Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-28T00:59:31.547Z Has data issue: false hasContentIssue false
  • English
  • Français

Diabetes-Induced Alterations in the Extracellular Matrix and Their Impact on Myocardial Function

Published online by Cambridge University Press:  05 January 2012

Brittany Law ,
Vennece Fowlkes ,
Jack G. Goldsmith ,
Wayne Carver  and
Edie C. Goldsmith
Brittany Law
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, 6439 Garners Ferry Rd., Columbia, SC 29209, USA
Vennece Fowlkes
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, 6439 Garners Ferry Rd., Columbia, SC 29209, USA
Jack G. Goldsmith
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, 6439 Garners Ferry Rd., Columbia, SC 29209, USA
Wayne Carver
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, 6439 Garners Ferry Rd., Columbia, SC 29209, USA
Edie C. Goldsmith*
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, 6439 Garners Ferry Rd., Columbia, SC 29209, USA
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

Diabetes is an increasing public health problem that is expected to escalate in the future due to the growing incidence of obesity in the western world. While this disease is well known for its devastating effects on the kidneys and vascular system, diabetic individuals can develop cardiac dysfunction, termed diabetic cardiomyopathy, in the absence of other cardiovascular risk factors such as hypertension or atherosclerosis. While much effort has gone into understanding the effects of elevated glucose or altered insulin sensitivity on cellular components within the heart, significant changes in the cardiac extracellular matrix (ECM) have also been noted. In this review article we highlight what is currently known regarding the effects diabetes has on both the expression and chemical modification of proteins within the ECM and how the fibrotic response often observed as a consequence of this disease can contribute to reduced cardiac function.

Keywords

diabetesextracellular matrixheartadvanced glycation end products (AGE)fibrosismyofibroblast
Type
Review Article
Information
Microscopy and Microanalysis , Volume 18 , Issue 1 , February 2012 , pp. 22 - 34
Copyright
Copyright © Microscopy Society of America 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

1

These authors contributed equally to this work.

References

REFERENCES

Aasum, E., Hafstad, A.D., Severson, D.L. & Larsen, T.S. (2003). Age-dependent changes in metabolism, contractile function and ischemic sensitivity in hearts from db/db mice. Diabetes 52, 434–441.CrossRefGoogle ScholarPubMed
Abbate, M., Zoja, C. & Remuzzi, G. (2006). How does proteinuria cause progressive renal damage? J Am Soc Nephrol 17, 2974–2984.CrossRefGoogle ScholarPubMed
Anavekar, N.S., McMurray, J.J., Velazquez, E.J., Solomon, S.D., Kober, L., Rouleau, J.L., White, H.D., Nordlander, R., Maggioni, A., Dickstein, K., Zelenkofske, S., Leimberger, J.D., Califf, R.M. & Pfeffer, M.A. (2004). Relation between renal dysfunction and cardiovascular outcomes after myocardial infarction. N Engl J Med 351, 1285–1295.CrossRefGoogle ScholarPubMed
Aneja, A., Tang, W.H.W., Bansilal, S., Garcis, M.J. & Farkouh, M.E. (2008). Diabetic cardiomyopathy: Insights into pathogenesis, diagnostic challenges and therapeutic options. Amer J Med 121, 748–757.Google Scholar
Ares-Carrasco, A., Picatoste, B., Benito-Martin, A., Zubiri, I., Sanz, A.B., Sanchez-Nino, M.D., Ortiz, A., Egido, J., Tunon, J. & Lorenzo, O. (2009). Myocardial fibrosis and apoptosis, but not inflammation, are present in long-term experimental diabetes. Am J Physiol Heart Circ Physiol 297, H2109–H2119.Google Scholar
Aronson, D. (2003). Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes. J Hypertens 21, 3–12.CrossRefGoogle ScholarPubMed
Banerjee, I., Fuseler, J.W., Price, R.L., Borg, T.K. & Baudino, T.A. (2007). Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol 293, H1883–H1891.Google Scholar
Barouch, L.A., Berkowitz, D.E., Harrison, R.W., O'Donnell, C.P. & Hare, J.M. (2003). Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation 108, 754–759.CrossRefGoogle ScholarPubMed
