The influence of elastin degradation products, glucose and atorvastatin on metalloproteinase-1, -2, -9 and tissue inhibitor of metalloproteinases-1, -2, -3 expression in human retinal pigment epithelial cells

• Authors: Mariola Dorecka , Tomasz Francuz , Wojciech Garczorz , Krzysztof Siemianowicz , Wanda Romaniuk
• Languages of publication: EN

Abstracts

EN

Purpose: Hyperglycemia and increased concentrations of elastin degradation products (EDPs) are common findings in patients with diabetes, atherosclerosis and hypertension. The aim of this study was to assess the influence of high glucose, EDPs and atorvastatin on MMP-1, MMP-2, MMP-9 and TIMP1-3 gene expression in human retinal pigment epithelial cells (HRPE) in vitro. Method: HRPE were cultured for 24 hours with the substances being tested (glucose, EDPs), alone or in combination. Additionally, the cells were treated with atorvastatin in two different concentrations (1 or 10 μM). After incubation, total cellular RNA was extracted and used for gene expression evaluation. Gene expression was measured using the real-time RT-PCR technique. Results: Glucose, EDPs and atorvastatin had no impact on TIMP-1 and TIMP-3 expression. HRPE cells treated with glucose or EDPs with the addition of atorvastatin had a statistically significant decrease of TIMP-2 expression; glucose alone decreased MMP-1 expression. Atorvastatin decreased expression of all assessed genes, except TIMP-1 and TIMP-3 in a dose-dependent manner. Conclusions: Our results confirm the importance of MMPs and TIMPs in retinal vascular biology. Atorvastatin-induced MMPs gene expression can deeply affect extracellular matrix turnover, which may play an important role in the progression of ocular diseases.

Keywords

EN

metalloproteinase; TIMP; atorvastatin; HRPE

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2014
• Volume: 61
• Issue: 2
• Pages: 265-270

Dates

published

2014

received

2013-06-14

revised

2014-03-26

accepted

2014-04-04

(unknown)

2014-06-06

Contributors

author

Mariola Dorecka

• Department of Ophthalmology, School of Medicine in Katowice, Medical University of Silesia, Katowice, Poland

author

Tomasz Francuz

• Department of Biochemistry, School of Medicine in Katowice, Medical University of Silesia, Katowice, Poland

author

Wojciech Garczorz

• Department of Biochemistry, School of Medicine in Katowice, Medical University of Silesia, Katowice, Poland

author

Krzysztof Siemianowicz

• Department of Biochemistry, School of Medicine in Katowice, Medical University of Silesia, Katowice, Poland

author

Wanda Romaniuk

• Department of Ophthalmology, School of Medicine in Katowice, Medical University of Silesia, Katowice, Poland

