Vascular basement membrane thickening in diabetic retinopathy

Current Eye Research

Volumn 35, Issue 12, 2010, Pages 1045-1056

  Roy, Sayon ^a   Ha, John ^a   Trudeau, Kyle ^a   Beglova, Ekaterina ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basement membrane; Basement membrane thickening; Diabetic retinopathy; Microangiopathy; Vascular lesions

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALDOSE REDUCTASE INHIBITOR; ANGIOTENSIN II; ANTISENSE OLIGONUCLEOTIDE; BOSENTAN; CANDESARTAN; CILAZAPRIL; COLLAGEN TYPE 4; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIN; FIBRONECTIN; GROWTH FACTOR; LAMININ; POLYOL; PROTEIN KINASE C; SMALL INTERFERING RNA;

CAPILLARY BASEMENT MEMBRANE; CAPILLARY BASEMENT MEMBRANE THICKENING; CLINICAL TRIAL; DIABETIC MICROANGIOPATHY; DIABETIC RETINOPATHY; DRUG INHIBITION; ENZYME ACTIVATION; HISTOPATHOLOGY; HUMAN; HYPERGLYCEMIA; INFLAMMATION; MEDICAL RESEARCH; MEMBRANE COMPONENT; NONHUMAN; PRIORITY JOURNAL; RETINA BLOOD VESSEL; RETINA CAPILLARY; RETINA INJURY; SHORT SURVEY; VASCULAR DISEASE;

ANIMALS; BASEMENT MEMBRANE; DIABETIC RETINOPATHY; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; RETINAL VESSELS;

EID: 78649731494     PISSN: 02713683     EISSN: 14602202     Source Type: Journal    
DOI: 10.3109/02713683.2010.514659     Document Type: Short Survey

References (137)

1. Wagener, H. P. and Wilder, R. M. The Retinitis of Diabetes Mellitus: Preliminary Report. J Am Med Assoc. 1921;76(6): p. 515-517.
2. Ashton, N. Vascular changes in diabetes with particular reference to the retinal vessels; preliminary report. Br J Ophthalmol. 1949;33(7): p. 407-20.
3. Botting, A.J., A.L. Brown and M.B. Divertie. The Pulmonary Lesion In A Patient With Goodpasture's Syndrome, As Studied With The Electron Microscope. Am J Clin Pathol. 1964;42: p. 387-94.
4. Kajikawa, K and S. Kakihara. An electron microscope study of the basement membrane of proliferated bile ductules. Exp Mol Pathol. 1969;11(1): p. 17-27.
5. Naccarato, R., G. Maschio, F. Sirigu, et al. The muscle in dia-betes mellitus. A histologic (light and electron microscope) and biochemical study by means of needle biopsy. Virchows Arch B Cell Pathol. 1970;4(4): p. 283-93.
6. Kozak, W.M., N.A. Marker and K.K. Elmer. Effects of aldose reductase inhibition on the retina and health indices of streptozotocin-diabetic rats. Doc Ophthalmol. 1986;64(4): p. 355-77.
7. Martinez-Hernandez, A. and P.S. Amenta. The basement membrane in pathology Lab Invest. 1983;48(6): p. 656-77.
8. Tang, J., S. Mohr, Y.D. Du, et al. Non-uniform distribution of lesions and biochemical abnormalities within the retina of diabetic humans. Curr Eye Res. 2003;27(1): p. 7-13.
9. Dische F.E, Anderson VE, Keane SJ, et al. Incidence of thin membrane nephropathy: morphometric investigation of a population sample. J Clin Pathol. 1990;43: p. 457-460
10. Haas M. Thin glomerular basement membrane nephropa-thy: Incidence in 3471 consecutive renal biopsies examined by electron microscopy Arch Pathol Lab Med. 2006;130: p. 699-706.
11. Vick, N.A. Skeletal muscle capillary basement membranes in humans. Acta Neuropathol. 1971;17(1): p. 1-5.
12. Begieneman M.P., van de Goot F.R., Krijnen PA, et al. The basement membrane of intramyocardial capillaries is thick-ened in patients with acute myocardial infarction. J Vasc Res. 2009; 47: p. 54-60.