Basta, G., Lazzerini, G., Massaro, M., Simoncini, T., Tanganelli, P., Fu, C., Kislinger, T., Stern, D.M., Schmidt, A.M. & DeCaterina, R. (2002). Advanced glycation end products activate endothelium through signal-transduction receptor RAGE: A mechanism for amplification of inflammatory responses. Circulation 105, 816–822.CrossRefGoogle Scholar
Baynes, J.W. (2001). The role of AGEs in aging: Causation or correlation. Exp Gerontol 36, 1527–1537.Google Scholar
Belke, D.D., Larsen, T.S. & Severson, D.L. (2001). Cardiac function in perfused hearts from diabetic mice. Adv Exp Med Biol 498, 241–245.CrossRefGoogle ScholarPubMed
Bidasee, K.R., Nallani, K., Henry, B., Dincer, U.D. & Besch, H.R. Jr. (2003). Chronic diabetes alters function and expression of ryanodine receptor calcium-release channels in rat hearts. Mol Cell Biochem 249, 113–123.CrossRefGoogle ScholarPubMed
Biemel, K.M., Friedl, D.A. & Lederer, M.O. (2002). Identification and quantification of major maillard cross-links in human serum albumin and lens protein. J Biol Chem 277, 24907–24915.Google Scholar
Bierhaus, A., Humpert, P.M., Morcos, M., Wendt, T., Chavakis, T., Arnold, B., Stern, D.M. & Nawroth, P.P. (2006). Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83, 876–886.CrossRefGoogle Scholar
Bierhaus, A., Stern, D.M. & Nawroth, P.P. (2005). RAGE in inflammation: A new therapeutic target? Curr Opin Invest Drugs 7, 985–991.Google Scholar
Bishop, J.E. & Laurent, G.J. (1995). Collagen turnover and its regulation in the normal and hypertrophying heart. Eur Heart J 16, 38–44.Google Scholar
Bochaton-Piallat, M.L., Kapetanios, A.D., Donati, G., Redard, M., Gabbiani, G. & Pournaras, C.J. (2000). TGF-b1, TGF-b receptor II and ED-A fibronectin expression in myofibroblast of vitreoretinopathy. Invest Ophthalmol Vis Sci 41, 2336–2342.Google Scholar
Booth, A.A., Khalifah, R.G., Todd, P. & Hudson, B.G. (1997). In vitro kinetic studies of formation of antigenic advanced glycation end products (AGEs). J Biol Chem 272, 5430–5437.CrossRefGoogle ScholarPubMed
Boudina, S. & Abel, E.D. (2010). Diabetic cardiomyopathy: Causes and effects. Rev Endocr Metab Disord 11, 31–39.CrossRefGoogle Scholar
Bouguerra, S., Benazzoug, Y., Bekkhoucha, F. & Bourdillon, M.C. (2004). Effect of high glucose concentration on collagen synthesis and cholesterol level in the phenotypic modulation of aortic cultured smooth muscle cells of sand rat (Psammomys obesus). Experimental Diab Res 5, 227–235.CrossRefGoogle Scholar
Brem, H. & Tomic-Canic, M. (2007). Cellular and molecular basis of wound healing in diabetes. J Clin Invest 117, 1219–1222.CrossRefGoogle ScholarPubMed
Brown, R.D., Ambler, S.K., Mitchell, M.D. & Long, C.S. (2005). The cardiac fibroblast: Therapeutic target in myocardial remodeling and failure. Annu Rev Pharmacol Toxicol 45, 657–687.Google Scholar
Brownlee, M. (1995). Advanced protein glycosylation in diabetes and aging. Ann Rev Med 46, 223–234.CrossRefGoogle Scholar
Brownlee, M., Vlassara, H. & Cerami, A. (1985). Nonenzymatic glycosylation products on collagen covalently trap low-density lipoprotein. Diabetes 34, 938–941.CrossRefGoogle ScholarPubMed
Candido, R., Forbes, J.M., Thomas, M.C., Thallas, V., Dean, R.G., Burns, W.C., Tikellis, C., Ritchie, R.H., Twigg, S.M., Cooper, M.E. & Burrell, L.M. (2003). A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res 92, 785–792.Google Scholar
Cassiman, D., Libbrecht, L., Desmet, V., Denef, C. & Roskams, T. (2002). Hepatic stellate cell/myofibroblast subpopulations in fibrotic human and rat livers. J Hepatol 36, 200–209.CrossRefGoogle ScholarPubMed
Caulfield, J.B. & Borg, T.K. (1979). The collagen network of the heart. Lab Invest 40, 364–372.Google Scholar
Chang, H.Y., Chi, J.T., Dudoit, S., Bondre, C., van de Rijn, M., Botstein, D. & Brown, P.O. (2002). Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99, 12877–12882.CrossRefGoogle ScholarPubMed
Dahl-Jørgensen, K., Larsen, J.R. & Hanssen, K.F. (2005). Atherosclerosis in childhood and adolescent type 1 diabetes: Early disease, early treatment? Diabetologia 48, 1445–1453.Google Scholar
Dai, Z., Wang, B., Sun, G., Xingjun, F., Anderson, V.E. & Monnier, V.M. (2008). Identification of glucose-derived cross-linking sites in ribonuclease A. J Proteome Res 7, 2756–2768.Google Scholar
Dalla Vestra, M., Saller, A., Bortoloso, E., Mauer, M. & Floretto, P. (2000). Structural involvement in type I and type 2 diabetic nephropathy. Diabetes Metab 4, 8–14.Google Scholar