References

• Ahir A, Guo L, Hussain AA, Marshall J (2002) Expression of metalloproteinases from human retinal pigment epithelial cells and their effects on the hydraulic conductivity of Bruch's membrane. Invest Ophthalmol Vis Sci 43: 458-465.
• Alge-Priglinger CS, Kreutzer T, Obholzer K, Wolf A, Mempel M, Kernt M, Kampik A et al. (2009) Oxidative stress-mediated induction of MMP-1 and MMP-3 in human RPE cells. Invest Ophthalmol Vis Sci 50: 5495-5503.
• Al-Shabrawey M, Bartoli M, El-Remessy AB, Ma G, Matragoon S, Lemtalsi T, Caldwell RW et al. (2008) Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Invest Ophthalmol Vis Sci 49: 3231-3238.
• Brassart B, Fuchs P, Huet E, Alix AJ, Wallach J, Tamburro AM, Delacoux F et al. (2001) Conformational dependence of collagenase (matrix metalloproteinase-1) up-regulation by elastin peptides in cultured fibroblasts. J Biol Chem 276: 5222-5227.
• Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477: 267-283.
• Chan CM, Huang JH, Chiang HS, Wu WB, Lin HH, Hong JY, Hung CF (2010) Effects of (-)-epigallocatechin gallate on RPE cell migration and adhesion. Mol Vis 16: 586-595.
• Chong NH, Alexander RA, Gin T, Bird AC, Luthert PJ (2000) TIMP-3, collagen, and elastin immunohistochemistry and histopathology of Sorsby's fundus dystrophy. Invest Ophthalmol Vis Sci 41: 898-902.
• Collin B, Busseuil D, Korandji C, Zeller M, Cottin Y, Duvillard L, Rioufol G et al. (2006) Short-term atorvastatin treatment does not modify neointimal morphology but reduces MMP-2 expression in normocholesterolemic rabbit stented arteries. J Cardiovasc Pharmacol 47: 428-436.
• Collins R, Armitage J, Parish S, Sleight P, Peto R (2004) Heart Protection Study Collaborative Group. Effects of cholesterol-lowering with simvastatin on stroke and other major vascular events in 20536 people with cerebrovascular disease or other high-risk conditions. Lancet 363: 757-767.
• Cui JZ, Chiu A, Maberley D, Ma P, Samad A, Matsubara JA (2007) Stage specificity of novel growth factor expression during development of proliferative vitreoretinopathy. Eye (Lond) 21: 200-208.
• Cusick M, Chew EY, Chan CC, Kruth HS, Murphy RP, Ferris FL (2003) Histopathology and regression of retinal hard exudates in diabetic retinopathy after reduction of elevated serum lipid levels. Ophthalmology 110: 2126-2133.
• Death AK, Fisher EJ, McGrath KC, Yue DK (2003) High glucose alters matrix metalloproteinase expression in two key vascular cells: potential impact on atherosclerosis in diabetes. Atherosclerosis 168: 263-269.
• Decanini A, Karunadharma PR, Nordgaard CL, Feng X, Olsen TW, Ferrington DA (2008) Human retinal pigment epithelium proteome changes in early diabetes. Diabetologia 51: 1051-1061.
• Dunaief JL, Dentchev T, Ying GS, Milam AH (2002) The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 120: 1435-1442.
• Eichler W, Friedrichs U, Thies A, Tratz C, Wiedemann P (2002) Modulation of matrix metalloproteinase and timp-1 expression by cytokines in human RPE cells. Invest Ophthalmol Vis Sci 43: 2767-2773.
• Evans JR (2001) Risk factors for age-related macular degeneration. Prog Retin Eye Res 20: 227-253.
• Giebel SJ, Menicucci G, McGuire PG, Das A (2005) Matrix metalloproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest 85: 597-607.
• Gupta A, Gupta V, Thapar S, Bhansali A (2004) Lipid-lowering drug atorvastatin as an adjunct in the management of diabetic macular edema. Am J Ophthalmol 137: 675-682.
• Hance KA, Tataria M, Ziporin SJ, Lee JK, Thompson RW (2002) Monocyte chemotactic activity in human abdominal aortic aneurysms: role of elastin degradation peptides and the 67-kD cell surface elastin receptor. J Vasc Surg 35: 254-261.
• Hoffmann S, Friedrichs U, Eichler W, Rosenthal A, Wiedemann P (2002) Advanced glycation end products induce choroidal endothelial cell proliferation, matrix metalloproteinase-2 and VEGF upregulation in vitro. Graefe's Arch Clin Exp Ophthalmol 240: 996-1002.
• Hoffmann S, He S, Ehren M, Ryan SJ, Wiedemann P, Hinton DR (2006) MMP-2 and MMP-9 secretion by RPE is stimulated by angiogenic molecules found in choroidal neovascular membranes. Retina 26: 454-461.
• Hollborn M, Stathopoulos C, Steffen A, Wiedemann P, Kohen L, Bringmann A (2007) Positive feedback regulation between MMP-9 and VEGF in human RPE cells. Invest Ophthalmol Vis Sci 48: 4360-4367.
• Ichihara S, Noda A, Nagata K, Obata K, Xu J, Ichihara G, Oikawa S et al. (2006) Pravastatin increases survival and suppresses an increase in myocardial matrix metalloproteinase activity in a rat model of heart failure. Cardiovasc Res 69: 726-735.
• Johnson PT, Lewis GP, Talaga KC, Brown MN, Kappel PJ, Fisher SK, Anderson DH et al. (2003) Drusen-associated degeneration in the retina. Invest Ophthalmol Vis Sci 44: 4481-4488.
• Jones CB, Sane DC, Herrington DM (2003) Matrix metalloproteinases: a review of their structure and role in acute coronary syndrome. Cardiovasc Res 59: 812-823.
• Kajimoto K, Miyauchi K, Kasai T, Shimada K, Kojima Y, Shimada A, Niinami H et al. (2009) Short-term 20-mg atorvastatin therapy reduces key inflammatory factors including c-Jun N-terminal kinase and dendritic cells and matrix metalloproteinase expression in human abdominal aortic aneurysmal wall. Atherosclerosis 206: 505-511.
• Kim JJ, Li JJ, Kim KS, Kwak SJ, Jung DS, Ryu DR, Yoo TH et al. (2008) High glucose decreases collagenase expression and increases TIMP expression in cultured human peritoneal mesothelial cells. Nephrol Dial Transplant 23: 534-541.
