Differential TGF-β signaling in retinal vascular cells: A role in diabetic retinopathy?

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 4, 2010, Pages 1857-1865

  van Geest, Rob J ^a   Klaassen, Ingeborg ^a   Vogels, Ilse M C ^a   van Noorden, Cornelis J F ^a   Schlingemann, Reinier O ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; MESSENGER RNA; SD 208; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD5 PROTEIN; SMAD7 PROTEIN; SMAD8 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN SERINE THREONINE KINASE; PTERIDINE DERIVATIVE; SD-208; TGF BETA TYPE I RECEPTOR; TGF-BETA TYPE I RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; COW; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; ENZYME INHIBITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RETINA CELL; RETINA VASCULAR CELL; SIGNAL TRANSDUCTION; STEADY STATE; UPREGULATION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING; ANIMAL; CATTLE; CYTOLOGY; DRUG ANTAGONISM; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; RETINA BLOOD VESSEL;

ANIMALS; BLOTTING, WESTERN; CATTLE; CELLS, CULTURED; DIABETIC RETINOPATHY; ENDOTHELIUM, VASCULAR; FIBRONECTINS; PERICYTES; PHOSPHORYLATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN-SERINE-THREONINE KINASES; PTERIDINES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RETINAL VESSELS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 77951224948     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4181     Document Type: Article

References (47)