Darby, I.A., Bisucci, T., Hewitson, T.D. & MacLellan, D.G. (1997). Apoptosis is increased in a model of diabetes-impaired wound healing in genetically diabetic mice. Int J Biochem Cell Biol 29, 191–200.Google Scholar
Depre, C., Young, M.E., Ying, J., Ahuja, H.S., Han, Q., Garza, N., Davies, P.J. & Taegtmeyer, H. (2000). Streptozotocin-induced changes in cardiac gene expression in the absence of severe contractile dysfunction. J Mol Cell Cardiol 32, 985–996.Google Scholar
Desmoulière, A., Chaponnier, C. & Gabbiani, G. (2005). Tissue repair, contraction, and the myofibroblast. Wound Repair Regen 13, 7–12.Google Scholar
Dhalla, N.S., Pierce, G.N., Innes, I.R. & Beamish, R.E. (1985). Pathogenesis of cardiac dysfunction in diabetes mellitus. Can J Cardiol 1, 263–281.Google ScholarPubMed
Dobler, D., Ahmed, N., Song, L., Eboigbodin, K.E. & Thornalley, P.J. (2006). Increased dicarbonyl metabolism in endothelial cells in hyperglycemia induces anoikis and impairs angiogenesis by RGD and GFOGER motif modification. Diabetes 55, 1961–1969.CrossRefGoogle ScholarPubMed
Du, Y.S., Zhu, H., Fu, J., Yan, S.F., Roher, A., Tourtellotte, W.W., Rajavashisth, T., Chen, X., Godman, G.C., Stern, D. & Schmidt, A.M. (1997). Amyloid-beta peptide-receptor for advanced glycation endproduct interaction elicits neuronal expression of macrophage-colony stimulating factor: A proinflammatory pathway in Alzheimer's disease. Proc Natl Acad Sci USA 94, 5296–5301.Google Scholar
Dunn, J.A., McCance, D.R., Thorpe, S.R., Lyons, T.J. & Baynes, J.W. (1991). Age-dependent accumulation of Nɛ-(carboxymethyl)hydroxylysine in human skin collagen. Biochemistry 30, 1205–1210.CrossRefGoogle Scholar
Dunn, J.A., Patrick, J.S., Thorpe, S.R. & Baynes, J.W. (1989). Oxidation of glycated proteins: Age-dependent accumulation of Nɛ-(carboxymethyl)lysine in len proteins. Biochemistry 28, 9644–9648.CrossRefGoogle Scholar
Eghbali, M. & Weber, K.T. (1990). Collagen and the myocardium: Fibrillar structure, biosynthesis and degradation in relation to hypertrophy and its regression. Mol Cell Biochem 96, 1–14.CrossRefGoogle ScholarPubMed
Falk, R.J., Scheinman, J.I., Mauer, S.M. & Michael, A.F. (1983). Polyantigenic expansion of basement membrane constituents in diabetic nephropathy. Diabetes 32, 34–39.CrossRefGoogle ScholarPubMed
Fathima, N.N., Madhan, B., Rao, J.R., Nair, B.N. & Ramasami, T. (2004). Interaction of aAldehydes with collagen: Effect on thermal, enzymatic, and conformational stability. Int J Biol Macromol 34, 241–247.CrossRefGoogle ScholarPubMed
Ferreira, A.E.N., Ponces Freire, A.M.J. & Voit, E.O. (2003). A quantitative model of the generation of Nɛ-(carboxylmethyl)lysine in the maillard reaction between collagen and glucose. Biochem J 376, 109–121.CrossRefGoogle Scholar
Frey, E.B., Degenhardt, T.P., Thorpe, S.R. & Baynes, J.W. (1998). Role of the Maillard reaction in aging of tissue proteins. J Biol Chem 273, 18714–18719.CrossRefGoogle Scholar
Frustaci, A., Kajstura, J., Chimenti, C., Jakoniuk, I., Leri, A., Maseri, A., Nadal-Ginard, B. & Anversa, P. (2000). Myocardial cell death in human diabetes. Circ Res 87, 1123–1132.CrossRefGoogle ScholarPubMed
Gabbiani, G. (2003). The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200, 500–503.CrossRefGoogle ScholarPubMed
Gao, X., He, X., Luo, B., Peng, L., Lin, J. & Zuo, Z. (2009). Angiotensin II increases collagen I expression via transforming growth factor-beta1 and extracellular signal-regulated kinase in cardiac fibroblasts. Eur J Pharmacol 606, 115–120.Google Scholar
Gilbert, R.E. & Cooper, M.E. (1999). The tubulointerstitium in progressive diabetic kidney disease: More than an aftermath of glomerular injury? Kidney Int 56, 1627–1637.Google Scholar
Goh, S.Y. & Cooper, M.E. (2008). The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 93, 1143–1152.CrossRefGoogle ScholarPubMed
Goldin, A., Beckman, J.A., Schmidt, A.M. & Creager, M.A. (2006). Advanced glycation end products: Sparking the development of diabetic vascular injury. Circulation 114, 597–605.Google Scholar
Gratzer, P.F., Santerre, J.P. & Lee, J.M. (2006). The effect of chemical modification of amino acid side-chains on collagen degradation by enzymes. J Biomed Mater Res Part B 81B, 1–11.Google Scholar
