Metalloproteinases in the pathogenesis and progression of metabolic syndrome: potential targets for improved outcomes

References

• Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev. 2005;85:1–31.
   PubMed Web of Science ®Google Scholar
• Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69:562–573.
   PubMed Web of Science ®Google Scholar
• Borkakoti N. Structural studies of matrix metalloproteinases. J Mol Med. 2000;78:261–268.
   PubMed Web of Science ®Google Scholar
• Nagase H. Metalloproteases. Curr Protoc Protein Sci. 2011;Chapter 21(Unit 21.4):1–13.
   Google Scholar
• Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115:3719–3727.
   PubMed Web of Science ®Google Scholar
• Vu TH, Werb Z. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 2000;14:2123–2133.
   PubMed Web of Science ®Google Scholar
• Roy R, Zhang B, Moses MA. Making the cut: protease-mediated regulation of angiogenesis. Exp Cell Res. 2006;312:608–622.
   PubMed Web of Science ®Google Scholar
• Newby AC. Metalloproteinases and vulnerable atherosclerotic plaques. Trends Cardiovasc Med. 2007;17:253–258.
   PubMed Web of Science ®Google Scholar
• Lijnen HR. Murine models of obesity and hormonal therapy. Thromb Res. 2011;127:S17–S20.
   Web of Science ®Google Scholar
• Berg G, Miksztowicz V, Schreier L. Metalloproteinases in metabolic syndrome. Clin Chim Acta. 2011;412:1731–1739.
   PubMed Web of Science ®Google Scholar
• de Nooijer R, Verkleij CJ, von der Thüsen JH, et al. Lesional overexpression of matrix metalloproteinase-9 promotes intraplaque hemorrhage in advanced lesions but not at earlier stages of atherogenesis. Arterioscler Thromb Vasc Biol. 2006;26:340–346.
   PubMed Web of Science ®Google Scholar
• Choudhary S, Higgins CL, Chen IY, et al. Quantitation and localization of matrix metalloproteinases and their inhibitors in human carotid endarterectomy tissues. Arterioscler Thromb Vasc Biol. 2006;26:2351–2358.
   PubMed Web of Science ®Google Scholar
• Bouloumie A, Sengenes C, Portolan G, Galitzky J, Lafontan M. Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes. 2001;50:2080–2086.
   PubMed Web of Science ®Google Scholar
• Lijnen HR, Maquoi E, Holvoet P, et al. Adipose tissue expression of gelatinases in mouse models of obesity. Thromb Haemost. 2001;85:1111–1116.
   PubMed Web of Science ®Google Scholar
• Van Hul M, Lijnen HR. Effect of weight loss on gelatinase levels in obese mice. Clin Exp Pharmacol Physiol. 2011;38:647–649.
   Web of Science ®Google Scholar
• Grundy SM, Cleeman JI, Merz CN, et al. Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III Guidelines. Circulation. 2004;110:227–239.
   PubMed Web of Science ®Google Scholar
• Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the international diabetes federation task force on epidemiology and prevention; National heart, lung, and blood institute; American heart association; World heart federation; International atherosclerosis society; and International Association for the Study of Obesity. Circulation. 2009;120:1640–1645.
   PubMed Web of Science ®Google Scholar
• Alberti KG, Zimmet P, Shaw J. The metabolic syndrome – a new worldwide definition. Lancet. 2005;366:1059–1062.
   PubMed Web of Science ®Google Scholar
• Olijhoek JK, van der Graaf Y, Banga JD, Algra A, Rabelink TJ, Visseren FL. The metabolic syndrome is associated with advanced vascular damage in patients with coronary heart disease, stroke, peripheral arterial disease or abdominal aortic aneurysm. Eur Heart J. 2004;25:342–348.
   PubMed Web of Science ®Google Scholar
• Hopps E, Caimi G. Matrix metaloproteases in metabolic syndrome. Eur J Intern Med. 2012;23:99–104.
   Web of Science ®Google Scholar
• Hoseini SM, Kalantari A, Afarideh M, et al. Evaluation of plasma MMP-8, MMP-9 and TIMP-1 identifies candidate cardiometabolic risk marker in metabolic syndrome: results from double-blinded nested case-control study. Metabolism. 2015;64:527–538.
   Web of Science ®Google Scholar
• Miksztowicz V, Muzzio ML, Royer M, et al. Increased plasma activity of metalloproteinase 2 in women with metabolic syndrome. Metabolism. 2008;57:1493–1496.
