Transforming growth factor-β1 induces apoptotic cell death in cultured retinal endothelial cells but not pericytes: Association with decreased expression of p21(waf1/cip1)

Journal of Cellular Biochemistry

Volumn 70, Issue 1, 1998, Pages 70-83

  Yan, Qi ^a   Sage, E Helene ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Angiogenesis; Apoptosis; Endothelial cells; Growth inhibition; P21(waf1 cip1); P53; Pericytes; Retina; TGF 1

Indexed keywords

4 [5 (4 METHYL 1 PIPERAZINYL)[2,5' BI 1H BENZIMIDAZOL] 2' YL]PHENOL; TRANSFORMING GROWTH FACTOR BETA1;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CATTLE; CELL DEATH; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; ENDOTHELIUM CELL; GROWTH INHIBITION; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RETINA CELL; RETINA NEOVASCULARIZATION;

ANIMALS; APOPTOSIS; CATTLE; CELL DIVISION; CELL SURVIVAL; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; ENDOTHELIUM, VASCULAR; RETINAL VESSELS; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0032126494     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19980701)70:1<70::AID-JCB8>3.0.CO;2-0     Document Type: Article

References (74)

1. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E (1995): Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nature Med 1:1024-1028.
2. Anderson DH, Guerin CJ, Hageman GS, Pfeffer BA, Flanders KC (1995): Distribution of transforming growth factor-beta isoforms in the mammalian retina. J Neurosci Res 42:63-79.
3. Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA (1989): An activated form of TGF-β is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci USA 86:4544-4548.
4. Arciniegas E, Sutton AB, Allen TD, Schor AM (1992): Transforming growth factor beta 1 promotes the differentiation of endothelial cells into smooth muscle-like cells in vitro. J Cell Sci 103:521-529.
5. Araki S, Shimada Y, Kaji K, Hayashi H (1990a): Apoptosis of vascular endothelial cells by fibroblast growth factor deprivation. Biochem Biophys Res Commun 168:1194-1200.
6. Araki S, Simada Y, Kaji K, Hayashi H (1990b): Role of protein kinase C in the inhibition by fibroblast growth factor of apoptosis in serum-depleted endothelial cells. Biochem Biophys Res Commun 172:1081-1085.
7. Boudreau N, Sympson CJ, Werb Z, Bissell MJ (1995): Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267:891-893.
8. Boudreau N, Werb Z, Bissell MJ (1996): Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc Natl Acad Sci USA 93:3509-3513.
9. Chan-Ling T, Gock B, Stone J (1995): The effect of oxygen on vasoformative cell division. Invest Ophthalmol Vis Sci 36:1201-1214.
10. Choi ME, Ballermann BJ (1995): Inhibition of capillary morphogenesis and associated apoptosis by dominant negative mutant transforming growth factor-beta receptors. J Biol Chem 270:21144-21150.
11. Clarke AR, Gledhill S, Hooper ML, Bird CC, Wyllie AH (1994): p53 dependence of early apoptotic and proliferative responses within the mouse intestinal epithelium following gamma-irradiation. Oncogene 9:1767-1773.
12. D'Amore PA (1994): Mechanisms of retinal and choroidal neovascularization. Invest Ophthalmol Vis Sci 35:3974-3979.
13. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF (1995): Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci USA 92:5545-5549.
14. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ (1995): Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121:1845-1854.
15. El-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B (1993): WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
16. Esser P, Heimann K, Bartz-Schmidt K, Fontana A, Schraermeyer U, Thumann G, Weller M (1997): Apoptosis in proliferative vitreoretinal disorders: Possible involvement of TGF-β-induced RPE cell apoptosis. Exp Eye Res 65:365-378.
17. Ewen ME, Sluss HK, Whitehouse LL, Livingston DM (1993): TGF beta inhibition of Cdk4 synthesis is linked to cell cycle arrest. Cell 74:1009-1020.
18. Ewen ME, Oliver CJ, Sluss HK, Miller SJ, Peeper DS (1995): p53-dependent repression of CDK4 translation in TGF-beta-induced G1 cell-cycle arrest. Genes Dev 9:204-217.
19. Fabregat I, SánchezA, Alvarez AM, Nakamura T, Benito M (1996): Epidermal growth factor, but not hepatocyte growth factor, suppresses the apoptosis induced by transforming growth factor-beta in fetal hepatocytes in primary culture. FEBS Lett 384:14-18.
20. Frisch SM, Francis H (1994): Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619-626.
21. Gansauge S, Gansauge F, Gause H, Poch B, Schoenberg MH, Beger HG (1997): The induction of apoptosis in proliferating human fibroblasts by oxygen radicals is associated with a p53-and p21WAF1CIP1 induction. FEBS Lett 404:6-10.