Greenhalgh, D.G., Sprugel, K.H., Murray, M.J. & Ross, R. (1990). PDGF and FGF stimulate wound healing in the genetically diabetic mouse. Am J Pathol 136, 1235–1246.Google Scholar
Gress, T.M., Menke, A., Bachem, M., Müller-Pillasch, F., Ellenrieder, V., Weidenbach, H., Wagner, M. & Adler, G. (1998). Role of extracellular matrix in pancreatic diseases. Digestion 59, 625–637.Google Scholar
Halse, R., Pearson, S.L., McCormack, J.G., Yeaman, S.J. & Taylor, R. (2001). Effects of tumor necrosis factor-alpha on insulin action in cultured human muscle cells. Diabetes 50, 1102–1109.CrossRefGoogle ScholarPubMed
Hamada, Y., Araki, N., Koh, N., Horiuchi, S. & Hotta, N. (1996). Rapid formation of advanced glycation end products by intermediate metabolites of glycolytic pathway and polyol pathway. Biochem Biophys Res Commun 228, 539–543.Google Scholar
Hartog, J.W., Voors, A.A., Bakker, S.J., Smit, A.J. & van Veldhuisen, D.J. (2007). Advance glycation end-products (AGEs) and heart failure: Pathophysiology and clinical implications. Eur J Heart Fail 9, 1146–1155.CrossRefGoogle ScholarPubMed
Hayden, M.R., Patel, K., Habibi, J., Gupta, D., Tekwani, S., Whaley-Connell, A. & Sowers, J. (2008). Attenuation of endocrine-exocrine pancreatic communication in type 2 diabetes: Pancreatic extracellular matrix ultrastructural abnormalities. J Cardiometab Syndr 4, 234–243.CrossRefGoogle Scholar
Heickendorff, L., Ledet, T. & Rasmussen, L.M. (1994). Glycosaminoglycans in the human aorta in diabetes-mellitus—A study of tunica media from areas with and without atherosclerotic plaque. Diabetologia 37, 286–292.Google Scholar
Herrmann, K.L., McCulloch, A.D. & Omens, J.H. (2003). Glycated collagen cross-linking alters cardiac mechanics in volume-overload hypertrophy. Am J Physiol Heart Circ Physiol 284, H1277–H1284.CrossRefGoogle ScholarPubMed
Hinz, B. (2007). Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127, 526–537.CrossRefGoogle ScholarPubMed
Hinz, B., Phan, S.H., Thannickal, V.J., Galli, A., Bochaton-Piallat, M.L. & Gabbiani, G. (2007). The myofibroblast: One function, multiple origins. Am J Pathol 170, 1807–1816.Google Scholar
Hofmann, M.A., Drury, S., Fu, C., Wu, Q., Taguchi, A., Lu, Y., Avila, C., Kambham, N., Slattery, T., Beach, D., McClary, J., Nagashima, M., Morser, J., Bierhaus, A., Neurath, M., Nawroth, P., Stern, D. & Schmidt, A.M. (1999). RAGE mediates a novel proinflammatory axis: The cell surface receptor for S100/calgranulin polypeptides. Cell 97, 889–901.CrossRefGoogle Scholar
Ikeda, S., Makino, H., Haramoto, T., Shikata, K., Kumagai, I. & Ota, Z. (1991). Changes in glomerular extracellular matrices components in diabetic nephropathy. J Diabetes Complicat 5, 186–188.CrossRefGoogle ScholarPubMed
Jackson, C.V., McGrath, G.M., Tahiliani, A.G., Vadlamudi, R.V. & McNeill, J.H. (1985). A functional and ultrastructural analysis of experimental diabetic rat myocardium. Manifestation of a cardiomyopathy. Diabetes 34, 876–883.CrossRefGoogle ScholarPubMed
Jaffe, A.S., Spadaro, J.J., Schechtman, K., Roberts, R., Geitman, E.M. & Sobel, B.E. (1984). Increased congestive heart failure after myocardial infarction of modest extent in patients with diabetes mellitus. Am Heart J 108, 31–37.CrossRefGoogle ScholarPubMed
Järvisalo, M.J., Jartti, L., Näntö-Salonen, K., Irjala, K., Rönnemaa, T., Hartiala, J.J., Celermajer, D.S. & Raitakari, O.T. (2001). Increased aortic intima-media thickness: A marker of preclinical atherosclerosis in high-risk children. Circulation 104, 2943–2947.CrossRefGoogle ScholarPubMed
Jefferson, J.A., Shankland, S.J. & Pichler, R.H. (2008). Proteinuria in diabetic kidney disease: A mechanistic viewpoint. Kidney Int 74, 22–36.CrossRefGoogle ScholarPubMed
Kim, J.K., Kim, Y.J., Fillmore, J.J., Chen, Y., Moore, I., Lee, J., Yuan, M., Li, Z.W., Karin, M., Perret, P., Shoelson, S.E. & Shulman, G.I. (2001). Prevention of fat-induced insulin resistance by salicylate. J Clin Invest 108, 437–446.Google Scholar
Kiryu, K., Morita, H., Fujita, Y., Kawasumi, M., Shinzato, T., Tsuruta, Y., Nakai, S. & Maeda, K. (1994). Phenotypic expressions of type I III, IV, V and VI collagens in patients with diabetic nephropathy: Immunohistochemical comparison between HD and non-HD patients. Nippon Jinzo Gakkai Shi 36, 365–373.Google Scholar
