic cardiomyopathy in rats. Br J Pharmacol 2008;155:1174–1184.
  • Lindeman JH, Abdul-Hussien H, van Bockel JH, Wolterbeek R, Kleemann R. Clinical trial of doxycycline for matrix metalloproteinase-9 inhibition in patients with an abdominal aneurysm: doxycycline selectively depletes aortic wall neutrophils and cytotoxic T cells. Circulation 2009;119:2209–2216.
  • Naini AE, Harandi AA, Moghtaderi J, Bastani B, Amiran A. Doxycycline: a pilot study to reduce diabetic proteinuria. Am J Nephrol 2007;27:269–273.
  • Lokeshwar BL, Selzer MG, Zhu BQ, Block NL, Golub LM. Inhibition of cell proliferation, invasion, tumor growth and metastasis by an oral non-antimicrobial tetracycline analog (COL-3) in a metastatic prostate cancer model. Int J Cancer 2002;98:297–309.
  • Seftor RE, Seftor EA, De Larco JE, Kleiner DE, Leferson J, Stetler-Stevenson WG, McNamara TF, Golub LM, Hendrix MJ. Chemically modified tetracyclines inhibit human melanoma cell invasion and metastasis. Clin Exp Metastasis 1998;16:217–225.
  • Coker ML, Doscher MA, Thomas CV, Galis ZS, Spinale FG. Matrix metalloproteinase synthesis and expression in isolated LV myocyte preparations. Am J Physiol 1999;277:H777–787.
  • Chapman RE, Scott AA, Deschamps AM, Lowry AS, Stroud RE, Ikonomidis JS, Spinale FG. Matrix metalloproteinase abundance in human myocardial fibroblasts: effects of sustained pharmacologic matrix metalloproteinase inhibition. J Mol Cell Cardiol 2003;35:539–548.
  • Bouvet C, Gilbert LA, Girardot D, deBlois D, Moreau P. Different involvement of extracellular matrix components in small and large arteries during chronic NO synthase inhibition. Hypertension 2005;45:432–437.
  • Thomas AC, Newby AC. Effect of matrix metalloproteinase-9 knockout on vein graft remodelling in mice. J Vasc Res 2010;47:299–308.
  • Bergman MR, Teerlink JR, Mahimkar R, Li L, Zhu BQ, Nguyen A, Dahi S, Karliner JS, Lovett DH. Cardiac matrix metalloproteinase-2 expression independently induces marked ventricular remodeling and systolic dysfunction. Am J Physiol Heart Circ Physiol 2007;292:H1847–1860.
  • Martinez ML, Lopes LF, Coelho EB, Nobre F, Rocha JB, Gerlach RF, Tanus-Santos JE. Lercanidipine reduces matrix metalloproteinase-9 activity in patients with hypertension. J Cardiovasc Pharmacol 2006;47:117–122.
  • Altieri P, Brunelli C, Garibaldi S, Nicolino A, Ubaldi S, Spallarossa P, Olivotti L, Rossettin P, Barsotti A, Ghigliotti G. Metalloproteinases 2 and 9 are increased in plasma of patients with heart failure. Eur J Clin Invest 2003;33:648–656.
  • Palei AC, Sandrim VC, Cavalli RC, Tanus-Santos JE. Comparative assessment of matrix metalloproteinase (MMP)-2 and MMP-9, and their inhibitors, tissue inhibitors of metalloproteinase (TIMP)-1 and TIMP-2 in preeclampsia and gestational hypertension. Clin Biochem 2008;41:875–880.
  • Sapadin AN, Fleischmajer R. Tetracyclines: nonantibiotic properties and their clinical implications. J Am Acad Dermatol 2006;54:258–265.
  • Peterson JT, Hallak H, Johnson L, Li H, O’Brien PM, Sliskovic DR, Bocan TM, Coker ML, Etoh T, Spinale FG. Matrix metalloproteinase inhibition attenuates left ventricular remodeling and dysfunction in a rat model of progressive heart failure. Circulation 2001;103:2303–2309.
  • Errami M, Galindo CL, Tassa AT, Dimaio JM, Hill JA, Garner HR. Doxycycline attenuates isoproterenol- and transverse aortic banding-induced cardiac hypertrophy in mice. J Pharmacol Exp Ther 2008;324:1196–1203.