22. Gaudric A, Glacet BA, Clement G, Falquerho L, Barritault D, Coscas G (1990): Transforming growth factor beta in the vitreous of patients with epiretinal proliferation. Ophthalmologie 4:51-52.
23. Geng Y, Weinberg RA (1993): Transforming growth factor beta effects on expression of G1 cyclins and cyclin-dependent protein kinases. Proc Natl Acad Sci USA 90: 10315-10319.
24. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993): The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
25. Jiang B, Bezhadian MA, Caldwell RB (1995): Astrocytes modulate retinal vasculogenesis: effects on endothelial cell differentiation. Glia 15:1-10.
26. Kingsley DW (1994): The TGF-β superfamily: New members, new receptors, and new genetic tests of function in different organisms. Genes Dev 8:133-146.
27. Koff A, Ohtsuki M, Polyak K, Roberts JM, Massague J (1993): Negative regulation of G1 in mammalian cells: inhibition of cyclin E-dependent kinase by TGF-beta. Science 260:536-539.
28. Kohner EM, Porta M, Hyer SL (1991): The pathogenesis of diabetic retinopathy and cataract. In Pickup J, Williams G (eds): "Textbook of Diabetes." Oxford: Blackwell, pp 564-574.
29. Ilio KY, Sensibar JA, Lee C (1995): Effect of TGF-beta 1, TGF-alpha, and EGF on cell proliferation and cell death in rat ventral prostatic epithelial cells in culture. J Androl 16:482-490.
30. Landesman Y, Bringold F, Milne DD, Meek DW (1997): Modifications of p53 protein and accumulation of p21 and gadd45 mRNA in TGF-beta 1 growth inhibited cells. Cell Signal 9:291-298.
31. Landstrom M, Eklov S, Colosetti P, Nilsson S, Damber JE, Bergh A, Funa K (1996): Estrogen induces apoptosis in a rat prostatic adenocarcinoma: Association with an increased expression of TGF-beta 1 and its type-I and type-II receptors. Int J Cancer 67:573-579.
32. Lomo J, Blomhoff HK, Beiske K, Stokke T, Smeland EB (1995): TGF-beta 1 and cyclic AMP promote apoptosis in resting human B lymphocytes. J Immunol 154:1634-1643.
33. Lutty GA, Merges C, Threlkeld AB, Crone S, McLeod DS (1993): Heterogeneity in localization of isoforms of TGF-β in human retina, vitreous, and choroid. Invest Ophthalmol Vis Sci 34:477-487.
34. Lyons RM, Moses HL (1990): Transforming growth factor β and the regulation of cell proliferation. Eur J Biochem 187:467-473.
35. Madri JA, Pratt BM, Tucker AM (1988): Phenotypic modulation of endothelial cells by transforming growth factor-beta depends upon the composition and organization of the extracellular matrix. J Cell Biol 106:1375-1384.
36. Mandriota SJ, Pepper MS (1997): Vascular endothelial growth factor-induced in vitro angiogenesis and plasminogen activator expression are dependent on endogenous basic fibroblast growth factor. J Cell Sci 110:2293-2302.
37. Massague J (1990): The transforming growth factor-β family. Annu Rev Cell Biol 6:597-641.
38. Massague J (1992): Receptors for the TGF-beta family. Cell 69:1067-1070.
39. Meredith JE Jr, Fazeli B, Schwartz MA (1993): The extracellular matrix as a cell survival factor. Mol Biol Cell 4:953-961.
40. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B, Reed JC (1994a): Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene 9:1799-1805.
41. Miyashita T, Harigai M, Hanada M, Reed JC (1994b) Identification of a p53-dependent negative response element in the bcl-2 gene. Cancer Res 54:3131-3135.
42. Mogi Y, Kato J, Horimoto M, Takimoto R, Murakami T, Hirayama A, Kohgo Y, Watanabe N, Niitsu Y (1994): Close correlation between the dephosphorylation of p53 and growth suppression by transforming growth factor-beta 1 in nasopharyngeal carcinoma cells transduced with adenovirus early region genes. Jpn J Cancer Res 85:459-463.
43. Montesano R, Vassalli JD, Baird A, Guillemin R, Orci L (1986): Basic fibroblast growth factor induces angiogenesis in vitro. Proc Natl Acad Sci USA 83:7297-7301.
44. Ohta S, Yanagihara K, Nagata K (1997): Mechanism of apoptotic cell death of human gastric carcinoma cells mediated by transforming growth factor β. Biochem J 324:777-782.
45. Orlidge A, D'Amore PA (1987): Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455-1462.
46. Pepper MS (1997): Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev 8:21-43.
47. Phillips GD, Whitehead RA, Stone AM, Ruebel MW, Goodkin ML, Knighton DR (1993): Transforming growth factor beta (TGF-B) stimulation of angiogenesis: An electron microscopic study. J Submicrosc Cytol Pathol 25:149-155.
48. Pierce DF Jr, Gorska AE, Chytil A, Meise KS, Page DL, Coffey RJ Jr, Moses HL (1995): Mammary tumor suppression by transforming growth factor beta 1 transgene expression. Proc Natl Acad Sci USA 92:4254-4258.