Klein, B.E., Klein, R., McBride, P.E., Cruickshanks, K.J., Palta, M., Knudtson, M.D., Moss, S.E. & Reinke, J.O. (2004). Cardiovascular disease, mortality and retinal microvascular characteristics in type 1 diabetes: Wisconsin epidemiological study of diabetic retinopathy. Arch Intern Med 164, 1917–1924.CrossRefGoogle ScholarPubMed
Ko, S.H., Hong, O.K., Kim, J.W., Ahn, Y.B., Song, K.H., Cha, B.Y., Son, H.Y., Kim, M.J., Jeong, I.K. & Yoon, K.H. (2006). High glucose increases extracellular matrix production in pancreatic stellate cells by activating the renin-angiotensin system. J Cell Biochem 98, 343–355.Google Scholar
Krenning, G., Zeisberg, E.M. & Kalluri, R. (2010). The origin of fibroblasts and mechanism of cardiac fibrosis. J Cell Physiol 225, 631–637.CrossRefGoogle ScholarPubMed
Kuwahara, F., Kai, H., Tokuda, K., Kai, M., Takeshita, A., Egashira, K. & Imaizumi, T. (2002). Transforming growth factor-beta function blocking prevents myocardial fibrosis and diastolic dysfunction in pressure-overloaded rats. Circulation 106, 130–135.CrossRefGoogle ScholarPubMed
Kwan, C.Y., Wang, R.R.J., Beazley, J.S. & Lee, R.M.K.W. (1988). Alterations of elastin and elastase-like activities in aortae of diabetic rats. Biochim Biophys Acta 967, 322–325.CrossRefGoogle ScholarPubMed
Lastra, G. & Manrique, C. (2007). The expanding role of oxidative stress, rennin angiotensin system, and β-cell dysfunction in the cardiometabolic syndrome and type 2 diabetes mellitus. Antioxid Redox Sign 7, 943–954.Google Scholar
Lawlor, M.A. & Alessi, D.R. (2001). PKB/Akt: A key mediator of cell proliferation, survival and insulin responses? J Cell Sci 114, 2903–2910.CrossRefGoogle ScholarPubMed
Leask, A. (2008). Targeting the TGFbeta, endothelin-1 and CCN2 axis to combat fibrosis in scleroderma. Cell Signal 20, 1409–1414.Google Scholar
Leask, A. (2010). Potential therapeutic targets for cardiac fibrosis: TGFbeta, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ Res 106, 1675–1680.CrossRefGoogle ScholarPubMed
Lehto, S., Pyorala, K., Miettinen, H., Ronnemaa, T., Palomaki, P., Tuomilehto, J. & Laakso, M. (1994). Myocardial infarct size and mortality in patients with non-insulin-dependent diabetes mellitus. J Intern Med 236, 291–297.CrossRefGoogle ScholarPubMed
Levinthal, G. & Tavill, A.S. (1999). Liver disease and diabetes mellitus. Clin Diabetes 17, 73–93.Google Scholar
Li, J.H., Wang, W., Huang, X.R., Oldfield, M., Schmidt, A.M., Cooper, M.E. & Lan, H.Y. (2004). Advanced glycation end products induce tubular epithelial-myofibroblast transition through the RAGE-ERK1/2 MAP kinase signaling pathway. Am J Pathol 164, 1389–1397.CrossRefGoogle ScholarPubMed
Malhotra, A., Penpargkul, S., Fein, F.S., Sonnenblick, E.H. & Scheuer, J. (1981). The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ Res 49, 1243–1250.Google Scholar
Mason, R.M. & Wahab, N.A. (2003). Extracellular matrix metabolism in diabetic nephropathy. J Am Soc Nephrol 14, 1358–1373.Google Scholar
McDonald, T.O., Gerrity, R.G., Jen, C., Chen, H.J., Wark, K. & Wight, T.N. (2007). Diabetes and arterial extracellular matrix changes in a porcine model of atherosclerosis. J Histochem Cytochem 55, 1149–1157.CrossRefGoogle Scholar
Miyazato, J., Horio, T., Takiuchi, S., Kamide, K., Sasaki, O., Nakamura, S., Nakahama, H., Inenaga, T., Takishita, S. & Kawano, Y. (2005). Left ventricular diastolic dysfunction in patients with chronic renal failure: Impact of diabetes mellitus. Diabetes Med 22, 730–736.Google Scholar
Nathan, D.M., Cleary, P.A., Backlund, J.Y., Genuth, S.M., Lachin, J.M., Orchard, T.J., Raskin, P. & Zinman, B. (2005). Diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) study research group intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 353, 2643–2653.Google Scholar
Naugle, J.E., Olson, E.R., Zhang, X., Mase, S.E., Pilati, C.F., Maron, M.B., Folkesson, H.G., Horne, W.I., Doane, K.J. & Meszaros, J.G. (2006). Type VI collagen induces cardiac myofibroblast differentiation: Implications for postinfarction remodeling. Am J Physiol Heart Circ Physiol 290, H323–330.Google Scholar