   PubMed Web of Science ®Google Scholar
• Muzzio ML, Miksztowicz V, Repetto EM, Brites F, Berg G, Schreier L. Increased MMP-2 in healthy postmenopausal women. Ann Clin Biochem. 2012;49:75–79.
   Web of Science ®Google Scholar
• Hopps E, Lo Presti R, Montana M, Noto D, Averna MR, Caimi G. Gelatinases and their tissue inhibitors in a group of subjects with metabolic syndrome. J Investig Med. 2013;61:978–983.
   PubMed Web of Science ®Google Scholar
• Gonçalves FM, Jacob-Ferreira AL, Gomes VA, et al. Increased circulating levels of matrix metalloproteinase (MMP)-8, MMP-9, and pro-inflammatory markers in patients with metabolic syndrome. Clin Chim Acta. 2009;403:173–177.
   PubMed Web of Science ®Google Scholar
• Johnson JL. Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev Cardiovasc Ther. 2007;5:265–282.
   PubMedGoogle Scholar
• Opstad TB, Arnesen H, Pettersen A, Seljeflot I. The MMP-9-1562 C/T polymorphism in the presence of metabolic syndrome increases the risk of clinical events in patients with coronary artery disease. PLoS One. 2014;9:e106816.
   Web of Science ®Google Scholar
• Gummesson A, Hagg D, Olson FJ, Hulthe J, Carlsson LM, Fagerberg B. Adipose tissue is not an important source for matrix metalloproteinase-9 in the circulation. Scand J Clin Lab Invest. 2009;69:636–642.
   PubMed Web of Science ®Google Scholar
• Boden G. Obesity and free fatty acids. Endocrinol Metab Clin North Am. 2008;37:635–646.
   PubMed Web of Science ®Google Scholar
• Maquoi E, Munaut C, Colige A, Collen D, Lijnen HR. Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes. 2002;51:1093–1101.
   PubMed Web of Science ®Google Scholar
• Christiaens V, Lijnen HR. Role of the fibrinolytic and matrix metalloproteinase systems in development of adipose tissue. Arch Physiol Biochem. 2006;112:254–259.
   PubMedGoogle Scholar
• Lijnen HR, Maquoi E, Hansen LB, Van Hoef B, Frederix L, Collen D. Matrix metalloproteinase inhibition impairs adipose tissue development in mice. Arterioscler Thromb Vasc Biol. 2002;22:374–379.
   PubMed Web of Science ®Google Scholar
• Miksztowicz V, Morales C, Zago V, Friedman S, Schreier L, Berg G. Effect of insulin-resistance on circulating and adipose tissue MMP-2 and MMP-9 activity in rats fed a sucrose-rich diet. Nutr Metab Cardiovasc Dis. 2014;24:294–300.
   PubMed Web of Science ®Google Scholar
• Pendás AM, Folgueras AR, Llano E, et al. Diet-induced obesity and reduced skin cancer susceptibility in matrix metalloproteinase 19-deficient mice. Mol Cell Biol. 2004;24:5304–5313.
   PubMed Web of Science ®Google Scholar
• Maquoi E, Demeulemeester D, Voros G, Collen D, Lijnen HR. Enhanced nutritionally induced adipose tissue development in mice with stromelysin-1 gene inactivation. Thromb Haemost. 2003;89:696–704.
   PubMed Web of Science ®Google Scholar
• Lijnen HR, Van HB, Frederix L, Rio MC, Collen D. Adipocyte hypertrophy in stromelysin-3 deficient mice with nutritionally induced obesity. Thromb Haemost. 2002;87:530–535.
   PubMed Web of Science ®Google Scholar
• Chun TH, Inoue M, Morisaki H, et al. Genetic link between obesity and MMP14-dependent adipogenic collagen turnover. Diabetes. 2010;59:2484–2494.
   PubMed Web of Science ®Google Scholar
• Despres JP, Lamarchie B, Mauriège P, et al. Hyperinsulinemia as an independent risk factor for ischemic heart disease. N Engl J Med. 1996;334:952–957.
   PubMed Web of Science ®Google Scholar
• Pyoralla K. Relationship of glucose tolerance and plasma insulin to the incidence of coronary heart disease: results from two population studies in Finland. Diabetes Care. 1979;2:131–141.
   Google Scholar
• Lee MPS, Sweeney G. Insulin increases gelatinase activity in rat glomerular mesangial cells via ERK- and PI-3 kinase-dependent signalling. Diabetes Obes Metab. 2005;8:281–288.