13. Siperstein, M.D., R.H. Unger and L.L. Madison. Studies of muscle capillary basement membranes in normal subjects, diabetic, and prediabetic patients. J Clin Invest. 1968;47(9): p. 1973-99.
14. Lindsay, D.C., I.S., Anand, J.G., Bennett, et al. Ultrastructural analysis of skeletal muscle. Microvascular dimensions and basement membrane thickness in chronic heart failure. Eur Heart J. 1994;15(11): p. 1470-6.
15. Quabbe, H.J., K.E. Schenk, H. Schneider, et al. Absence of muscle capillary basement membrane thickening and retinopathy in patients with myocardial infarction and impaired i.v. glucose tolerance. Acta Diabetol Lat. 1983;20(4): p. 321-7.
16. Kuiper E.J., van Zijderveld R., Roestenberg P., et al. Connective tissue growth factor is necessary for retinal cap-illary basal lamina thickening in diabetic mice. J Histochem Cytochem. 2008; 56: p. 785-792.
17. Carlson, E.C., J.L. Audette, NJ. Veitenheimer, et al. Ultrastructural morphometry of capillary basement mem-brane thickness in normal and transgenic diabetic mice. Anat Rec A Discov Mol Cell Evol Biol. 2003;271(2): p. 332-41.
18. Cherian, S., S. Roy, A. Pinheiro, et al. Tight glycemic control regulates fbronectin expression and basement membrane thickening in retinal and glomerular capillaries of diabetic rats. Invest Ophthalmol Vis Sci. 2009;50(2): p. 943-9.
19. Dosso, A.A., E. Rungger-Brandle and P.M. Leuenberger. Ultrastructural alterations in capillaries of the diabetic hypertensive rat retina: protective effects of ACE inhibition. Diabetologia. 2004;47(7): p. 1196-201.
20. Mansour, S.Z., D.L. Hatchell, D., Chandler, et al. Reduction of basement membrane thickening in diabetic cat retina by sulindac Invest Ophthalmol Vis Sci. 1990;31(3): p. 457-63.
21. Hood, J.C., J. Savige, A.E. Seymour, et al. Ultrastructural appearance of renal and other basement membranes in the Bull terrier model of autosomal dominant hereditary nephritis. Am J Kidney Dis. 2000;36(2): p. 378-91.
22. Stitt, A.W., H.R., Anderson, T.A., Gardiner, et al. Diabetic retinopathy: quantitative variation in capillary basement membrane thickening in arterial or venous environments. Br J Ophthalmol. 1994;78(2): p. 133-7.
23. Ljubimov, A.V., R.E. Burgeson, R.J. Butkowski, et al. Basement membrane abnormalities in human eyes with diabetic retinopathy J Histochem Cytochem. 1996;44(12): p. 1469-79.
24. Timpl, R., M. Dziadek, S. Fujiwara, et al. Nidogen: a new, self-aggregating basement membrane protein. Eur J Biochem. 1983;137(3): p. 455-65.
25. Charonis, A.S. and E.C. Tsilibary., 1990. Assembly of Basement Membrane Protein, in Organization and Assembly of Plant and Animal Extracellular Matrix, S.W., Adair and R.P. Mecham, Editors. San Diego, CA: Academic Press, Inc. p. 85-117.
26. Brazel, D., R. Pollner, I. Oberbaumer, et al. Human basement membrane collagen (type IV). The amino acid sequence of the alpha 2(IV) chain and its comparison with the alpha 1(IV) chain reveals deletions in the alpha 1(IV) chain. Eur J Biochem. 1988;172(1): p. 35-42.
27. Vuorio E, de Crombrugghe B. The family of collagen genes. Annu Rev Biochem.1990; 59: p. 837-872.
28. Hudson BG, Tryggvason K, Sundaramoorthy M, et al. Alport's syndrome, Goodpasture's syndrome, and type IV collagen. N Engl J Med. 2003; 348: p. 2543-2556.