Neumann, S., Huse, K., Semrau, R., Diegeler, A., Gebhardt, R., Buniatian, G.H. & Scholz, G.H. (2002). Aldosterone and D-glucose stimulate the proliferation of human cardiac myofibroblasts in vitro. Hypertension 39, 756–760.Google Scholar
Nguyen, T.Q., Chon, H., van Nieuwenhoven, F.A., Braam, B., Verhaar, M.C. & Goldschmeding, R. (2006). Myofibroblast progenitor cells are increased in number in patients with type 1 diabetes and express less bone morphogenetic protein 6: A novel clue to adverse tissue remodelling? Diabetologia 49, 1039–1048.CrossRefGoogle ScholarPubMed
Nichols, G.A., Guillon, C.M., Koro, C.E., Ephross, S.A. & Brown, J.B. (2004). The incidence of congestive heart failure in type 2 diabetes: An update. Diabetes Care 27, 1879–1884.CrossRefGoogle ScholarPubMed
Nielsen, J.M., Kristiansen, S.B., Norregaard, R., Andersen, C.L., Denner, L., Nielsen, T.T., Flyvbjerg, A. & Botker, H.E. (2009). Blockage of receptor for advanced glycation end products prevents development of cardiac dysfunction in db/db type 2 diabetic mice. Eur J Heart Fail 11, 638–647.CrossRefGoogle ScholarPubMed
Nishida, M., Onohara, N., Sato, Y., Suda, R., Ogushi, M., Tanabe, S., Inoue, R., Mori, Y. & Kurose, H. (2007). Galpha12/13-mediated up-regulation of TRPC6 negatively regulates endothelin-1-induced cardiac myofibroblast formation and collagen synthesis through nuclear factor of activated T cells activation. J Biol Chem 282, 23117–23128.CrossRefGoogle ScholarPubMed
Norton, G.R., Candy, G. & Woodiwiss, A.J. (1996). Aminoguanidine prevents the decreased myocardial compliance produced by streptozotocin-induced diabetes mellitus in rats. Circulation 93, 1905–1912.CrossRefGoogle ScholarPubMed
Oldfield, M.D., Bach, L.A., Forbes, J.M., Nikolic-Paterson, D., McRobert, A., Thallas, V., Atkins, R.C., Osicka, T., Jerums, G. & Cooper, M.E. (2001). Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 108, 1853–1863.Google Scholar
Orchard, T.J., Olson, J.C., Erbey, J.R., Williams, K., Forrest, K.Y., Smithline Kinder, L., Ellis, D. & Becker, D.J. (2003). Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year follow-up data from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care 26, 1374–1379.Google Scholar
Osterby, R., Tapia, J., Nyberg, G., Tencer, J., Willner, J., Rippe, B. & Torffvit, O. (2001). Renal structures in type 2 diabetic patients with elevated albumin excretion rate. APMIS 109, 751–761.CrossRefGoogle ScholarPubMed
Picano, E. (2003). Diabetic cardiomyopathy. The importance of being earliest. J Am Coll Cardiol 42, 454–457.Google Scholar
Poirier, P., Bogaty, P., Garneau, C., Marois, L. & Dumesnil, J.G. (2001). Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: Importance of maneuvers in echocardiographic screeing for preclinical diabetic cardiomyopathy. Diabetes Care 24, 5–10.CrossRefGoogle Scholar
Poornima, I.G., Parikh, P. & Shannon, R.P. (2006). Diabetic cardiomyopathy, the search for a unifying hypothesis. Circ Res 98, 596–605.Google Scholar
Porter, K.E. & Turner, N.A. (2009). Cardiac fibroblasts: At the heart of myocardial remodeling. Pharmacol Ther 123, 255–278.CrossRefGoogle ScholarPubMed
Regan, T.J., Wu, C.F. & Yeh, C. (1981). Myocardial composition and function in diabetes—The effects of chronic insulin use. Circ Res 49, 1268–1277.CrossRefGoogle ScholarPubMed
Retnakaran, R. & Zinman, B. (2008). Type 1 diabetes, hyperglycaemia, and the heart. Lancet 371, 1790–1799.Google Scholar
Rubler, S., Dlugash, J., Yuceoglu, Y.Z., Kumral, T., Branwood, A.W. & Grishman, A. (1972). New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30, 595–602.CrossRefGoogle ScholarPubMed
Schäfer, S., Huber, J., Wihler, C., Rütten, H., Busch, A.E. & Linz, W. (2006). Impaired left ventricular relaxation in type 2 diabetic rats is related to myocardial accumulation of N(epsilon)-(carboxymethyl) lysine. Eur J Heart Fail 8, 2–6.CrossRefGoogle Scholar
Scognamiglio, R., Avogaro, A., Negut, C., Piccolotto, R., Vigili de Kreutzenberg, S. & Tiengo, A. (2004). Early myocardial dysfunction in the diabetic heart: Current research and clinical applications. Am J Cardiol 93, 17A–20A.CrossRefGoogle ScholarPubMed
Sell, D.R., Biemel, K.M., Reihl, O., Lederer, M.O., Strauch, C.M. & Monnier, V.M. (2005). Glucosepane is a major protein cross-link of the senescent human extracellular matrix: Relationship with diabetes. J Biol Chem 280, 12310–12315.CrossRefGoogle Scholar