• Lambert V, Munaut C, Jost M, Noël A, Werb Z, Foidart JM, Rakic JM (2002) Matrix metalloproteinase-9 contributes to choroidal neovascularization. Am J Pathol 161: 1247-1253.
• Lapis K, Tímár J (2002) Role of elastin-matrix interactions in tumor progression. Semin Cancer Biol 12: 209-217.
• Lee D, Kim JS, Cho HK, Lee JH (2004) The effects of glucose on the expression of MMP and TIMP in cultured retinal pigment epithelial cells. Korean J Ophthalmol 18: 132.
• Luan Z, Chase AJ, Newby AC (2003) Statins inhibit secretion of metalloproteinases-1, -2, -3, and -9 from vascular smooth muscle cells and macrophages. Arterioscler Thromb Vasc Biol 23: 769-775.
• Ludwig S, Shen GX (2006) Statins for diabetic cardiovascular complications. Curr Vasc Pharmacol 4: 245-251.
• Marin-Castaño ME, Csaky KG, Cousins SW (2005) Nonlethal oxidant injury to human retinal pigment epithelium cells causes cell membrane blebbing but decreased MMP-2 activity. Invest Ophthalmol Vis Sci 46: 3331-3340.
• Nagineni CN, Detrick B, Hooks JJ (1994) Synergistic effects of gamma interferon on inflammatory mediators that induce interleukin-6 gene expression and secretion by human retinal pigment epithelial cells. Clin Diagn Laboratory Immunol 1: 569-577.
• Nagineni CN, Detrick B, Hooks JJ (2000) Toxoplasma gondii infection induces gene expression and secretion of interleukin 1 (IL-1), IL-6, granulocyte-macrophage colony stimulating factor, and intracellular adhesion molecule 1 by human retinal pigment epithelial cells. Infect Immun 68: 407-410.
• Noda K, Ishida S, Inoue M, Obata K, Oguchi Y, Okada Y, Ikeda E (2003) Production and activation of matrix metalloproteinase-2 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 44: 2163-2170.
• Ntayi C, Labrousse AL, Debret R, Birembaut P, Bellon G, Antonicelli F, Hornebeck W et al. (2004) Elastin-derived peptides upregulate matrix metalloproteinase-2-mediated melanoma cell invasion through elastin-binding protein. J Invest Dermatol 122: 256-265.
• Padgett LC, Lui GM, Werb Z, LaVail MM (1997) Matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-1 in the retinal pigment epithelium and interphotoreceptor matrix: vectorial secretion and regulation. Exp Eye Res 64: 927-938.
• Pepper MS (2001) Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler Thromb Vasc Biol 21: 1104-1117.
• Petersen E, Wågberg F, Ängquist KA (2002) Serum concentrations of elastin-derived peptides in patients with specific manifestations of atherosclerotic Disease. Eur J Vasc Endovasc Surg 24: 440-444.
• Robinet A, Fahem A, Cauchard JH, Huet E, Vincent L, Lorimier S, Antonicelli F et al. (2005) Elastin-derived peptides enhance angiogenesis by promoting endothelial cell migration and tubulogenesis through upregulation of MT1-MMP. J Cell Sci 118: 343-356.
• Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R et al. (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96: 1395-1403.
• Sen K, Misra A, Kumar A, Pandey RM (2002) Simvastatin retards progression of retinopathy in diabetic patients with hypercholesterolemia. Diabetes Res Clin Pract 56: 1-11.
• Sheridan CM, Occleston NL, Hiscott P, Kon CH, Khaw PT, Grierson I (2001) Matrix metalloproteinases: a role in the contraction of vitreo-retinal scar tissue. Am J Pathol 159: 1555-1566.
• Sivaprasad S, Chong NV, Bailey TA (2005) Serum elastin-derived peptides in age-related macular degeneration. Invest Ophthalmol Vis Sci 46: 3046-3051.
• Spraul CW, Kaven C, Lang GK, Lang GE (2004) Effect of growth factors on bovine retinal pigment epithelial cell migration and proliferation. Ophthalmic Res 36: 166-171.
• Strauss O (2005) The retinal pigment epithelium in visual function. Physiol Rev 85: 845-881.
• Sulochana KN, Ramakrishnan S, Rajesh M, Coral K, Badrinath SS (2001) Diabetic retinopathy: Molecular mechanisms, present regime of treatment and future perspectives. Current Science 80: 133-142.
• Troger J, Sellemond S, Kieselbach G, Kralinger M, Schmid E, Teuchner B, Nguyen QA et al. (2003) Inhibitory effect of certain neuropeptides on the proliferation of human retinal pigment epithelial cells. Br J Ophthalmol 87: 1403-1408.
• Uemura S, Matsushita H, Li W, Glassford AJ, Asagami T, Lee KH, Harrison DG et al. (2001) Diabetes mellitus enhances vascular matrix metalloproteinase activity: role of oxidative stress. Circ Res 88: 1291-1298.
• Villarroel M, García-Ramírez M, Corraliza L, Hernández C, Simó R (2009) Effects of high glucose concentration on the barrier function and the expression of tight junction proteins in human retinal pigment epithelial cells. Exp Eye Res 89: 913-920.
• Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92: 827-839.
• Webster L, Chignell AH, Limb GA (1999) Predominance of MMP-1 and MMP-2 in epiretinal and subretinal membranes of proliferative vitreoretinopathy. Exp Eye Res 68: 91-98.
• Yamagishi S, Nakamura K, Matsui T, Sato T, Takeuchi M (2006) Potential utility of statins, 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors in diabetic retinopathy. Med Hypotheses 66: 1019-1021.
• Yoshida A, Elner SG, Bian ZM, Kunkel SL, Lukacs NW, Elner VM (2001) Thrombin regulates chemokine induction during human retinal pigment epithelial cell/monocyte interaction. Am J Pathol 159: 1171-1180.
• Zhuge Y, Xu J (2001) Rac1 mediates type I collagen-dependent MMP-2 activation. Role in cell invasion across collagen barrier. J Biol Chem 276: 16248-16256.