29. Khoshnoodi, J., V. Pedchenko and B.G. Hudson. Mammalian collagen IV. Microsc Res Tech. 2008;71(5): p. 357-70.
30. Risteli, J., H.P. Bachinger, J. Engel, et al. 7-S collagen: char-acterization of an unusual basement membrane structure. Eur J Biochem. 1980;108(1): p. 239-50.
31. Timpl, R., H. Wiedemann, V. van Delden, et al. A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem. 1981;120(2): p. 203-11.
32. Timpl R, et al. Macromolecular organization of type IV col-lagen. In: New Trends in Basement Membrane Research. New York: Raven Press, 1982; p. 57.
33. de Fougerolles, A.R., A.G. Sprague, C.L. Nickerson-Nutter, et al. Regulation of infammation by collagen-binding inte-grins alpha1beta1 and alpha2beta1 in models of hypersen-sitivity and arthritis. J Clin Invest. 2000;105(6): p. 721-9.
34. Pankov, R., and K.M. Yamada. Fibronectin at a glance. J Cell Sci. 2002;115(Pt 20): p. 3861-3.
35. Geiger, B., A. Bershadsky, R. Pankov, et al. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001;2(11): p. 793-805.
36. Mandarino LJ, Sundarraj N, Finlayson J, et al. Regulation of fbronectin and laminin synthesis by retinal capillary endothelial cells and pericytes in vitro. Exp Eye Res. 1993; 57: p. 609-621.
37. Cagliero E, Maiello M, Boeri D, et al. Increased expression of basement membrane components in human endothe-lial cells cultured in high glucose. J Clin Invest. 1988; 82: p. 735-738.
38. Roy S, Cagliero E, Lorenzi M. Fibronectin overexpression in retinal microvessels of patients with diabetes. Invest Ophthalmol Vis Sci. 1996;37:258-266.
39. Foidart, J.M., E.W. Bere, Jr., M. Yaar, et al. Distribution and immunoelectron microscopic localization of laminin, a non-collagenous basement membrane glycoprotein. Lab Invest. 1980;42(3): p. 336-42.
40. Madri, J.A., F.J. Roll, H. Furthmayr, et al. Ultrastructural localization of fbronectin and laminin in the basement membranes of the murine kidney. J Cell Biol. 1980;86(2): p. 682-7.
41. Laurie, G.W., C.P. Leblond and G.R. Martin. Localization of type IV collagen, laminin, heparan sulfate proteoglycan, and fbronectin to the basal lamina of basement membranes. J Cell Biol. 1982;95(1): p. 340-4.
42. Engel, J., E. Odermatt, A. Engel, et al. Shapes, domain organizations and fexibility of laminin and fbronectin, two multifunctional proteins of the extracellular matrix. J Mol Biol. 1981;150(1): p. 97-120.
43. Marinkovich, M.P. Tumour microenvironment: laminin 332 in squamous-cell carcinoma. Nat Rev Cancer. 2007;7(5): p. 370-80.
44. Timpl, R., D. Tisi, J.F. Talts, et al. Structure and function of laminin LG modules. Matrix Biol. 2000;19(4): p. 309-17.
45. Hynes, R.O. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110(6): p. 673-87.
46. Sung, U., J.J., O'Rear and P.D. Yurchenco. Localization of heparin binding activity in recombinant laminin G domain. Eur J Biochem. 1997;250(1): p. 138-43.
47. Terranova, V.P., D.H. Rohrbach and G.R. Martin. Role of laminin in the attachment of PAM 212 (epithelial) cells to basement membrane collagen. Cell. 1980;22(3): p. 719-26.
48. Kumar, V, A.B. Abbas, N. Fausto, et al. 2007. Robbins Basic Pathology, 8th Ed. Philadelphia, PA: Saunders.
49. Ledbetter, S.R., L.W. Fisher and J.R. Hassell. Domain structure of the basement membrane heparan sulfate proteoglycan. Biochemistry. 1987;26(4): p. 988-95.