Sell, D.R., Lane, M.A., Johnson, W.A., Masoro, E.J., Mock, O.B., Reiser, K.M., Fogarty, J.F., Cutler, R.G., Ingram, D.K., Roth, G.S. & Monnier, V.M. (1996). Longevity and the genetic determination of collagen glycoxidation kinetics in mammalian senescence. Proc Natl Acad Sci USA 93, 485–490.Google Scholar
Seneviratne, B. (1977). Diabetic cardiomyopathy: The preclinical phase. Br Med J 1, 1444–1446.Google Scholar
Shamhart, P.E., Luther, D.J., Hodson, B.R., Koshy, J.C., Ohanyan, V. & Meszaros, J.G. (2009). Impact of type 1 diabetes on cardiac fibroblast activation enchanced cell cycle progression and reduced myofibroblast content in diabetic myocardium. Am J Physiol Endocrinol Metab 297, E1147–E1153.Google Scholar
Shapiro, L., Howat, A. & Calter, M. (1981a). Left ventricular function in diabetes mellitus—I. Methodology and prevalence and spectrum of abnormalities. Br Heart J 45, 122–128.Google Scholar
Shapiro, L., Leatherdale, B. & MacKinnon, J. (1981b). Left ventricular function in diabetes mellitus—II. Relation between clinical features and left ventricular function. Br Heart J 45, 129–132.CrossRefGoogle ScholarPubMed
Shehadeh, A. & Regan, T.J. (1995). Cardiac consequences of diabetes mellitus. Clin Cardiol 18, 301–305.Google Scholar
Shimizu, M., Umeda, K. & Sugihara, N. (1993). Collagen remodelling in myocardia of patients with diabetes. J Clin Pathol 46, 32–36.Google Scholar
Shi-Wen, X., Chen, Y., Denton, C.P., Eastwood, M., Renzoni, E.A., Bou-Gharios, G., Pearson, J.D., Dashwood, M., du Bois, R.M., Black, C.M., Leask, A. & Abraham, D.J. (2004). Endothelin-1 promotes myofibroblast induction through the ETA receptor via a rac/phosphoinositide 3-kinase/Akt-dependent pathway and is essential for the enhanced contractile phenotype of fibrotic fibroblasts. Mol Biol Cell 15, 2707–2719.Google Scholar
Shulman, G.I. (2000). Cellular mechanisms of insulin resistance. J Clin Invest 106, 171–176.Google Scholar
Siperstein, M.D., Unger, R.H. & Madison, L.L. (1968). Studies of muscle capillary basement membrane in normal subjects, diabetic, and prediabetic patients. J Clin Invest 47, 1973–1999.Google Scholar
Smit, A.J. & Garrits, E.G. (2010). Skin autofluorescence as a measure of advanced glycation endproduct deposition: A novel risk marker in chronic kidney disease. Curr Opin Nephrol Hypertens 19, 527–533.Google Scholar
Song, W. & Ergul, A. (2006). Type-2 diabetes-induced changes in vascular extracellular matrix gene expression: Relation to vessel size. Cardiovasc Diabetol 5, 3.Google Scholar
Spiro, M.J. & Crowley, T.J. (1993). Increased rat myocardial type VI collagen in diabetes mellitus and hypertension. Diabetologia 36, 93–98.Google Scholar
Steffes, M.W., Osterby, R., Chavers, B. & Mauer, S.M. (1989). Mesangial expansion as a central mechanism for loss of kidney function in diabetic patients. Diabetes 38, 1077–1081.Google Scholar
Tabas, I., Williams, K.J. & Boren, J. (2007). Subendothelial lipoprotein retention as the initiating process in atherosclerosis: Update and therapeutic implications. Circulation 116, 1832–1844.Google Scholar
Tahiliani, A.G. & McNeill, J.H. (1986). Diabetes-induced abnormalities in the myocardium. Life Sci 38, 959–974.Google Scholar
Targher, G. (2004). Associations between liver histology and early carotid atherosclerosis in subjects with nonalcoholic fatty liver disease. Hepatology 42, 974–975.Google Scholar
Targher, G., Bertolini, L., Padovani, R., Poli, F., Scala, L., Tessari, R., Zenari, L. & Falezza, G. (2005). Increased prevalence of cardiovascular disease in Type 2 diabetic patients with non-alcoholic fatty liver disease. Diabet Med 4, 403–409.Google Scholar
Tarnow, L., Rossing, P., Gall, M.A., Nielsen, F.S. & Parving, H.H. (1994). Prevalence of arterial hypertension in diabetic patients before and after the Jnc-V. Diabetes Care 17, 1247–1251.Google Scholar
Tikellis, C., Thomas, M.C., Harcourt, B.E., Coughman, M.T., Pete, J., Bialkowski, K., Tan, A., Bierhaus, A., Cooper, M.E. & Forbes, J.M. (2008). Cardiac inflammation associated with a western diet is mediated via activation of RAGE by AGEs. Am J Physiol Endocrinol Metab 295, E323–E330.Google Scholar
Ulrich, P. & Cerami, A. (2001). Protein glycation, diabetes, and aging. Rec Prog Horm Res 56, 1–21.CrossRefGoogle Scholar