   Web of Science ®Google Scholar
• Risinger GM, Hunt TS, Updike DL, Bullen EC, Howard EW. Matrix metalloproteinase-2 expression by vascular smooth muscle cells is mediated by both stimulatory and inhibitory signals in response to growth factors. J Biol Chem. 2006;281:25915–25925.
   Web of Science ®Google Scholar
• Saltiel AR, Kahn CR. Insulin signaling and the regulation of glucose and lipid metabolism. Nature. 2001;414:799–806.
   PubMed Web of Science ®Google Scholar
• Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes. 1997;46:3–10.
   PubMed Web of Science ®Google Scholar
• Boden G, Song W, Pashko L, Kresge K. In vivo effects of insulin and free fatty acids on matrix metalloproteinases in rat aorta. Diabetes. 2008;57:476–483.
   PubMed Web of Science ®Google Scholar
• Boden G, Song W, Kresge K, Mozzoli M, Cheung P. Effects of hyperinsulinemia on hepatic metalloproteinases and their tissue inhibitors. Am J Physiol Endocrinol Metab. 2008;295:e692–e697.
   Web of Science ®Google Scholar
• Trayhurn P, Alomar SY. Oxygen deprivation and the cellular response to hypoxia in adipocytes – perspectives on white and brown adipose tissues in obesity. Front Endocrinol. 2015;6:19.
   PubMed Web of Science ®Google Scholar
• Ntaios G, Gatselis NK, Makaritsis K, Dalekos GN. Adipokines as mediators of endothelial function and atherosclerosis. Atherosclerosis. 2013;227:216–221.
   PubMed Web of Science ®Google Scholar
• Sweeney G. Leptin signaling. Cell Signal. 2002;14:655–663.
   PubMed Web of Science ®Google Scholar
• Park HY, Kwon HM, Lim HJ, et al. Potential role of leptin in angiogenesis: leptin induces endothelial cell proliferation and expression of matrix metalloproteinases in vivo and in vitro. Exp Mol Med. 2001;33:95–102.
   PubMed Web of Science ®Google Scholar
• Oda A, Taniguchi T, Yokoyama M. Leptin stimulates rat aortic smooth muscle cell proliferation and migration. Kobe J Med Sci. 2001;47:141–150.
   PubMedGoogle Scholar
• Li L, Mamputu JC, Wiernsperger N, Renier G. Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin. Diabetes. 2005;54:2227–2234.
   PubMed Web of Science ®Google Scholar
• Madani S, De Girolamo S, Munoz DM, Li RK, Sweeney G. Direct effects of leptin on size and extracellular matrix components of human pediatric ventricular myocytes. Cardiovasc Res. 2005;69:716–725.
   Web of Science ®Google Scholar
• Schram K, Wong MM, Palanivel R, No EK, Dixon IM, Sweeney G. Increased expression and cell surface localization of MT1-MMP plays a role in stimulation of MMP-2 activity by leptin in neonatal rat cardiac myofibroblasts. J Mol Cell Cardiol. 2008;44:874–881
   PubMed Web of Science ®Google Scholar
• Moon HS, Lee HG, Seo JH, et al. Leptin-induced matrix metalloproteinase-2 secretion I suppressed by trans-10,cis-12 conjugated linoleic acid. Biochem Biophys Res Commun. 2007;356:955–956.
   PubMed Web of Science ®Google Scholar
• Reilly MP, Iqbal N, Schutta M, et al. Plasma leptin levels are associated with coronary atherosclerosis in type 2 diabetes. J Clin Endocrinol Metab. 2004;89:3872–3878.
   PubMed Web of Science ®Google Scholar
• Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie. 2012;94:2143–2149.
   PubMed Web of Science ®Google Scholar
• Matsuzawa Y. Adiponectin: identification, physiology and clinical relevance in metabolic and vascular disease. Atheroscler Suppl. 2005;6:7–14.
   PubMed Web of Science ®Google Scholar
• Arita Y, Kihara S, Ouchi N, et al. Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation. 2002;105:2893–2898.
   PubMed Web of Science ®Google Scholar
• Tong KM, Chen CP, Huang KC, et al. Adiponectin increases MMP-3 expression in human chondrocytes through AdipoR1 signaling pathway. J Cell Biochem. 2011;112:1431–1440.
   PubMed Web of Science ®Google Scholar
• Kumada M, Kihara S, Ouchi N, et al. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation. 2004;109:2046–2049.