49. Poluha W, Poluha DK, Chang B, Crosbie NE, Schonhoff CM, Kilpatrick DL, Ross AH (1996): The cyclin-dependent kinase inhibitor p21 (WAF1) is required for survival of differentiating neuroblastoma cells. Mol Cell Biol 16: 1335-1341.
50. Puro DG (1995): Growth factors and Muller cells. Prog Eye Retinal Res 15:89-101.
51. Raynal S, Jullien P, Lawrence DA (1994): Transforming growth factor-beta 1 enhances serum-induced dephosphorylation of the P53 protein in cell lines growth-inhibited by this factor. Growth Factors 11:197-203.
52. Reiss M, Vellucci VF, Zhou ZL (1993): Mutant p53 tumor suppressor gene causes resistance to transforming growth factor beta 1 in murine keratinocytes. Cancer Res 53:899-904.
53. Roberts AB, Sporn MB (1989): Regulation of endothelial cell growth, architecture, and matrix synthesis by TGF-β1. Am Rev Respir Dis 140:1126-1128.
54. Rotello RJ, Lieberman RC, Purchio AF, Gerschenson LE (1991): Coordinated regulation of apoptosis and cell proliferation by transforming growth factor beta 1 in cultured uterine epithelial cells. Proc Natl Acad Sci USA 88:3412-3415.
55. Sato Y, Rifkin DB (1989): Inhibition of endothelial cell movement by pericytes and smooth muscle cells: Activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J Cell Biol 109: 309-315.
56. Sankar S, Mahooti-Brooks N, Bensen L, McCarthy TL, Centrella M, Madri JA (1996): Modulation of transforming growth factor β receptor levels on microvascular endothelial cells during in vitro angiogenesis. J Clin Invest 97:1436-1446.
57. Schor AM, Schor SL (1986): The isolation and culture of endothelial cells and pericytes from the bovine retinal microvasculature: A comparative study with large vessel vascular cells. Microvasc Res 32:21-38.
58. Selvakumaran M, Reed JC, Liebermann D, Hoffman B (1994): Progression of the myeloid differentiation program is dominant to transforming growth factor-beta 1-induced apoptosis in M1 myeloid leukemic cells. Blood 84:1036-1042.
59. Shepro D, Morel NML (1993): Pericyte physiology. FASEB J 7:1031-1038.
60. Shi L, Nishioka WK, Th'ng J, Bradbury EM, Litchfield DW, Greenberg AH (1994): Premature p34cdc2 activation required for apoptosis. Science 263:1143-1145.
61. Sporn MB, Roberts AB (1992): Transforming growth factor-beta: recent progress and new challenges. J Cell Biol 119:1017-1021.
62. Stone J, Maslim J (1997): Mechanisms of retinal angiogenesis. Prog Eye Retinal Res 16:157-181.
63. Strasser A, Harris AW, Jacks T, Cory S (1994): DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79:329-339.
64. Stromblad S, Becker JC, Yebra M, Brooks PC, Cheresh DA (1996): Suppression of p53 activity and p21WAF1/CIP1 expression by vascular cell integrin alpha Vbeta3 during angiogenesis. J Clin Invest 98:426-433.
65. Suzuki K, Ono T, Takahashi K (1992): Inhibition of DNA synthesis by TGF-beta 1 coincides with inhibition of phosphorylation and cytoplasmic translocation of p53 protein. Biochem Biophys Res Commun 183:1175-1183.
66. Symonds H, Krall L, Remington L, Saenz-Robles M, Lowe S, Jacks T, Van-Dyke T (1994): p53-Dependent apoptosis suppresses tumor growth and progression in vivo. Cell 78:703-711.
67. Tanihara H, Inatani M, Honda Y (1997): Growth factors and their receptors in the retina and pigment epithelium. Prog Retina Eye Res 16:271-301.
68. Thieme H, Aiello LP, Takagi H, Ferrara N, King G (1995): Comparative analysis of vascular endothelial growth factor receptors on retinal and aortic vascular endothelial cells. Diabetes 44:98-103.
69. Tsukada T, Eguchi K, Migita K, Kawabe Y, Kawakami A, Matsuoka N, Takashima H, Mizokami A, Nagataki S (1995): Transforming growth factor beta 1 induces apoptotic cell death in cultured human umbilical vein endothelial cells with down-regulated expression of bcl-2. Biochem Biophys Res Commun 210: 1076-1082.
70. Wang J, Walsh K (1996): Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 273:359-361.
71. Xiong Y, Hannon GJ, Zhang H, Casso D, Kobayashi R, Beach D (1993): p21 is a universal inhibitor of cyclin kinases. Nature 366:701-704.
72. Yamamoto M, Maehara Y, Sakaguchi Y, Kusumoto T, Ichiyoshi Y, Sugimachi K (1996): Transforming growth factor-beta 1 induces apoptosis in gastric cancer cells through a p53-independent pathway. Cancer 77:1628-1633.
73. Yan Q, Vernon RB, Hendrickson AE, Sage EH (1996): Primary culture and characterization of microvascular endothelial cells from Macaca monkey retina. Invest Ophthalmol Vis Sci 37:2185-2194.
74. Yan Q, Sage EH, Hendrickson AE (1998): SPARC is expressed by ganglion cells and astrocytes in bovine retina. J Histochem Cytochem 46:3-10.