Inhibition of growth factor-induced Ras signaling in vascular endothelial cells and angiogenesis by 3,3′-diindolylmethane

Carcinogenesis

Volumn 27, Issue 3, 2006, Pages 541-550

  Chang, Xiaofei ^a   Firestone, Gary L ^b   Bjeldanes, Leonard F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,3' DIINDOLYLMETHANE; ANGIOGENESIS INHIBITOR; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN TYROSINE KINASE; RAF PROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANIMAL EXPERIMENT; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; ENDOTHELIUM CELL; ENZYME ACTIVATION; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

ANTICARCINOGENIC AGENTS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; DNA; ENDOTHELIAL CELLS; HUMANS; INDOLES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; RAS PROTEINS; SIGNAL TRANSDUCTION; UMBILICAL CORD; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33644930299     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgi230     Document Type: Article

References (67)

1. Beecher,C.W. (1994) Cancer preventive properties of varieties of Brassica oleracea: A review. Am. J. Clin. Nutr., 59, 1166S-1170S.
2. Block,G., Patterson,B. and Subar,A. (1992) Fruit, vegetables, and cancer prevention: A review of the epidemiological evidence. Nutr. Cancer, 18, 1-29.
3. Steinmetz,K.A. and Potter,J.D. (1991) Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control, 2, 325-357.
4. Steinmetz,K.A. and Potter,J.D. (1991) Vegetables, fruit, and cancer. II. Mechanisms. Cancer Causes Control, 2, 427-442.
5. Lopez-Otin,C. and Diamandis,E.P. (1998) Breast and prostate cancer: An analysis of common epidemiological, genetic, and biochemical features. Endocr. Rev., 19, 365-396.
6. Kristal,A.R. and Lampe,J.W. (2002) Brassica vegetables and prostate cancer risk: A review of the epidemiological evidence. Nutr. Cancer, 42, 1-9.
7. Wattenberg,L.W. and Loub,W.D. (1978) Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res., 38, 1410-1413.
8. Grubbs,C.J., Steele,V.E., Casebolt,T., Juliana,M.M., Eto,I., Whitaker,L.M., Dragnev,K.H., Kelloff,G.J. and Lubet,R.L. (1995) Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res., 15, 709-716.
9. Stoewsand,G.S., Anderson,J.L. and Munson,L. (1988) Protective effect of dietary brussels sprouts against mammary carcinogenesis in Sprague-Dawley rats. Cancer Lett., 39, 199-207.
10. Chen,I., McDougal,A., Wang,F. and Safe,S. (1998) Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis, 19, 1631-1639.
11. He,Y.H. and Schut,H.A. (1999) Inhibition of DNA adduct formation of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine and 2-amino-3-methylimidazo[4,5-f]quinoline by dietary indole-3-carbinol in female rats. J. Biochem. Mol. Toxicol., 13, 239-247.
12. He,Y.H., Friesen,M.D., Ruch,R.J. and Schut,H.A. (2000) Indole-3-carbinol as a chemopreventive agent in 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) carcinogenesis: inhibition of PhIP-DNA adduct formation, acceleration of PhIP metabolism, and induction of cytochrome P450 in female F344 rats. Food Chem. Toxicol., 38, 15-23.
13. Bradfield,C.A. and Bjeldanes,L.F. (1984) Effect of dietary indole-3-carbinol on intestinal and hepatic monooxygenase, glutathione S-transferase and epoxide hydrolase activities in the rat. Food Chem. Toxicol., 22, 977-982.
14. Cover,C.M., Hsieh,S.J., Tran,S.H., Hallden,G., Kim,G.S., Bjeldanes,L.F. and Firestone,G.L. (1998) Indole-3-carbinol inhibits the expression of cyclin-dependent kinase-6 and induces a G1 cell cycle arrest of human breast cancer cells independent of estrogen receptor signaling. J. Biol. Chem., 273, 3838-3847.