50. Paulsson, M., P.D. Yurchenco, G.C. Ruben, et al. Structure of low density heparan sulfate proteoglycan isolated from a mouse tumor basement membrane. J Mol Biol. 1987;197(2): p. 297-313.
51. Laurie, G.W., S. Inoue, J.T. Bing, et al. Visualization of the large heparan sulfate proteoglycan from basement membrane. Am J Anat. 1988;181(3): p. 320-6.
52. Hassell, J.R., W.C. Leyshon, S.R. Ledbetter, et al. Isolation of two forms of basement membrane proteoglycans. J Biol Chem. 1985;260(13): p. 8098-105.
53. Fransson, L.A., I. Carlstedt, L. Coster, et al. The functions of the heparan sulphate proteoglycans. Ciba Found Symp. 1986;124: p. 125-42.
54. Frisch, S.M., and E. Ruoslahti. Integrins and anoikis. Curr Opin Cell Biol. 1997;9(5): p. 701-6.
55. Brem, R.B., S.G. Robbins, D.J. Wilson, et al. Immunolocalization of integrins in the human retina. Invest Ophthalmol Vis Sci. 1994;35(9): p. 3466-74.
56. Heino J. The collagen receptor integrins have distinct ligand recognition and signaling functions. Matrix Biol. 2000;19:319-323.
57. Hemler M.E., Huang C., Schwarz L. The VLA protein family. Characterization of fve distinct cell surface heterodimers each with a common 130,000 molecular weight beta subunit. J Biol Chem. 1987;262:3300-3309.
58. Hemler M.E., Crouse C., Takada Y, et al. Multiple very late antigen (VLA) heterodimers on platelets. Evidence for distinct VLA-2, VLA-5 (fbronectin receptor), and VLA-6 structures. J Biol Chem. 1988; 263: p. 7660-7665.
59. Chakrabarti, S., N. Ma and A.A. Sima. Anionic sites in diabetic basement membranes and their possible role in diffusion barrier abnormalities in the BB-rat. Diabetologia. 1991;34(5): p. 301-6.
60. Beltramo E., Pomero F., Allione A., et al. Pericyte adhesion is impaired on extracellular matrix produced by endothelial cells in high hexose concentrations. Diabetologia. 2002; 45: p. 416-419.
61. Beltramo E., Buttiglieri S., Pomero F., et al. A study of capil-lary pericyte viability on extracellular matrix produced by endothelial cells in high glucose. Diabetologia. 2003; 46: p. 409-415.
62. Roy S., Sato T. Role of vascular basement membrane com-ponents in diabetic microangiopathy Drug News Perspect. 2000;13(2): p. 91-8.
63. Roy S., Sato T., Paryani G., et al. Downregulation of fbronec-tin overexpression reduces basement membrane thickening and vascular lesions in retinas of galactose-fed rats. Diabetes. 2003; 52: p. 1229-1234.
64. Roy S., Lorenzi M. Early biosynthetic changes in the dia-betic-like retinopathy of galactosefed rats. Diabetologia. 1996;39: p. 735-738.
65. Oshitari, T., P. Polewski, M. Chadda, et al. Effect of com-bined antisense oligonucleotides against high-glucoseand diabetes-induced overexpression of extracellular matrix components and increased vascular permeability Diabetes. 2006;55(1): p. 86-92.
66. Chronopoulos, A., K. Trudeau, S. Roy et al. Altered Basement Membrane Composition and Increased Vascular Permeability in Diabetic Retinopathy Invest Ophthalmol Vis Sci. 2009;50(E-Abstract 26/A13).
67. Chronopoulos, A., P. Trackman and S., Roy. Effect of High Glucose on Lysyl Oxidase Expression in Rat Retinal Endothelial Cells. Diabetes. 2009;58(suppl 1): p. 866-P.
68. Nishikawa, T., I., Giardino, D., Edelstein, et al. Changes in diabetic retinal matrix protein mRNA levels in a common transgenic mouse strain. Curr Eye Res. 2000;21(1): p. 581-7.
