Inhibition of Platelet-Derived Growth Factor Promotes Pericyte Loss and Angiogenesis in Ischemic Retinopathy

American Journal of Pathology

Volumn 164, Issue 4, 2004, Pages 1263-1273

  Wilkinson Berka, Jennifer L ^a   Babic, Sanja ^a   De Gooyer, Tanyth ^a   Stitt, Alan W ^b   Jaworski, Kassie ^a   Ong, Leslie G T ^a   Kelly, Darren J ^c   Gilbert, Richard E ^c  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; CASPASE 3; IMATINIB; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN C;

AMBIENT AIR; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; APOPTOSIS; ARTICLE; CELL DEGENERATION; CELL LOSS; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE EXPRESSION; GENE OVEREXPRESSION; HISTOPATHOLOGY; NONHUMAN; OXYGEN TENSION; PERICYTE; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RETINA GANGLION CELL; RETROLENTAL FIBROPLASIA;

EID: 1642321880     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63214-2     Document Type: Article

References (45)

1. Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Levison SW: Diabetic retinopathy: more than meets the eye. Surv Ophthalmol 2002, Suppl 2:S253-S262
2. Klein R, Klein B, Moss S: Epidemiology of proliferative diabetic retinopathy. Diabetes Care 1992, 15:1875-1891
3. Stone J, Itin A, Alon T, Peer J, Gnessin H, Chan-Ling T, Keshet E: Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 1995, 15:4738-4747
4. Reynaud X, Dorey CK: Extraretinal neovascularization induced by hypoxic episodes in the neonatal rat. Invest Ophthalmol Vis Sci 1994, 35:3169-3177
5. Verbeek MM, Otte-Holler I, Wesseling P, Ruiter DJ, de Waal RM: Induction of α-smooth muscle actin expression in cultured human brain pericytes by transforming growth factor-β 1. Am J Pathol 1994, 144:372-382
6. Desmouliere A, Geinoz A, Gabbiani F, Gabbiani G: Transforming growth factor-β 1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993, 122:103-111
7. Cogan DG, Toussaint D, Kuwabara T: Retinal vascular patterns: IV. diabetic retinopathy. Arch Ophthalmol 1961, 66:366-378
8. Buzney SM, Frank RN, Varma SD, Tanishima T, Gabbay KH: Aldose reductase in retinal mural cells. Invest Ophthalmol Vis Sci 1977, 16:392-396
9. Leveen P, Pekny M, Gebre-Medhin S, Swolin B, Larsson E, Betsholtz C: Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 1994, 8:1875-1887
10. Lindahl P, Johansson BR, Leveen P, Betsholtz C: Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997, 277:242-245
11. Hellstrom M, Kal n M, Lindahl P, Abramsson A, Betsholtz C: Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999, 126:3047-3055
12. Hellstrom M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C: Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 2001, 153:543-554
13. Hammes H-P, Lin J, Renner O, Shani M, Lundqvist A, Betsholtz C, Brownlee M, Deutsch U: Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 2002, 51:3107-3112
14. Reinmuth N, Liu W, Jung YD, Ahmad SA, Shaheen RM, Fan F, Bucana CD, McMahon G, Gallick GE, Ellis LM: Induction of VEGF in perivascular cells defines a potential paracrine mechanism for endothelial cell survival. EMBO J 2001, 15:1239-1241
15. Affleck DG, Bull DA, Bailey SH, Albanil A, Connors R, Stringham JC, Karwande SV: PDGF(BB) increases myocardial production of VEGF: shift in VEGF mRNA splice variants after direct injection of bFGF, PDGF(BB), and PDGF(AB). J Surg Res 2002, 107:203-209
16. Shultz PJ, DiCorleto PE, Silver BJ, Abboud HE: Mesangial cells express PDGF mRNAs and proliferate in response to PDGF. Am J Physiol Heart Circ Physiol 1988, 255:F674-F684
17. Pierce GF, Mustoe TA, Altrock BW, Deuel TF, Thomason A: Role of platelet-derived growth factor in wound healing. J Cell Biochem 1991, 45:319-326
18. Doi T, Vlassara H, Kirstein M, Yamada Y, Striker GE, Striker LJ: Receptor-specific 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, 89:2873-2877
19. Capdeville R, Buchdunger E, Zimmermann J, Matter A: Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat Rev Drug Discov 2002, 1:493-502
20. Buchdunger E, O'Reilly T, Wood J: Pharmacology of imatinib (STI571). Eur J Cancer 2002, 38 Suppl 5:S28-S36
21. Penn JS, Tolman BL, Lowery LA: Variable oxygen exposure causes preretinal neovascularization in the newborn rat. Invest Ophthalmol Vis Sci 1993, 34:576-585