15. Cram,E.J., Liu,B.D., Bjeldanes,L.F. and Firestone,G.L. (2001) Indole-3-carbinol inhibits CDK6 expression in human MCF-7 breast cancer cells by disrupting Sp1 transcription factor interactions with a composite element in the CDK6 gene promoter. J. Biol. Chem., 276, 22332-22340.
16. Chinni,S.R., Li,Y., Upadhyay,S., Koppolu,P.K. and Sarkar,F.H. (2001) Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene, 20, 2927-2936.
17. Ge,X., Fares,F.A. and Yannai,S. (1999) Induction of apoptosis in MCF-7 cells by indol-3-carbinol is independent of p53 and bax. Anticancer Res., 19, 3199-3203.
18. WAP1/CIP1 expression. Carcinogenesis, 23, 1297-1305.
19. Hong,C., Firestone,G.L. and Bjeldanes,L.F. (2002) Bcl-2 family-mediated apoptosc effects of 3,3′-diindolylmethane (DIM) in human breast cancer cells. Biochem. Pharmacol., 63, 1085-1097.
20. Cover,C.M., Hsieh,S.J., Cram,E.J., Hong,C., Riby,J.E., Bjeldanes,L.F. and Firestone,G.L. (1999) Indole-3-carbinol and tamoxifen cooperate to arrest the cell cycle of MCF-7 human breast cancer cells. Cancer Res., 59, 1244-1251.
21. Auborn,K.J. (2002) Therapy for recurrent respiratory papillomatosis. Antivir. Ther., 7, 1-9.
22. Folkman,J. (1995) Seminars in Medicine of the Beth Israel Hospital, Boston. Clinical applications of research on angiogenesis. N. Engl. J. Med., 333, 1757-1763.
23. Hanahan,D. and Folkman,J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
24. Folkman,J. (1975) Tumor angiogenesis: A possible control point in tumor growth. Ann. Intern. Med., 82, 96-100.
25. Senger,D.R., Perruzzi,C.A., Feder,J. and Dvorak,H.F. (1986) A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Cancer Res., 46, 5629-5632.
26. Risau,W. (1997) Mechanisms of angiogenesis. Nature, 386, 671-674.
27. Kim,K.J., Li,B., Winer,J., Armanini,M., Gillett,N., Phillips,H.S. and Ferrara,N. (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature, 362, 841-844.
28. Ferrara,N. (1999) Vascular endothelial growth factor: Molecular and biological aspects. Curr. Top. Microbiol. Immunol., 237, 1-30.
29. Millauer,B., Longhi,M.P., Plate,K.H., Shawver,L.K., Risau,W., Ullrich,A. and Strawn,L.M. (1996) Dominant-negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo. Cancer Res., 56, 1615-1620.
30. Goldman,C.K., Kendall,R.L., Cabrera,G., Soroceanu,L., Heike,Y., Gillespie,G.Y., Siegal,G.P., Mao,X., Bett,A.J., Huckle,W.R., Thomas,K.A. and Curiel,D.T. (1998) Paracrine expression of a native soluble vascular endothelial growth factor receptor inhibits tumor growth, metastasis, and mortality rate. Proc. Natl Acad. Sci. USA, 95, 8795-8800.
31. Prewett,M., Huber,J., Li,Y., Santiago,A., O'Connor,W., King,K., Overholser,J., Hooper,A., Pytowski,B., Witte,L., Bohlen,P. and Hicklin,D.J. (1999) Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors. Cancer Res., 59, 5209-5218.
32. De Vries,C., Escobedo,J.A., Ueno,H., Houck,K., Ferrara,N. and Williams,L.T. (1992) The fins-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science, 255, 989-991.
33. Millauer,B., Wizigmann-Voos,S., Schnurch,H., Martinez,R., Moller,N.P., Risau,W. and Ullrich,A. (1993) High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell, 72, 835-846.