69. Davis, G.E. and D.R. Senger. Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ Res. 2005;97(11): p. 1093-107.
70. Gerhardt, H and C. Betsholtz. Endothelial-pericyte interac-tions in angiogenesis. Cell Tissue Res. 2003;314(1): p. 15-23.
71. Tucker B, Klassen H, Yang L, et al. Elevated MMP Expression in the MRL Mouse Retina Creates a Permissive Environment for Retinal Regeneration. Invest Ophthalmol Vis Sci. 2008; 49: 1686-1695.
72. De Taeye B., Gils A., Declerck P.J. The story of the serpin plasminogen activator inhibitor 1: Is there any need for another mutant? Thromb Haemost. 2004;92:898-924.
73. Das A., Boyd N., Jones T.R., et al. Inhibition of choroidal neovascularization by a peptide inhibitor of the urokinase plasminogen activator and receptor system in a mouse model. Arch Ophthalmol. 2004;122:1844-1849.
74. Zhang X., Cheng M., Chintala SK. Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration. Invest Ophthalmol Vis Sci. 2004;45:2374-2383.
75. Tsilibary E.C. Microvascular basement membranes in dia-betes mellitus. J Pathol. 2003;200(4): p. 537-46.
76. Giebel, S.J., G. Menicucci, P.G. McGuire, et al. Matrix metal-loproteinases in early diabetic retinopathy and their role in alteration of the blood-retinal barrier. Lab Invest. 2005;85(5): p. 597-607.
77. Xue, M., P.J. Thompson, R. Clifton-Bligh, et al. Leukocyte matrix metalloproteinase-9 is elevated and contributes to lymphocyte activation in type I diabetes. Int J Biochem Cell Biol. 2005;37(11): p. 2406-16.
78. Das, A., P.G. McGuire, C. Eriqat, et al. Human diabetic neovascular membranes contain high levels of urokinase and metalloproteinase enzymes. Invest Ophthalmol Vis Sci. 1999;40(3): p. 809-13.
79. Yang, R., H. Liu, I. Williams, et al. Matrix metalloproteinase-2 expression and apoptogenic activity in retinal pericytes: implications in diabetic retinopathy. Ann N Y Acad Sci. 2007;1103: p. 196-201.
80. Roy S, Maiello M, Lorenzi M. Increased expression of base-ment membrane collagen in human diabetic retinopathy J Clin Invest. 1994;93:438-442.
81. Robison, W.G., P.F. Kador and J.H. Kinoshita. Retinal capillaries: basement membrane thickening by galac-tosemia prevented with aldose reductase inhibitor Science. 1983;221(4616): p. 1177-9.
82. Sorbinil Retinopathy Trial Research Group. A randomized trial of sorbinil, an aldose reductase inhibitor, in diabetic retinopathy Arch Ophthalmol. 1990;108:1234-1244.64.
83. Lorenzi, M. The polyol pathway as a mechanism for diabetic retinopathy: attractive, elusive, and resilient. Exp Diabetes Res. 2007;2007: p. 61038.
84. Xia, P., R.M. Kramer and G.L. King. Identifcation of the mechanism for the inhibition of Na+,K(+)-adenosine triphosphatase by hyperglycemia involving activation of protein kinase C and cytosolic phospholipase A2. J Clin Invest. 1995;96(2): p. 733-40.
85. Lee, T.S., K.A. Saltsman, H. Ohashi, et al. Activation of protein kinase C by elevation of glucose concentration: proposal for a mechanism in the development of diabetic vascular complications. Proc Natl Acad Sci USA. 1989;86(13): p. 5141-5.
86. Kreisberg, J.I. Hyperglycemia and microangiopathy Direct regulation by glucose of microvascular cells. Lab Invest. 1992;67(4): p. 416-26.
87. Studer, R.K., PA. Craven and F.R. DeRubertis. Role for protein kinase C in the mediation of increased fbronectin accumulation by mesangial cells grown in high-glucose medium. Diabetes. 1993;42(1): p. 118-26.
