3,3′-diindolylmethane inhibits angiogenesis and the growth of transplantable human breast carcinoma in athymic mice

Carcinogenesis

Volumn 26, Issue 4, 2005, Pages 771-778

  Chang, Xiaofei ^a   Tou, Janet C ^a   Hong, Chibo ^a   Kim, Hyeon A ^a   Riby, Jacques E ^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; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1B; INDOLE DERIVATIVE; MATRIGEL; UNCLASSIFIED DRUG; 3,3'-DIINDOLYLMETHANE; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOMA; CANCER GROWTH; CANCER TRANSPLANTATION; CARCINOGENESIS; CELL CULTURE; CELL CYCLE G1 PHASE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG INHIBITION; FEMALE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT; ANIMAL; BREAST TUMOR; C57BL MOUSE; CANCER INVASION; CELL MOTION; COMPARATIVE STUDY; DRUG EFFECT; DRUG SCREENING; ENDOTHELIUM CELL; HUMAN; METABOLISM; PATHOLOGY; TRANSPLANTATION; UMBILICAL VEIN; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTICARCINOGENIC AGENTS; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; ENDOTHELIAL CELLS; FEMALE; G1 PHASE; HUMANS; INDOLES; MICE; MICE, INBRED C57BL; MICE, NUDE; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; TUMOR CELLS, CULTURED; UMBILICAL VEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 17844381889     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgi018     Document Type: Article

References (48)