   PubMed Web of Science ®Google Scholar
• Derosa G, Maffioli P, D’Angelo A, et al. Evaluation of metalloproteinase 2 and 9 levels and their inhibitors in combined dyslipidemia. Clin Invest Med. 2009;32:E124–E132.
   Web of Science ®Google Scholar
• Miksztowicz V, Fernandez Machulsky N, Lucero D, Fassio E, Schreier L, Berg G. Adiponectin predicts MMP-2 activity independently of obesity. Eur J Clin Invest. 2014;44:951–957.
   Web of Science ®Google Scholar
• Belo VA, Lacchini R, Miranda JA, Lanna CM, Souza-Costa DC, Tanus-Santos JE. Increased activity of MMP-2 in hypertensive obese children is associated with hypoadiponectinemia. Obesity. 2015;23:177–182.
   PubMed Web of Science ®Google Scholar
• Cheng M, Hashmi S, Mao X, Zeng QT. Relationships of adiponectin and matrix metalloproteinase-9 to tissue inhibitor of metalloproteinase-1 ratio with coronary plaque morphology in patients with acute coronary syndrome. Can J Cardiol. 2008;24:385–390.
   PubMed Web of Science ®Google Scholar
• Hwang J, Yang W, Chiang F, et al. Association of circulating matrix metalloproteinase-1, but not adiponectin, with advanced coronary artery disease. Atherosclerosis. 2009;204:293–297.
   Web of Science ®Google Scholar
• Farrell GC, Larter CZ. Nonalcoholic fatty liver disease: from steatosis to cirrhosis. Hepatology. 2006;43:s99–s112.
   PubMed Web of Science ®Google Scholar
• Angulo P. GI epidemiology: nonalcoholic fatty liver disease. Aliment Pharmacol Ther. 2007;25:883–889.
   PubMed Web of Science ®Google Scholar
• Musso G, Gambino R, Bo S, et al. Should nonalcoholic fatty liver disease be included in the definition of metabolic syndrome? A cross-sectional comparison with adult treatment panel III criteria in non-obese non-diabetic subjects. Diabetes Care. 2008;31(3):562–568.
   PubMed Web of Science ®Google Scholar
• Ahmed MH, Barakat S, Almobarak AO. Nonalcoholic fatty liver disease and cardiovascular disease: has the time come for cardiologists to be hepatologists? J Obes. 2012;2012:483135.
   PubMedGoogle Scholar
• Friedman SL. Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N Eng J Med. 1993;328:1828–1835.
   PubMed Web of Science ®Google Scholar
• Hemmann S, Graf J, Roderfeld M, Roeb E. Expression of MMPs and TIMPs in liver fibrosis a systematic review with special emphasis on anti-fibrotic strategies. J Hepatol. 2007;46:955–975.
   PubMed Web of Science ®Google Scholar
• Knittel T, Mehde M, Grundmann A, Saile B, Scharf J, Ramadori G. Expression of matrix metalloproteinases and their inhibitors during hepatic tissue repair in the rat. Histochem Cell Biol. 2000;113:443–453.
   PubMed Web of Science ®Google Scholar
• Wanninger J, Walter R, Bauer S, et al. MMP-9 activity is increased by adiponectin in primary human hepatocytes but even negatively correlates with serum adiponectin in a rodent model of non-alcoholic steatohepatitis. Exp Mol Pathol. 2011;91:603–607.
   PubMed Web of Science ®Google Scholar
• Takahara T, Furui K, Funaki J, et al. Increased expression of matrix metalloproteinase-II in experimental liver fibrosis in rats. Hepatology. 1995;21:787–795.
   Web of Science ®Google Scholar
• Okazaki I, Nabeshima K. Introduction: MMPs, ADAMs/ADAMTSs research products to achieve big dream. Anticancer Agents Med Chem. 2012;12:688–706.
   PubMed Web of Science ®Google Scholar
• Evans JM1, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD. Metformin and reduced risk of cancer in diabetic patients. Br Med J. 2005;330:1304–1305.
   PubMed Web of Science ®Google Scholar
• Bowker SL1, Majumdar SR, Veugelers P, Johnson JA. Increased cancer-related mortality for patients with type 2 diabetes who use sulfonylureas or insulin. Diabetes Care. 2006;29:254–258.