88. Aiello, L.P., R.L. Avery P.G. Arrigg, et al. Vascular endothe-lial growth factor in ocular fuid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med. 1994;331(22): p. 1480-7.
89. Katsura, Y., T. Okano, M. Noritake, et al. Hepatocyte growth factor in vitreous fuid of patients with proliferative diabetic retinopathy and other retinal disorders. Diabetes Care. 1998;21(10): p. 1759-63.
90. Pfeiffer, A. and H. Schatz. Diabetic microvascular compli-cations and growth factors. Exp Clin Endocrinol Diabetes. 1995;103(1): p. 7-14.
91. Budhiraja, S. and J. Singh. Protein kinase C beta inhibitors: a new therapeutic target for diabetic nephropathy and vas-cular complications. Fundam Clin Pharmacol. 2008;22(3): p. 231-40.
92. Koya, D., M.R. Jirousek, Y.W. Lin, et al. Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extra-cellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest. 1997;100(1): p. 115-26.
93. Eli Lilly, A.C. (Pressrelease): Data Presented at ADA: Roboxistaurin mesylate may reduce moderate visual loss in people with moderate to severe diabetic retinopathy 2003;June14,2003.
94. Clarke M, Dodson PM. PKC inhibition and diabetic micro-vascular complications. BestPract Res Clin Endocrinol Metab. 2007;21:573-586
95. Eli Lilly AC Data presented at ADA: Roboxistaurin mesy-late may reduce moderate visual loss in people with mod-erate to severe diabetic retinopathy Press Release: June 14, 2003.
96. Degenhardt, T.P., S.R. Thorpe and J.W. Baynes. Chemical modifcation of proteins by methylglyoxal. Cell Mol Biol (Noisy-le-grand). 1998;44(7): p. 1139-45.
97. Stitt, A.W., Y.M. Li, T.A. Gardiner, et al. Advanced glycation end products (AGEs) co-localize with AGE receptors in the retinal vasculature of diabetic and of AGE-infused rats. Am J Pathol. 1997;150(2): p. 523-31.
98. Bhatwadekar AD, Glenn JV, Li G, et al. Advanced glycation of fbronectin impairs vascular repair by endothelial pro-genitor cells: implications for vasodegeneration in diabetic retinopathy Invest Ophthalmol Vis Sci. 2008; 49: 1232-1241.
99. McDonald DM, Coleman G, Bhatwadekar A, et al. Advanced glycation of the Arg-Gly-Asp (RGD) tripeptide motif modu-lates retinal microvascular endothelial cell dysfunction. Mol Vis. 2009; 15: 1509-1520.
100. Kalfa, T.A., M.E. Gerritsen, E.C. Carlson, et al. Altered pro-liferation of retinal microvascular cells on glycated matrix. Invest Ophthalmol Vis Sci. 1995;36(12): p. 2358-67.
101. Mott, J.D., R.G. Khalifah, H. Nagase, et al. Nonenzymatic glycation of type IV collagen and matrix metalloproteinase susceptibility Kidney Int. 1997;52(5): p. 1302-12.
102. Doi, T., H. Vlassara, M. Kirstein, et al. Receptor-specifc increase in extracellular matrix production in mouse mesangial cells by advanced glycosylation end products is mediated via platelet-derived growth factor Proc Natl Acad Sci USA. 1992;89(7): p. 2873-7.
103. Kirstein, M., C. Aston, R. Hintz, et al. Receptor-specifc induction of insulin-like growth factor I in human mono-cytes by advanced glycosylation end product-modifed proteins. J Clin Invest. 1992;90(2): p. 439-46.
104. Skolnik, E.Y., Z. Yang, Z. Makita, et al. Human and rat mesangial cell receptors for glucose-modifed proteins: potential role in kidney tissue remodelling and diabetic nephropathy J Exp Med. 1991;174(4): p. 931-9.
105. Gardiner, T.A., H.R. Anderson and A.W. Stitt. Inhibition of advanced glycation end-products protects against retinal capillary basement membrane expansion during long-term diabetes. J Pathol. 2003;201(2): p. 328-33.