1. Zimmet P, Alberti KGMM, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782-787.
2. Klein BEK. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol. 2007;14:179-183.
3. Garner A. Histopathology of diabetic retinopathy in man. Eye. 1993;7:250-253.
4. Lorenzi M, Gerhardinger C. Early cellular and molecular changes induced by diabetes in the retina. Diabetologia. 2001;44:791-804.
5. Cai J, Boulton M. The pathogenesis of diabetic retinopathy: old concepts and new questions. Eye. 2002;16:242-260.
6. Kuiper EJ, van Zijderveld R, Roestenberg P, et al. Connective tissue growth factor is necessary for retinal capillary basal lamina thickening in diabetic mice. J Histochem Cytochem. 2008;56:785-792.
7. Roy S, Sato T, Paryani G, Kao R. Downregulation of fibronectin overexpression reduces basement membrane thickening and vascular lesions in retinas of galactose-fed rats. Diabetes. 2003;52: 1229-1234.
8. Oshitari T, Polewski P, Chadda M, Li A, Sato T, Roy S. Effect of combined antisense oligonucleotides against high-glucose-and diabetes-induced overexpression of extracellular matrix components and increased vascular permeability. Diabetes. 2006;55:86-92.
9. Nishikawa T, Giardino I, Edelstein D, Brownlee M. Changes in diabetic retinal matrix protein mRNA levels in a common transgenic mouse strain. Curr Eye Res. 2000;21:581-587.
10. Roy S, Maiello M, Lorenzi M. Increased expression of basementmembrane collagen in human diabetic-retinopathy. J Clin Invest. 1994;93:438-442.
11. Spirin KS, Saghizadeh M, Lewin SL, Zardi L, Kenney MC, Ljubimov AV. Basement membrane and growth factor gene expression in normal and diabetic human retinas. Curr Eye Res. 1999;18:490-499.
12. Arden GB, Sidman RL, Arap W, Schlingemann RO. Spare the rod and spoil the eye. Br J Ophthalmol. 2005;89:764-769.
13. Kuiper EJ, Hughes JM, Van Geest RJ, et al. Effect of VEGF-A on expression of profibrotic growth factor and extracellular matrix genes in the retina. Invest Ophthalmol Vis Sci. 2007;48:4267-4276.
14. Branton MH, Kopp JB. TGF-beta and fibrosis. Microbes Infect. 1999;1:1349-1365.
15. Fujimoto M, Maezawa Y, Yokote K, et al. Mice lacking Smad3 are protected against streptozotocin-induced diabetic glomerulopathy. Biochem Biophys Res Commun. 2003;305:1002-1007.
16. Wolf G, Chen SD, Ziyadeh FN. From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes. 2005;54:1626-1634.
17. Wyss-Coray T, Lin C, Von Euw D, Masliah E, Mucke L, Lacombe P. Alzheimer's disease-like cerebrovascular pathology in transforming growth factor-beta 1 transgenic mice and functional metabolic correlates. Ann NY Acad Sci. 2000;903:317-323.
18. Gerhardinger C, Dagher Z, Sebastiani P, Park YS, Lorenzi M. The transforming growth factor-beta pathway is a common target of drugs that prevent experimental diabetic retinopathy. Diabetes. 2009;58:1659-1667.
19. Hughes JM, Kuiper EJ, Klaassen I, et al. Advanced glycation end products cause increased CCN family and extracellular matrix gene expression in the diabetic rodent retina. Diabetologia. 2007; 50:1089-1098.
20. Massague J. TGF-beta signal transduction. Annu Rev Biochem. 1998;67:753-791.
21. Nguyen TQ, Goldschmeding R. Bone morphogenetic protein-7 and connective tissue growth factor: novel targets for treatment of renal fibrosis? Pharm Res. 2008;25:2416-2426.
22. Massague J. The transforming growth-factor-beta family. Annu Rev Cell Biol. 1990;6:597-641.
23. Saika S. TGF beta pathobiology in the eye. Lab Invest. 2006;86: 106-115.
24. Valdimarsdottir G, Goumans MJ, Itoh F, Itoh S, Heldin CH, ten Dijke P. Smad7 and protein phosphatase 1 alpha are critical determinants in the duration of TGF-beta/ALKI signaling in endothelial cells. BMC Cell Biol. 2006;7.
25. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 2002;21:1743-1753.
26. Goumans MJ, Lebrin F, Valdimarsdottir G. Controlling the angiogenic switch: a balance between two distinct TGF-beta receptor signaling pathways. Trends Cardiovasc Med. 2003;13:301-307.
27. Lebrin F, Goumans MJ, Jonker L, et al. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J. 2004;23:4018-4028.
28. Kang YB, Chen CR, Massague J. A self-enabling TGF beta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell. 2003;11:915-926.
29. Ten Dijke P, Korchynskyi E, Valdimarsdottir G, Goumans MJ. Controlling cell fate by bone morphogenetic protein receptors. Mol Cell Endocrinol. 2003;211:105-113.
30. Obata H, Kaji Y, Yamada H, Kato M, Tsuru T, Yamashita H. Expression of transforming growth factor-beta superfamily receptors in rat eyes. Acta Ophthalmol Scand. 1999;77:151-156.
31. Goumans MJ, Valdimarsdottir G, Itoh S, et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFP/ALK5 signaling. Mol Cell. 2003;12:817-828.
32. Uhl M, Aulwurm S, Wischhusen J, et al. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res. 2004;64: 7954-7961.
33. Kapoun AM, Gaspar NJ, Wang Y, et al. Transforming growth factor-beta receptor type 1 (TGF beta RI) kinase activity but not p38 activation is required for TGF beta RI-induced myofibroblast differentiation and profibrotic gene expression. Mol Pharmacol. 2006;70:518-531.
34. Sambrook J, Gething MJ. Protein-structure-chaperones, paperones. Nature. 1989;342:224-225.
35. Vandesompele J, De Preter K, Pattyn F, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3: RESEARCH0034.
36. Kuiper EJ, Witmer AN, Klaassen I, Oliver N, Goldschmeding R, Schlingemann RO. Differential expression of connective tissue growth factor in microglia and pericytes in the human diabetic retina. Br J Ophthalmol. 2004;88:1082-1087.
37. Walshe TE, Saint-Geniez M, Maharaj AS, Sekiyama E, Maldonado AE, D'Amore PA. TG. F-beta is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLoS ONE. 2009;4:e5149.
38. Stewart PA, Tuor UI. Blood-eye barriers in the rat: correlation of ultrastructure with function. J Comp Neurol. 1994;340:566-576.
39. Stefansson S, Lawrence DA. The serpin PAI-1 inhibits cell migration by blocking integrin alpha (v) beta(3) binding to vitronectin. Nature. 1996;383:441-443.
40. Sawdey M, Podor TJ, Loskutoff DJ. Regulation of type-1 plasminogen-activator inhibitor gene-expression in cultured bovine aortic endothelial-cells: induction by transforming growth factor-beta, lipopolysaccharide, and tumor necrosis factor-alpha. J Biol Chem. 1989;264:10396-10401.
41. Ban CR, Twigg SM. Fibrosis in diabetes complications: pathogenic mechanisms and circulating and urinary markers. Vasc Health Risk Manag. 2008;4:575-596.
42. Nguyen TQ, Roestenberg P, van Nieuwenhoven FA, et al. CTGF Inhibits BMP-7 Signaling in diabetic nephropathy. J Am Soc Nephrol. 2008;19:2098-2107.
43. Kuiper EJ, de Smet MD, van Meurs JC, et al. Association of connective tissue growth factor with fibrosis in vitreoretinal disorders in the human eye. Arch Ophthalmol. 2006;124:1457-1462.
44. Kuiper EJ, van Nieuwenhoven FA, de Smet MD, et al. The angiofibrotic switch of VEGF and CTGF in proliferative diabetic retinopathy. PLoS ONE. 2008;3:e2675.
45. Witmer AN, van Blijswijk BC, Van Noorden CJ, Vrensen GF, Schlingemann RO. In vivo angiogenic phenotype of endothelial cells and pericytes induced by vascular endothelial growth factor-A. J Histochem Cytochem. 2004;52:39-52.
46. Duncan MR, Frazier KS, Abramson S, et al. Connective tissue growth factor mediates transforming growth factor beta-induced collagen synthesis: downregulation by cAMP. FASEB J. 1999;13: 1774-1786.
47. Leask A, Abraham DJ. The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol. 2003;81:355-363.