34. Waltenberger,J., Claesson-Welsh,L., Siegbahn,A., Shibuya,M. and Heldin,C.H. (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem., 269, 26988-26995.
35. Sawano,A., Takahashi,T., Yamaguchi,S. and Shibuya,M. (1997) The phosphorylated 1169-tyrosine containing region of flt-1 kinase (VEGFR-1) is a major binding site for PLCgamma. Biochem. Biophys. Res. Commun., 238, 487-491.
36. Sato,Y., Kanno,S., Oda,N., Abe,M., Ito,M., Shitara,K. and Shibuya,M. (2000) Properties of two VEGF receptors, Flt-1 and KDR, in signal transduction. Ann. N.Y. Acad. Sci., 902, 201-205.
37. Kroll,J. and Waltenberger,J. (1997) The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J. Biol. Chem., 272, 32521-32527.
38. Kanno,S., Oda,N., Abe,M., Terai,Y., Ito,M., Shitara,K., Tabayashi,K., Shibuya,M. and Sato,Y. (2000) Roles of two VEGF receptors, Flt-1 and KDR, in the signal transduction of VEGF effects in human vascular endothelial cells. Oncogene, 19, 2138-2146.
39. Cobb,M.H. and Goldsmith,E.J. (1995) How MAP kinases are regulated. J. Biol. Chem., 270, 14843-14846.
40. Marshall,C.J. (1996) Ras effectors. Curr. Opin. Cell Biol., 8, 197-204.
41. Ray,L.B. and Sturgill,T.W. (1988) Insulin-stimulated microtubule-associated protein kinase is phosphorylated on tyrosine and threonine in vivo. Proc. Natl Acad. Sci. USA, 85, 3753-3757.
42. Cobb,M.H., Boulton,T.G. and Robbins,D.J. (1991) Extracellular signal-regulated kinases: ERKs in progress. Cell Regul., 2, 965-978.
43. Huang,W., Alessandrini,A., Crews,C.M. and Erikson,R.L. (1993) Raf-1 forms a stable complex with Mek1 and activates Mek1 by serine phosphorylation. Proc. Natl Acad. Sci. USA, 90, 10947-10951.
44. Chang,X., Tou,J.C., Hong,C., Kim,H.A., Riby,J.E., Firestone,G.L. and Bjeldanes,L.F. (2005) 3,3′-Diindolylmethane inhibits angiogenesis and the growth of transplantable human breast carcinoma in athymic mice. Carcinogenesis, 26, 771-778.
45. Bradfield,C.A. and Bjeldanes,L.F. (1987) Structure-activity relationships of dietary indoles: A proposed mechanism of action as modifiers of xenobiotic metabolism. J. Toxicol. Environ. Health, 21, 311-323.
46. Grose,K.R. and Bjeldanes,L.F. (1992) Oligomerization of indole-3-carbinol in aqueous acid. Chem. Res. Toxicol., 5, 188-193.
47. Bjeldanes,L.F., Kim,J.Y., Grose,K.R., Bartholomew,J.C. and Bradfield,C.A. (1991) Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc. Natl Acad. Sci. USA, 88, 9543-9547.
48. Yusoff,P., Lao,D.H., Ong,S.H., Wong,E.S., Lim,J., Lo,T.L., Leong,H.F., Fong,C.W. and Guy,G.R. (2002) Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J. Biol. Chem., 277, 3195-3201.
49. Wu,L.W., Mayo,L.D., Dunbar,J.D., Kessler,K.M., Baerwald,M.R., Jaffe,E.A., Wang,D., Warren,R.S. and Donner,D.B. (2000) Utilization of distinct signaling pathways by receptors for vascular endothelial cell growth factor and other mitogens in the induction of endothelial cell proliferation. J. Biol. Chem., 275, 5096-5103.