106. Stitt, A., T.A., Gardiner, N.L., Alderson, et al. The AGE inhibitor pyridoxamine inhibits development of retin-opathy in experimental diabetes. Diabetes. 2002;51(9): p. 2826-32.
107. Clements, R.S., W.G. Robison and M.P. Cohen. Anti-glycated albumin therapy ameliorates early retinal micro-vascular pathology in db/db mice. J Diabetes Complications. 1998;12(1): p. 28-33.
108. Bolton WK, Cattran DC, Williams ME, et al. Randomized trial of an inhibitor of formation of advanced glycation end products in diabetic nephropathy Am J Nephrol. 2004; 24: 32-40.
109. Gore-Hyer, E., J. Pannu, E.A. Smith, et al. Selective stimulation of collagen synthesis in the presence of costimulatory insulin signaling by connective tissue growth factor in scleroderma fbroblasts. Arthritis Rheum. 2003;48(3): p. 798-806.
110. Paradis, V., G. Perlemuter, F. Bonvoust, et al. High glucose and hyperinsulinemia stimulate connective tissue growth factor expression: a potential mechanism involved in progression to fbrosis in nonalcoholic steatohepatitis. Hepatology. 2001;34(4 Pt 1): p. 738-44.
111. Twigg, S.M., M.M. Chen, A.H. Joly, et al. Advanced glyco-sylation end products up-regulate connective tissue growth factor (insulin-like growth factor-binding protein-related protein 2) in human fbroblasts: a potential mechanism for expansion of extracellular matrix in diabetes mellitus. Endocrinology. 2001;142(5): p. 1760-9.
112. Twigg, S.M., A.H. Joly, M.M. Chen, et al. Connective tissue growth factor/IGF-binding protein-related protein-2 is a mediator in the induction of fbronectin by advanced glycosylation end-products in human dermal fbroblasts. Endocrinology. 2002;143(4): p. 1260-9.
113. Zhou, G., C. Li and L. Cai. Advanced glycation end-prod-ucts induce connective tissue growth factor-mediated renal fbrosis predominantly through transforming growth fac-tor beta-independent pathway Am J Pathol. 2004;165(6): p. 2033-43.
114. Kuiper, E.J., J.M. Hughes, R.J. Van Geest, et al. Effect of VEGF-A on expression of profbrotic growth factor and extracellular matrix genes in the retina. Invest Ophthalmol Vis Sci. 2007;48(9): p. 4267-76.
115. Qi, W., X. Chen, S. Twigg, et al. Tranilast attenuates con-nective tissue growth factor-induced extracellular matrix accumulation in renal cells. Kidney Int. 2006;69(6): p. 989-95.
116. Sohn, M., Y. Tan, B. Wang, et al. Mechanisms of low-density lipoprotein-induced expression of connective tissue growth factor in human aortic endothelial cells. Am J Physiol Heart Circ Physiol. 2006;290(4): p. H1624-34.
117. Otani A, Takagi H, Oh H, et al. Angiotensin II-stimulated vascular endothelial growth factor expression in bovine retinal pericytes. Invest Ophthalmol Vis Sci. 2000; 41: 1192-1199.
118. Zheng Z, Chen H, Xu X, et al. Effects of angiotensin-con-verting enzyme inhibitors and beta-adrenergic blockers on retinal vascular endothelial growth factor expression in rat diabetic retinopathy Exp Eye Res. 2007; 84: 745-752.
119. Gardiner, T.A., H.R. Anderson, T. Degenhardt, et al. Prevention of retinal capillary basement membrane thick-ening in diabetic dogs by a non-steroidal anti-infammatory drug. Diabetologia. 2003;46(9): p. 1269-75.
120. Evans, T., D.X. Deng, S. Chen, et al. Endothelin receptor blockade prevents augmented extracellular matrix compo-nent mRNA expression and capillary basement membrane thickening in the retina of diabetic and galactosefed rats. Diabetes. 2000;49(4): p. 662-6.