  • Vinet L, Rouet-Benzineb P, Marniquet X, Pellegrin N, Mangin L, Louedec L, Samuel JL, Mercadier JJ. Chronic doxycycline exposure accelerates left ventricular hypertrophy and progression to heart failure in mice after thoracic aorta constriction. Am J Physiol Heart Circ Physiol 2008;295:H352–360.
  • Manning MW, Cassis LA, Daugherty A. Differential effects of doxycycline, a broad-spectrum matrix metalloproteinase inhibitor, on angiotensin II-induced atherosclerosis and abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 2003;23:483–488.
  • Villarreal FJ, Griffin M, Omens J, Dillmann W, Nguyen J, Covell J. Early short-term treatment with doxycycline modulates postinfarction left ventricular remodeling. Circulation 2003;108:1487–1492.
  • Haas TL, Doyle JL, Distasi MR, Norton LE, Sheridan KM, Unthank JL. Involvement of MMPs in the outward remodeling of collateral mesenteric arteries. Am J Physiol Heart Circ Physiol 2007;293:H2429–2437.
  • Griffin MO, Jinno M, Miles LA, Villarreal FJ. Reduction of myocardial infarct size by doxycycline: a role for plasmin inhibition. Mol Cell Biochem 2005;270:1–11.
  • Garcia RA, Go KV, Villarreal FJ. Effects of timed administration of doxycycline or methylprednisolone on post-myocardial infarction inflammation and left ventricular remodeling in the rat heart. Mol Cell Biochem 2007;300:159–169.
  • Pacher P, Mabley JG, Liaudet L, Evgenov OV, Marton A, Hasko G, Kollai M, Szabo C. Left ventricular pressure-volume relationship in a rat model of advanced aging-associated heart failure. Am J Physiol Heart Circ Physiol 2004;287:H2132–2137.
  • Cingolani OH, Yang XP, Liu YH, Villanueva M, Rhaleb NE, Carretero OA. Reduction of cardiac fibrosis decreases systolic performance without affecting diastolic function in hypertensive rats. Hypertension 2004;43:1067–1073.
  • Zhou X, Li YM, Ji WJ, Jiang TM, Sun XN, Zhu Y, Shi R. Phenytoin can accelerate the healing process after experimental myocardial infarction? Int J Cardiol 2006;107:21–29.
  • Whittaker P, Kloner RA, Boughner DR, Pickering JG. Quantitative assessment of myocardial collagen with picrosirius red staining and circularly polarized light. Bas Res Cardiol 1994;89:397–410.
  • Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, Riggs CM. Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat 2003;274:157–168.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402–408.
  • Li YY, McTiernan CF, Feldman AM. Proinflammatory cytokines regulate tissue inhibitors of metalloproteinases and disintegrin metalloproteinase in cardiac cells. Cardiovasc Res 1999;42:162–172.
  • Goldberg GI, Strongin A, Collier IE, Genrich LT, Marmer BL. Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 1992;267:4583–4591.
  • Cheung C, Marchant D, Walker EK, Luo Z, Zhang J, Yanagawa B, Rahmani M, Cox J, Overall C, Senior RM, Luo H, McManus BM. Ablation of matrix metalloproteinase-9 increases severity of viral myocarditis in mice. Circulation 2008;117:1574–1582.
  • Castro MM, Rizzi E, Prado CM, Rossi MA, Tanus-Santos JE, Gerlach RF. Imbalance between matrix metalloproteinases and tissue inhibitor of metalloproteinases in hypertensive vascular remodeling. Matrix Biol 2010;29:194–201.
  • Briest W, Holzl A, Rassler B, Deten A, Baba HA, Zimmer HG. Significance of matrix metalloproteinases in norepinephrine-induced remodelling of rat hearts. Cardiovasc Res 2003;57:379–387.
  • Takimoto E, Champion HC, Li M, Ren S, Rodriguez ER, Tavazzi B, Lazzarino G, Paolocci N, Gabrielson KL, Wang Y, Kass DA. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 2005;115:1221–1231.