50. Abedi,H. and Zachary,I. (1997) Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem., 272, 15442-15451.
51. Pouyssegur,J., Volmat,V. and Lenormand,P. (2002) Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Biochem. Pharmacol., 64, 755-763.
52. Chong,H., Vikis,H.G. and Guan,K.L. (2003) Mechanisms of regulating the Raf kinase family. Cell Signal., 15, 463-469.
53. Diaz,B., Barnard,D., Filson,A., MacDonald,S., King,A. and Marshall,M. (1997) Phosphorylation of Raf-1 serine 338-serine 339 is an essential regulatory event for Ras-dependent activation and biological signaling. Mol. Cell Biol., 17, 4509-4516.
54. Alessi,D.R., Saito,Y., Campbell,D.G., Cohen,P., Sithanandam,G., Rapp,U., Ashworth,A., Marshall,C.J. and Cowley,S. (1994) Identification of the sites in MAP kinase kinase-1 phosphorylated by p74raf-1. EMBO J., 13, 1610-1619.
55. Takahashi,T., Yamaguchi,S., Chida,K. and Shibuya,M. (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J., 20, 2768-2778.
56. Takahashi,T., Ueno,H. and Shibuya,M. (1999) VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene, 18, 2221-2230.
57. Schlessinger,J. (1993) How receptor tyrosine kinases activate Ras. Trends Biochem. Sci., 18, 273-275.
58. Downward,J. (1996) Control of ras activation. Cancer Surv., 27, 87-100.
59. Shu,X., Wu,W., Mosteller,R.D. and Broek,D. (2002) Sphingosine kinase mediates vascular endothelial growth factor-induced activation of ras and mitogen-activated protein kinases. Mol. Cell Biol., 22, 7758-7768.
60. Casey,P.J., Solski,P.A., Der,C.J. and Buss,J.E. (1989) p21ras is modified by a farnesyl isoprenoid. Proc. Natl Acad. Sci. USA, 86, 8323-8327.
61. Adachi,T., Pimentel,D.R., Heibeck,T., Hou,X., Lee,Y.J., Jiang,B., Ido,Y. and Cohen,R.A. (2004) S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J. Biol. Chem., 279, 29857-29862.
62. Fuhler,G.M., Knol,G.J., Drayer,A.L. and Vellenga,E. (2005) Impaired interleukin-8- and GRO{alpha}-induced phosphorylation of extracellular signal-regulated kinase result in decreased migration of neutrophils from patients with myelodysplasia. J. Leukoc. Biol., 77, 257-266.
63. Stupack,D.G., Cho,S.Y. and Klemke,R.L. (2000) Molecular signaling mechanisms of cell migration and invasion. Immunol. Res., 21, 83-88.
64. Nguyen,D.H., Webb,D.J., Catling,A.D., Song,Q., Dhakephalkar,A., Weber,M.J., Ravichandran,K.S. and Gonias,S.L. (2000) Urokinase-type plasminogen activator stimulates the Ras/Extracellular signal-regulated kinase (ERK) signaling pathway and MCF-7 cell migration by a mechanism that requires focal adhesion kinase, Src, and Shc. Rapid dissociation of GRB2/Sps-Shc complex is associated with the transient phosphorylation of ERK in urokinase-treated cells. J. Biol. Chem., 275, 19382-19388.
65. Nguyen,D.H., Catling,A.D., Webb,D.J., Sankovic,M., Walker,L.A., Somlyo,A.V., Weber,M.J. and Gonias,S.L. (1999) Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J. Cell Biol., 146, 149-164.
66. Klemke,R.L., Cai,S., Giannini,A.L., Gallagher,P.J., de Lanerolle,P. and Cheresh,D.A. (1997) Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol., 137, 481-492.
67. Fincham,V.J., James,M., Frame,M.C. and Winder,S.J. (2000) Active ERK/MAP kinase is targeted to newly forming cell-matrix adhesions by integrin engagement and v-Src. EMBO J., 19, 2911-2923.