1. Folkman, J. (1995) Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med., 1, 27-31.
2. 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.
3. Folkman, J., Bach, M., Rowe, J.W., Davidoff, F., Lambert, P., Hirsch, C., Goldberg, A., Hiatt, H.H., Glass, J. and Henshaw, E. (1971) Tumor angiogenesis-therapeutic implications. N. Engl. J. Med., 285, 1182-1186.
4. Folkman, J. and Shing, Y. (1992) Angiogenesis. J. Biol. Chem., 267, 10931-10934.
5. Pili, R., Chang, J., Partis, R.A., Mueller, R.A., Chrest, F.J. and Passaniti, A. (1995) The alpha-glucosidase I inhibitor castanospermine alters endothelial cell glycosylation, prevents angiogenesis, and inhibits tumor growth. Cancer Res., 55, 2920-2926.
6. Folkman, J. (1975) Tumor angiogenesis: a possible control point in tumor growth. Ann. Intern. Med., 82, 96-100.
7. McDougal, A., Gupta, M.S., Ramamoorthy, K., Sun, G. and Safe, S.H. (2000) Inhibition of carcinogen-induced rat mammary tumor growth and other estrogen-dependent responses by symmetrical dihalo-substituted analogs of diindolylmethane. Cancer Lett., 151, 169-179.
8. 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-para-dioxin. Proc. Natl Acad. Sci. USA, 88, 9543-9547.
9. Bradfield, C.A. and Bjeldanes, L.F. (1987) Structure-activity relationship of dietary indoles-a proposed mechanism of action as modifiers of xenobiotic metabolism. J. Toxicol. Environ. Health, 21, 311-323.
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. Grose, K.R. and Bjeldanes, L.F. (1992) Oligomerization of indole-3-carbinol in aqueous acid. Chem. Res. Toxicol., 5, 188-193.
12. Grant, D.S., Tashiro, K., Segui-Real, B., Yamada, Y., Martin, G.R. and Kleinman, H.K. (1989) Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell, 58, 933-943.
13. Kubota, Y., Kleinman, H.K., Martin, G.R. and Lawley, T.J. (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol., 107, 1589-1598.
14. Passaniti, A., Taylor, R.M., Pili, R., Guo, Y., Long, P.V., Haney, J.A., Pauly, R.R., Grant, D.S. and Martin, G.R. (1992) A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab. Invest., 67, 519-528.
15. Tomayko, M.M. and Reynolds, C.P. (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother. Pharmacol., 24, 148-154.
16. I phase progression: cycling on cue. Cell, 79, 551-555.
17. Morgan, D.O. (1995) Principles of CDK regulation. Nature, 374, 131-134.
18. I control in mammalian cells. J. Cell Sci. Suppl., 18, 69-73.
19. I-phase progression. Genes Dev., 13, 1501-1512.
20. I events and regulation of cell-proliferation. Science, 246, 603-608.
21. Stoker, M., Oneill, C., Berryman, S. and Waxman, V. (1968) Anchorage and growth regulation in normal and virus-transformed cells. Int. J. Cancer, 3, 683-693.
22. I control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol. Cell. Biol., 15, 2600-2611.
23. I-to-S phase transition. Mol. Cell. Biol., 15, 2612-2624.
24. el Deiry, W.S., Tokino, T., Velculescu, V.E., Levy, D.B., Parsons, R., Trent, J.M., Lin, D., Mercer, W.E., Kinzler, K.W. and Vogelstein, B. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell, 75, 817-825.
25. Polyak, K., Kato, J.Y., Solomon, M.J., Sherr, C.J., Massague, J., Roberts, J.M. and Koff, A. (1994) p27Kip1, a cyclin-Cdk inhibitor, links transforming growth factor-beta and contact inhibition to cell cycle arrest. Genes Dev., 8, 9-22.
26. I cyclin-dependent kinases. Genes Dev., 9, 1149-1163.
27. Hong, C.B., Kim, H.A., Firestone, G.L. and Bjeldanes, L.F. (2002) 3,3′-Diindolylmethane (DIM) induces a G(1) cell cycle arrest in human breast cancer cells that is accompanied by Sp1-mediated activation of p21(Waf1/Cip1) expression. Carcinogenesis, 23, 1297-1305.
28. Cirri, L., Donnini, S., Morbidelli, L., Chiarugi, P., Ziche, M. and Ledda, F. (1999) Endostatin: a promising drug for antiangiogenic therapy. Int. J. Biol. Markers, 14, 263-267.
29. Moore, K.S., Wehrli, S., Roder, H., Rogers, M., Forrest, J.N., Jr, McCrimmon, D. and Zasloff, M. (1993) Squalamine: an aminosterol antibiotic from the shark. Proc. Natl Acad. Sci. USA, 90, 1354-1358.
30. Maione, T.E., Gray, G.S., Petro, J., Hunt, A.J., Donner, A.L., Bauer, S.I., Carson, H.F. and Sharpe, R.J. (1990) Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science, 247, 77-79.
31. Kusaka, M., Sudo, K., Matsutani, E., Kozai, Y., Marui, S., Fujita, T., Ingber, D. and Folkman, J. (1994) Cytostatic inhibition of endothelial-cell growth by angiogenesis inhibitor TNP-470 (AGM-1470). Br. J. Cancer, 69, 212-216.
32. Gentilini, G., Kirschbaum, N.E., Augustine, J.A., Aster, R.H. and Visentin, G.P. (1999) Inhibition of human umbilical vein endothelial cell proliferation by the CXC chemokine, platelet factor 4 (PF4), is associated with impaired downregulation of p21(Cip1/WAF1). Blood, 93, 25-33.
33. Abe, J., Zhou, W., Takuwa, N., Taguchi, J., Kurokawa, K., Kumada, M. and Takuwa, Y. (1994) A fumagillin derivative angiogenesis inhibitor, AGM-1470, inhibits activation of cyclin-dependent kinases and phosphorylation of retinoblastoma gene product but not protein tyrosyl phosphorylation or protooncogene expression in vascular endothelial cells. Cancer Res., 54, 3407-3412.
34. Hori, A., Ikeyama, S. and Sudo, K. (1994) Suppression of cyclin D1 messenger-RNA-expression by the angiogenesis inhibitor TNP-40 (AGM-1470) in vascular cells endothelial. Biochem. Biophys. Res. Commun., 204, 1067-1073.
35. Ingber, D., Fujita, T., Kishimoto, S., Sudo, K., Kanamaru, T., Brem, H. and Folkman, J. (1990) Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature, 348, 555-557.
36. Bhargava, P., Marshall, J.L., Rizvi, N., Dahut, W., Yoe, J., Figuera, M., Phipps, K., Ong, V.S., Kato, A. and Hawkins, M.J. (1999) A phase I and pharmacokinetic study of TNP-470 administered weekly to patients with advanced cancer. Clin. Cancer Res., 5, 1989-1995.
37. Kudelka, A.P., Levy, T., Verschraegen, C.F., Edwards, C.L., Piamsomboon, S., Termrungruanglert, W., Freedman, R.S., Kaplan, A.L., Kieback, D.G., Meyers, C.A., Jaeckle, K.A., Loyer, E., Steger, M., Mante, R., Mavligit, G., Killian, A., Tang, R.A., Gutterman, J.U. and Kavanagh, J.J. (1997) A phase I study of TNP-470 administered to patients with advanced squamous cell cancer of the cervix. Clin. Cancer Res., 3, 1501-1505.
38. Fotsis, T., Pepper, M., Adlercreutz, H., Hase, T., Montesano, R. and Schweigerer, L. (1995) Genistein, a dietary ingested isoflavonoid, inhibits cell proliferation and in vitro angiogenesis. J. Nutr., 125, 790S-797S.
39. Zhou, J.R., Gugger, E.T., Tanaka, T., Guo, Y., Blackburn, G.L. and Clinton, S.K. (1999) Soybean phytochemicals inhibit the growth of transplantable human prostate carcinoma and tumor angiogenesis in mice. J. Nutr., 129, 1628-1635.
40. Garbisa, S., Biggin, S., Cavallarin, N., Sartor, L., Benelli, R. and Albini, A. (1999) Tumor invasion: molecular shears blunted by green tea. Nat. Med., 5, 1216.
41. Tang, F.Y. and Meydani, M. (2001) Green tea catechins and vitamin E inhibit angiogenesis of human microvascular endothelial cells through suppression of IL-8 production. Nutr. Cancer, 41, 119-125.
42. Brakenhielm, E., Cao, R.H. and Cao, Y.H. (2001) Suppression of angiogenesis, tumor growth, and wound healing by resveratrol, a natural compound in red wine and grapes. FASEB J., 15, U568-U581.
43. Bailar, J.C. and Gornik, H.L. (1997) Cancer undefeated. N. Engl. J. Med., 336, 1569-1574.
44. Boehm, T., Folkman, J., Browder, T. and O'Reilly, M.S. (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature, 390, 404-407.
45. Kerbel, R.S. (1991) Inhibition of tumor angiogenesis as a strategy to circumvent acquired-resistance to anticancer therapeutic agents. Bioessays, 13, 31-36.
46. Klohs, W.D. and Hamby, J.M. (1999) Antiangiogenic agents. Curr. Opin. Biotechnol., 10, 544-549.
47. Holmgren, L., O'Reilly, M.S. and Folkman, J. (1995) Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med., 1, 149-153.
48. Leong, H.Y., Firestone, G.L. and Bjeldanes, L.F. (2001) Cytostatic effects of 3,3′-diindolylmethane in human endometrial cancer cells result from an estrogen receptor-mediated increase in transforming growth factor-alpha expression. Carcinogenesis, 22, 1809-1817.