22. Wilkinson-Berka JL, Alousis NS, Kelly DJ, Gilbert RE: COX-2 inhibition and retinal angiogenesis in a mouse model of retinopathy of prematurity. Invest Ophthalmol Vis Sci 2003, 44:974-999
23. Vaughan AT, Beth CJ, Villalobos MJ: Surviving apoptosis. Apoptosis 2002, 7:73-177
24. Bandopadhyay R, Orte C, Lawrenson JG, Reid AR, De Silva S, Allt G: Contractile proteins at the blood-brain and blood retinal barriers. J Neurocytol 2001, 30:35-44
25. Gilbert R, Vranes D, Berka JL, Cox A, Kelly DJ, Stacker S, Cooper ME: Vascular endothelial growth factor and its receptors in control and diabetic rat eyes. Lab Invest 1998, 78:1017-1027
26. Mulder H, Ahren B, Sundler F: Islet amyloid polypeptide and insulin gene expression are regulated in parallel by glucose in vivo in rats. Am J Physiol 1996, 271:E1008-E1014
27. Moravski CJ, Skinner SL, Stubbs AJ, Sarlos S, Kelly DJ, Cooper ME, Gilbert RE, Wilkinson-Berka JL: The renin-angiotensin system influences ocular endothelial cell proliferation in diabetes: transgenic and interventional studies. Am J Pathol 2003, 162:151-160
28. Moravski CJ, Kelly DJ, Cooper ME, Gilbert RE, Bertram J, Shahinfar S, Skinner SL, Wilkinson-Berka JL: Retinal neovascularization is prevented by blockade of the renin-angiotensin system. Hypertension 2000, 36:1099-1104
29. Enge M, Bjarnegard M, Gerhardt H, Gustafsson E, Kalen M, Asker N, Hammes H-P, Shani M, Fassler R, Betsholtz C: Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 2002, 21:4307-4316
30. Dudley A, Gilbert RE, Thomas D, Cox A, Price JT, Best J, Jenkins A: STI-571 inhibits in vitro angiogenesis. Biochem Biophys Res Commun 2003, 310:136-143
31. Holmgren L, Glaser A, Pfeifer-Ohlsson S, Ohlsson R: Angiogenesis during human extraembryonic development involves the spatiotemporal control of PDGF ligand and receptor gene expression. Development 1991, 113:749-754
32. Gilbert R, Kelly DJ, McKay T, Chadban S, Hill PA, Cooper ME, Atkins RC, Nikolic-Patterson DJ: PDGF signal transduction inhibition ameliorates experimental mesangial proliferative glomerulonephritis. Kidney Int 2001, 59:1324-1332
33. Schlondorff D: The glomerular mesangial cell: an expanding role for a specialized pericyte. EMBO J 1987, 1:272-281
34. Hirschi KK, D'Amore PA: Pericytes in the microvasculature. Cardiovasc Res 1996, 32:687-698
35. Crocker DJ, Murad TM, Geer JC: Role of the pericyte in wound healing: an ultrastructural study. Exp Mol Pathol 1970, 13:51-63
36. Ferrara N: Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 2001, 280: C1358-C1366
37. Benjamin LE, Hemo I, Keshet E: A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998, 125:1591-1598
38. Stone J, Chanling T, Peer J, Itin A, Gnessin H, Keshet E: Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest Ophthalmol Vis Sci 1996, 37:290-299
39. Hammes HP, Lin JH, Bretzel RG, Brownlee M, Breier G: Up-regulation of the vascular endothelial growth factor receptor system in experimental background diabetic retinopathy of the rat. Diabetes 1998, 47:401-406
40. Yokota T, Ma RC, Park JY, Isshiki K, Sotiropoulos KB, Rauniyar RK, Bornfeldt KE, King GL: Role of protein kinase C on the expression of platelet-derived growth factor and endothelin-1 in the retina of diabetic rats and cultured retinal capillary pericytes. Diabetes 2003, 52:8338-8845
41. Su E, Alder V, Yu D, Yu P, Cringle S, Yogesan K: Continued progression of retinopathy despite spontaneous recovery to normoglycemia in a long-term study of streptozotocin-induced diabetes in rats. Graefes Arch Clin Exp Ophthalmol 2000, 238:163-173
42. Engerman R, Finkelstein D, Aguirre G, Diddie KR, Fox RR, Frank RN, Varma SD: Ocular complications. Diabetes 1982, 31:82-88
43. Okuda Y, Adrogue HJ, Nakajima T, Mizutani M, Asano M, Tachi Y, Suzuki S, Yamashita K: Increased production of PDGF by angiotensin and high glucose in human vascular endothelium. Life Sci 1996, 59:1455-1461
44. Inaba T, Ishibashi S, Gotoda T, Kawamura M, Morino N, Nojima Y, Kawakami M, Yazaki Y, Yamada N: Enhanced expression of platelet-derived growth factor-β receptor by high glucose: involvement of platelet-derived growth factor in diabetic angiopathy. Diabetes 1996, 45:507-512
45. Freyberger H, Brocker M, Yakut H, Hammer J, Effert R, Schifferdecker E, Schatz H, Derwahl M: Increased levels of platelet-derived growth factor in vitreous fluid of patients with proliferative diabetic retinopathy. Exp Clin Endocrinol Diabetes 2000, 108:106-109