  • Sariahmetoglu M, Crawford BD, Leon H, Sawicka J, Li L, Ballermann BJ, Holmes C, Berthiaume LG, Holt A, Sawicki G, Schulz R. Regulation of matrix metalloproteinase-2 (MMP-2) activity by phosphorylation. FASEB J 2007;21:2486–2495.
  • Sawicki G, Leon H, Sawicka J, Sariahmetoglu M, Schulze CJ, Scott PG, Szczesna-Cordary D, Schulz R. Degradation of myosin light chain in isolated rat hearts subjected to ischemia-reperfusion injury: a new intracellular target for matrix metalloproteinase-2. Circulation 2005;112:544–552.
  • Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JR, Sawicki G, Schulz R. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation 2002;106:1543–1549.
  • Zhou HZ, Ma X, Gray MO, Zhu BQ, Nguyen AP, Baker AJ, Simonis U, Cecchini G, Lovett DH, Karliner JS. Transgenic MMP-2 expression induces latent cardiac mitochondrial dysfunction. Biochem Biophys Res Commun 2007;358:189–195.
  • Griffin MO, Fricovsky E, Ceballos G, Villarreal F. Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature. Am J Physiol Cell Physiol 2010;299:C539–548.
  • Kivela-Rajamaki M, Maisi P, Srinivas R, Tervahartiala T, Teronen O, Husa V, Salo T, Sorsa T. Levels and molecular forms of MMP-7 (matrilysin-1) and MMP-8 (collagenase-2) in diseased human peri-implant sulcular fluid. J Periodontal Res 2003;38:583–590.
  • Nip LH, Uitto VJ, Golub LM. Inhibition of epithelial cell matrix metalloproteinases by tetracyclines. J Periodontal Res 1993;28:379–385.
  • Smith GN, Jr., Jr. Mickler EA, Hasty KA, Brandt KD. Specificity of inhibition of matrix metalloproteinase activity by doxycycline: relationship to structure of the enzyme. Arthritis Rheum 1999;42:1140–1146.
  • Janicki JS, Brower GL, Gardner JD, Forman MF, Stewart JA, Jr., Jr. Murray DB, Chancey AL. Cardiac mast cell regulation of matrix metalloproteinase-related ventricular remodeling in chronic pressure or volume overload. Cardiovasc Res 2006;69:657–665.
  • Rocha R, Chander PN, Khanna K, Zuckerman A, Stier CT, Jr., Jr. Mineralocorticoid blockade reduces vascular injury in stroke-prone hypertensive rats. Hypertension 1998;31:451–458.
  • Stier CT, Jr., Jr., Benter IF, Ahmad S, Zuo HL, Selig N, Roethel S, Levine S, Itskovitz HD. Enalapril prevents stroke and kidney dysfunction in salt-loaded stroke-prone spontaneously hypertensive rats. Hypertension 1989;13:115–121.
  • Stier CT, Jr. Jr., Rocha R, Chander PN. Effect of aldosterone and MR blockade on the brain and the kidney. Heart Fail Rev 2005;10:53–62.
  • Wang M, Zhang J, Spinetti G, Jiang LQ, Monticone R, Zhao D, Cheng L, Krawczyk M, Talan M, Pintus G, Lakatta EG. Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am J Pathol 2005;167:1429–1442.
  • Castoldi G, di Gioia CR, Travaglini C, Busca G, Redaelli S, Bombardi C, Stella A. Angiotensin II increases tissue-specific inhibitor of metalloproteinase-2 expression in rat aortic smooth muscle cells in vivo: evidence of a pressure-independent effect. Clin Exp Pharmacol Physiol 2007;34:205–209.
  • Guo RW, Yang LX, Wang H, Liu B, Wang L. Angiotensin II induces matrix metalloproteinase-9 expression via a nuclear factor-kappaB-dependent pathway in vascular smooth muscle cells. Regul Pept 2008;147:37–44.
  • McElmurray JH, 3rd, 3rd, Mukherjee R, New RB, Sampson AC, King MK, Hendrick JW, Goldberg A, Peterson TJ, Hallak H, Zile MR, Spinale FG. Angiotensin-converting enzyme and matrix metalloproteinase inhibition with developing heart failure: comparative effects on left ventricular function and geometry. J Pharmacol Exp Ther 1999;291:799–811.

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