Vadlamudi, R.V. & McNeill, J.H. (1983). Effect of alloxan- and streptozotocin-induced diabetes on isolated heart responsiveness to carbachol. J Pharmacol Exp Ther 225, 410–415.Google Scholar
van den Bergh, A., Flameng, W. & Herijgers, P. (2006). Type II diabetic mice exhibit contractile dysfunction but maintain cardiac output by favourable loading conditions. Eur J Heart Fail 8, 777–783.CrossRefGoogle ScholarPubMed
van Heerebeek, L., Hamdani, N., Handoko, M.L., Falcao-Pires, I., Musters, R.J., Kupreishvili, K., Ijsselmuiden, A.J., Schalkwijk, C.G., Bronzwaer, J.G., Diamant, M., Borbély, A., van der Velden, J., Stienen, G.J., Laarman, G.J., Niessen, H.W. & Paulus, W.J. (2008). Diastolic stiffness of the failing diabetic heart: Importance of fibrosis, advanced glycation end products and myocyte resting tension. Circulation 117, 43–51.CrossRefGoogle ScholarPubMed
van Hoeven, K.H. & Factor, S.M. (1990). A comparison of the pathological spectrum of hypertensive, diabetic, and hypertensive-diabetic heart disease. Circulation 82, 848–855.Google Scholar
Vernier, R.L., Steffes, M.W., Sisson-Ross, S. & Mauer, S.M. (1992). Heparan sulfate proteoglycans in the glomerular basement membrane in type 1 diabetes mellitus. Kidney Int 41, 1070–1080.Google Scholar
Verzijl, N., DeGroot, J., Zaken, C.B., Braun-Benjamin, O., Maroudas, A., Bank, R.A., Mizrahi, J., Schalkwijk, C.G., Thorpe, S.R., Baynes, J.W., Bijlsma, J.W.J., Lafeber, F.P.J.G. & TeKoppele, J.M. (2002). Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage. Arthrit Rheumat 46, 114–123.Google Scholar
Villanova, N., Moscatiello, S., Ramilli, S., Bugianesi, E., Magalotti, D. & Vanni, E. (2005). Endothelial dysfunction and cardiovascular risk profile in non-alcoholic fatty liver disease. Hepatology 42, 473–478.Google Scholar
Volzke, H., Robinson, D.M., Kleine, V., Deutscher, R., Hoffmann, W. & Ludemann, J. (2005). Hepatic steatosis is associated with an increased risk of carotid atherosclerosis. World J Gastronterol 11, 1848–1853.Google Scholar
Walshe, R., Esser, P., Wiedemann, P. & Heimann, K. (1992). Proliferative retinal diseases: Myofibroblasts cause chronic vitreoretinal traction. Br J Ophthalmol 76, 550–552.Google Scholar
Wang, S.L., Head, J., Stevens, L. & Fuller, J.H. (1996). Excess mortality and its relation to hypertension and proteinuria in diabetic patients. The World Health Organization multinational study of vascular disease in diabetes. Diabetes Care 19, 305–312.Google Scholar
Yamada, H., Sasaki, T., Niwa, S., Tohoru, O., Murata, M., Kawakami, T. & Aimoto, S. (2004). Intact glycation end products containing carboxymethyl-lysine and glyoxal lysine dimer obtained from synthetic collagen model peptide. Bioorg Med Chem Lett 14, 5677–5680.Google Scholar
Yan, S.D., Zhu, H., Zhu, A., Golabek, A., Du, H., Roher, A., Yu, J., Soto, C., Schmidt, A.M., Stern, D. & Kindy, M. (2000). Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med 6, 643–651.Google Scholar
Yang, F., Chung, A.C., Huang, X.R. & Lan, H.Y. (2009). Angiotensin II induces connective tissue growth factor and collagen I expression via transforming growth factor-beta-dependent and -independent Smad pathways: The role of Smad3. Hypertension 54, 877–884.Google Scholar
Yang, J. & Liu, Y. (2001). Dissection of key events in tubular epithelial to myofibroblast transition and its implications in renal interstitial fibrosis. Am J Pathol 159, 1465–1475.CrossRefGoogle ScholarPubMed
Yoshikawa, H., Kihara, Y., Taguchi, M., Yamaguchi, T., Nakamura, H. & Otsuki, M. (2002). Role of TGF-β1 in the development of pancreatic fibrosis in Otsuka Long–Evans Tokushima fatty rats. Am J Physiol Gastrointest Liver Physiol 282, G549–G555.Google Scholar
Yuen, A., Laschinger, C., Talior, I., Lee, W., Chan, M., Birek, J., Young, E.W., Sivagurunathan, K., Won, E., Simmons, C.A. & McCulloch, C.A. (2010). Methylglyoxal-modified collagen promotes myofibroblast differentiation. Matrix Biol 29, 537–548.Google Scholar
Zhu, D., Kim, Y., Steffes, M.W., Groppoli, T.J., Butkowski, R.J. & Mauer, S.M. (1994). Application of electron microscopic immunocytochemistry to the human kidney: Distribution of type IV and type VI collagen in normal human kidney. J Histochem Cytochem 42, 577–584.Google Scholar