121. Deng D, Evans T, Mukherjee K, et al. Diabetes-induced vascular dysfunction in the retina: role of endothelins. Diabetologia. 1999; 42: 1228-1234.
122. Roy, S. and T. Roth. Proliferative effect of high glucose is modulated by antisense oligonucleotides against fbronec-tin in rat endothelial cells. Diabetologia. 1997;40(9): p. 1011-7.
123. Roy, S., K. Zhang, T. Roth, et al. Reduction of fbronectin expression by intravitreal administration of antisense oli-gonucleotides. Nat Biotechnol. 1999;17(5): p. 476-9.
124. Smith, M.R., T. Xie, Z.Z. Zhou, et al. Effcacy of treatment with antisense oligonucleotides comple-mentary to immunoglobulin sequences of bcl-2/immunoglobulin fusion transcript in a t(14;18) human lymphoma-scid mouse model. Clin Cancer Res. 2001;7(2): p. 400-6.
125. Leung, S., H. Miyake, T. Zellweger, et al. Synergistic chemosensitization and inhibition of progression to andro-gen independence by antisense Bcl-2 oligodeoxynucleotide and paclitaxel in the LNCaP prostate tumor model. Int J Cancer. 2001;91(6): p. 846-50.
126. Miyake, H., B.P. Monia and M.E. Gleave. Inhibition of pro-gression to androgen-independence by combined adjuvant treatment with antisense BCL-XL and antisense Bcl-2 oli-gonucleotides plus taxol after castration in the Shionogi tumor model. Int J Cancer. 2000;86(6): p. 855-62.
127. Oshitari, T., D. Brown,and S. Roy. SiRNA strategy against overexpression of extracellular matrix in diabetic retinopa-thy. Exp Eye Res. 2005;81(1): p. 32-7.
128. Kagami, S., W.A. Border, D.E. Miller, et al. Angiotensin II stimulates extracellular matrix protein synthesis through induction of transforming growth factor-beta expression in rat glomerular mesangial cells. J Clin Invest. 1994;93(6): p. 2431-7.
129. Ray P.E., LA. Bruggeman, S. Horikoshi, et al. Angiotensin II stimulates human fetal mesangial cell proliferation and fbronectin biosynthesis by binding to AT1 receptors. Kidney Int. 1994;45(1): p. 177-84.
130. Singh, R., N. Alavi, A.K. Singh, et al. Role of angiotensin II in glucose-induced inhibition of mesangial matrix degra-dation. Diabetes. 1999;48(10): p. 2066-73.
131. Wolf, G., U. Haberstroh and E.G. Neilson. Angiotensin II stimulates the proliferation and biosynthesis of type I collagen in cultured murine mesangial cells. Am J Pathol. 1992;140(1): p. 95-107.
132. Ziyadeh, F.N., K. Sharma, M. Ericksen, et al. Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-beta. J Clin Invest. 1994;93(2): p. 536-42.
133. Sugiyama T, Okuno T, Fukuhara M, et al. Angiotensin II receptor blocker inhibits abnormal accumulation of advanced glycation end products and retinal dam-age in a rat model of type 2 diabetes. Exp Eye Res. 2007;85:406-512.
134. Frank RN, et al., Keirn RJ, Kennedy A, et al. Galactose-induced retinal capillary basement membrane thicken-ing: Prevention by Sorbinil. Invest Ophthalmol Vis Sci. 1983;24:1519-1524.
135. Chakrabarti S, Sima AA. Effect of aldose reductase inhi-bition and insulin treatment on retinal capillary base-ment membrane thickening in BB rats. Diabetes. 1989;38: 1181-1186.
136. McCaleb ML, McKean ML, Hohman TC, et al. Intervention with the aldose reductase inhibitor, tolrestat, in renal and retinal lesions of streptozotocindiabetic rats. Diabetologia. 1991;34:695-701.
137. Robison WG, Jr., Kador PF, Akagi Y, et al. Prevention of basement membrane thickening in retinal capillaries by a novel inhibitor of aldose reductase, tolrestat. Diabetes. 1986;35:295-299.