   PubMed Web of Science ®Google Scholar
• Hwang YP, Jeong HG. Metformin blocks migration and invasion of tumour cells by inhibition of matrix metalloproteinase-9 activation through a calcium and protein kinase Calpha-dependent pathway: phorbol-12-myristate-13-acetate-induced/extracellular signal-regulated kinase/activator protein-1. Br J Pharmacol. 2010;160:1195–1211.
   PubMed Web of Science ®Google Scholar
• Esfahanian N, Shakiba Y, Nikbin B, et al. Effect of metformin on the proliferation, migration, and MMP-2 and -9 expression of human umbilical vein endothelial cells. Mol Med Rep. 2012;5:1068–1074.
   Web of Science ®Google Scholar
• Sharma AK, Raikwar SK, Kurmi MK, Srinivasan BP. Gemfibrozil and its combination with metformin on pleiotropic effect on IL-10 and adiponectin and anti-atherogenic treatment in insulin resistant type 2 diabetes mellitus rats. Inflammopharmacology. 2013;21:137–145.
   PubMed Web of Science ®Google Scholar
• Goldstein BJ, Weissman PN, Wooddell MJ, Waterhouse BR, Cobitz AR. Reductions in biomarkers of cardiovascular risk in type 2 diabetes with rosiglitazone added to metformin compared with dose escalation of metformin: an EMPIRE trial sub-study. Curr Med Res Opin. 2006;22(9):1715–1723.
   PubMed Web of Science ®Google Scholar
• Huang Z, Lei MX, Liu L, Tang QB. Effects of rosiglitazone on the IMTc and serum MMP-9 levels in newly diagnosed type 2 diabetic patients. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2006;31:367–372.
   Google Scholar
• Kiyici S1, Ersoy C, Kaderli A, et al. Effect of rosiglitazone, metformin and medical nutrition treatment on arterial stiffness, serum MMP-9 and MCP-1 levels in drug naive type 2 diabetic patients. Diabetes Res Clin Pract. 2009;86:44–50.
   Web of Science ®Google Scholar
• Hanefeld M, Pfützner A, Forst T, Kleine I, Fuchs W. Double-blind, randomized, multicentre, and active comparator controlled investigation of the effect of pioglitazone, metformin, and the combination of both on cardiovascular risk in patients with type 2 diabetes receiving stable basal insulin therapy: the PIOCOMB study. Cardiovasc Diabetol. 2011;10:65.
   PubMed Web of Science ®Google Scholar
• Blaschke F, Spanheimer R, Khan M, Law RE. Vascular effects of TZDs: new implications. Vascul Pharmacol. 2006;45:3–18.
   PubMed Web of Science ®Google Scholar
• Pfützner A, Weise A, Pfützner-Riehn E, et al. Downregulation of the proinflammatory state of circulating mononuclear cells by short-term treatment with pioglitazone in patients with type 2 diabetes mellitus and coronary artery disease. PPAR Res. 2011;2011:647017.
   PubMed Web of Science ®Google Scholar
• Zhang J, Huang X, Wang L. Pioglitazone inhibits the expression of matrix metalloproteinase-9, a protein involved in diabetes-associated wound healing. Mol Med Rep. 2014;10:1084–1088.
   Web of Science ®Google Scholar
• Chen R, Yan J, Liu P, Wang Z. Effects of thiazolidinedione therapy on inflammatory markers of type 2 diabetes: a meta-analysis of randomized controlled trials. PLoS One. 2015;10:e0123703.
   PubMedGoogle Scholar
• 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–C548.
   PubMed Web of Science ®Google Scholar
• Peterson JT. Matrix metalloproteinase inhibitor development and the remodeling of drug discovery. Heart Fail Rev. 2004;9:63–79.
   PubMed Web of Science ®Google Scholar
• 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;112:544–552.
   PubMed Web of Science ®Google Scholar
• Wang W, Schulze CJ, Suarez-Pinzon WL, Dyck JRB, Sawicki G, Schulz R. Intracellular action of matrix metalloproteinase-2 accounts for acute myocardial ischemia and reperfusion injury. Circulation. 2002;106:1543–1549.
   PubMed Web of Science ®Google Scholar
• Donato M, D’Annunzio V, Buchholz B, et al. Role of matrix metalloproteinase-2 in the cardioprotective effect of ischaemic postconditioning. Exp Physiol. 2010;95:274–281.
   Web of Science ®Google Scholar
• Cheung PY, Sawicki G, Wozniak M, Wang W, Radomski MW, Schulz R. Matrix metalloproteinase-2 contributes to ischemia-reperfusion injury in the heart. Circulation. 2000;101:1833–1839.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar