3,3'-Diindolylmethane (DIM) inhibits the growth and invasion of drug-resistant human cancer cells expressing EGFR mutants

Cancer Letters

Volumn 295, Issue 1, 2010, Pages 59-68

  Rahimi, Massod ^a   Huang, Kai Ling ^a   Tang, Careen K ^a  

^a GEORGETOWN UNIVERSITY   (United States)

Author keywords

DIM; Drug resistance; EGFR; Growth; Invasion; Mutants

Indexed keywords

3,3' DIINDOLYLMETHANE; EPIDERMAL GROWTH FACTOR RECEPTOR; GROWTH FACTOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL STRAIN MCF 7; CONTROLLED STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SOLID TUMOR;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, ERBB-1; GLIOMA; HUMANS; INDOLES; MUTANT PROTEINS; MUTATION; NEOPLASM INVASIVENESS; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 77953614022     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.02.014     Document Type: Article

References (54)

1. Schmidt M., Lichtner R.B. EGF receptor targeting in therapy-resistant human tumors. Drug Resist. Update 2002, 5:11-18.
2. Chan S.K., Hill M.E., Gullick W.J. The role of the epidermal growth factor receptor in breast cancer. J. Mammary Gland Biol. Neoplasia 2006, 11:3-11.
3. Gee J.M., Robertson J.F., Gutteridge E., Ellis I.O., Pinder S.E., Rubini M., Nicholson R.I. Epidermal growth factor receptor/HER2/insulin-like growth factor receptor signalling and oestrogen receptor activity in clinical breast cancer. Endocr. Relat. Cancer 2005, 12(Suppl. 1):S99-S111.
4. Chakravarti A., Dicker A., Mehta M. The contribution of epidermal growth factor receptor (EGFR) signaling pathway to radioresistance in human gliomas: a review of preclinical and correlative clinical data. Int. J. Radiat. Oncol. Biol. Phys. 2004, 58:927-931.
5. Huang P.H., Cavenee W.K., Furnari F.B., White F.M. Uncovering therapeutic targets for glioblastoma: a systems biology approach. Cell Cycle 2007, 6:2750-2754.
6. Lynch T.J., Bell D.W., Sordella R., Gurubhagavatula S., Okimoto R.A., Brannigan B.W., Harris P.L., Haserlat S.M., Supko J.G., Haluska F.G., Louis D.N., Christiani D.C., Settleman J., Haber D.A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. New Engl. J. Med. 2004, 350:2129-2139.
7. Paez J.G., Janne P.A., Lee J.C., Tracy S., Greulich H., Gabriel S., Herman P., Kaye F.J., Lindeman N., Boggon T.J., Naoki K., Sasaki H., Fujii Y., Eck M.J., Sellers W.R., Johnson B.E., Meyerson M. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004, 304:1497-1500.
8. Pao W., Miller V., Zakowski M., Doherty J., Politi K., Sarkaria I., Singh B., Heelan R., Rusch V., Fulton L., Mardis E., Kupfer D., Wilson R., Kris M., Varmus H. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl. Acad. Sci. USA 2004, 101:13306-13311.
9. Sordella R., Bell D.W., Haber D.A., Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004, 305:1163-1167.
10. Higdon J.V., Delage B., Williams D.E., Dashwood R.H. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol. Res. 2007, 55:224-236.
11. Safe S., Papineni S., Chintharlapalli S. Cancer chemotherapy with indole-3-carbinol, bis(3'-indolyl)methane and synthetic analogs. Cancer Lett. 2008, 269:326-338.
12. Chen I., McDougal A., Wang F., Safe S. Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 1998, 19:1631-1639.
13. Ichite N., Chougule M.B., Jackson T., Fulzele S.V., Safe S., Singh M. Enhancement of docetaxel anticancer activity by a novel diindolylmethane compound in human non-small cell lung cancer. Clin. Cancer Res. 2009, 15:543-552.
14. Kassie F., Anderson L.B., Scherber R., Yu N., Lahti D., Upadhyaya P., Hecht S.S. Indole-3-carbinol inhibits 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone plus benzo(a)pyrene-induced lung tumorigenesis in A/J mice and modulates carcinogen-induced alterations in protein levels. Cancer Res. 2007, 67:6502-6511.
15. McDougal A., Gupta M.S., Morrow D., Ramamoorthy K., Lee J.E., Safe S.H. Methyl-substituted diindolylmethanes as inhibitors of estrogen-induced growth of T47D cells and mammary tumors in rats. Breast Cancer Res. Treat. 2001, 66:147-157.
16. Qin C., Morrow D., Stewart J., Spencer K., Porter W., Smith R., Phillips T., Abdelrahim M., Samudio I., Safe S. A new class of peroxisome proliferator-activated receptor gamma (PPARgamma) agonists that inhibit growth of breast cancer cells: 1,1-bis(3'-indolyl)-1-(p-substituted phenyl)methanes. Mol. Cancer Ther. 2004, 3:247-260.
17. Chang X., Tou J.C., Hong C., Kim H.A., Riby J.E., Firestone G.L., Bjeldanes L.F. 3,3'-Diindolylmethane inhibits angiogenesis and the growth of transplantable human breast carcinoma in athymic mice. Carcinogenesis 2005, 26:771-778.
18. McGuire K.P., Ngoubilly N., Neavyn M., Lanza-Jacoby S. 3,3'-Diindolylmethane and paclitaxel act synergistically to promote apoptosis in HER2/Neu human breast cancer cells. J. Surg. Res. 2006, 132:208-213.
19. Rahman K.M., Ali S., Aboukameel A., Sarkar S.H., Wang Z., Philip P.A., Sakr W.A., Raz A. Inactivation of NF-kappaB by 3,3'-diindolylmethane contributes to increased apoptosis induced by chemotherapeutic agent in breast cancer cells. Mol. Cancer Ther. 2007, 6:2757-2765.
20. Firestone G.L., Bjeldanes L.F. Indole-3-carbinol and 3,3'-diindolylmethane antiproliferative signaling pathways control cell-cycle gene transcription in human breast cancer cells by regulating promoter-Sp1 transcription factor interactions. J. Nutr. 2003, 133:2448S-2455S.
21. Hong C., Kim H.A., Firestone G.L., Bjeldanes L.F. 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 2002, 23:1297-1305.
22. Rahman K.W., Li Y., Wang Z., Sarkar S.H., Sarkar F.H. Gene expression profiling revealed survivin as a target of 3,3'-diindolylmethane-induced cell growth inhibition and apoptosis in breast cancer cells. Cancer Res. 2006, 66:4952-4960.
23. Vanderlaag K., Samudio I., Burghardt R., Barhoumi R., Safe S. Inhibition of breast cancer cell growth and induction of cell death by 1,1-bis(3'-indolyl)methane (DIM) and 5,5'-dibromoDIM. Cancer Lett. 2006, 236:198-212.
24. Vanderlaag K., Su Y., Frankel A.E., Grage H., Smith R., Khan S., Safe S. 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes inhibit proliferation of estrogen receptor-negative breast cancer cells by activation of multiple pathways. Breast Cancer Res. Treat. 2008, 109:273-283.
25. Wang Z., Yu B.W., Rahman K.M., Ahmad F., Sarkar F.H. Induction of growth arrest and apoptosis in human breast cancer cells by 3,3-diindolylmethane is associated with induction and nuclear localization of p27kip. Mol. Cancer Ther. 2008, 7:341-349.
26. Hong C., Firestone G.L., Bjeldanes L.F. Bcl-2 family-mediated apoptotic effects of 3,3'-diindolylmethane (DIM) in human breast cancer cells. Biochem. Pharmacol. 2002, 63:1085-1097.
27. Riby J.E., Xue L., Chatterji U., Bjeldanes E.L., Firestone G.L., Bjeldanes L.F. Activation and potentiation of interferon-gamma signaling by 3,3'-diindolylmethane in MCF-7 breast cancer cells. Mol. Pharmacol. 2006, 69:430-439.
28. Wang T.T., Milner M.J., Milner J.A., Kim Y.S. Estrogen receptor alpha as a target for indole-3-carbinol. J. Nutr. Biochem. 2006, 17:659-664.
29. Xue L., Firestone G.L., Bjeldanes L.F. DIM stimulates IFNgamma gene expression in human breast cancer cells via the specific activation of JNK and p38 pathways. Oncogene 2005, 24:2343-2353.
30. Rahman K.W., Sarkar F.H. Inhibition of nuclear translocation of nuclear factor-{kappa}B contributes to 3,3'-diindolylmethane-induced apoptosis in breast cancer cells. Cancer Res. 2005, 65:364-371.
31. Ali S., Banerjee S., Ahmad A., El-Rayes B.F., Philip P.A., Sarkar F.H. Apoptosis-inducing effect of erlotinib is potentiated by 3,3'-diindolylmethane in vitro and in vivo using an orthotopic model of pancreatic cancer. Mol. Cancer Ther. 2008, 7:1708-1719.
32. Li Y., Chinni S.R., Sarkar F.H. Selective growth regulatory and pro-apoptotic effects of DIM is mediated by AKT and NF-kappaB pathways in prostate cancer cells. Front. Biosci. 2005, 10:236-243.
33. Moiseeva E.P., Heukers R., Manson M.M. EGFR and Src are involved in indole-3-carbinol-induced death and cell cycle arrest of human breast cancer cells. Carcinogenesis 2007, 28:435-445.
34. Tang C.K., Gong X.Q., Moscatello D.K., Wong A.J., Lippman M.E. Epidermal growth factor receptor vIII enhances tumorigenicity in human breast cancer. Cancer Res. 2000, 60:3081-3087.
35. Zhang Y., Su H., Rahimi M., Tochihara R., Tang C. EGFRvIII-induced estrogen-independence, tamoxifen-resistance phenotype correlates with PgR expression and modulation of apoptotic molecules in breast cancer. Int. J. Cancer 2009, 125:2021-2028.
36. Eder J.P., Vande Woude G.F., Boerner S.A., LoRusso P.M. Novel therapeutic inhibitors of the c-Met signaling pathway in cancer. Clin. Cancer Res. 2009, 15:2207-2214.
37. Kong D.S., Song S.Y., Kim D.H., Joo K.M., Yoo J.S., Koh J.S., Dong S.M., Suh Y.L., Lee J.I., Park K., Kim J.H., Nam D.H. Prognostic significance of c-Met expression in glioblastomas. Cancer 2009, 115:140-148.
38. Ross J.S., Slodkowska E.A., Symmans W.F., Pusztai L., Ravdin P.M., Hortobagyi G.N. The HER-2 receptor and breast cancer: 10years of targeted anti-HER-2 therapy and personalized medicine. Oncologist 2009, 14:320-368.
39. Chen H.J., Mok T.S., Chen Z.H., Guo A.L., Zhang X.C., Su J., Wu Y.L. Clinicopathologic and molecular features of epidermal growth factor receptor T790M mutation and c-MET amplification in tyrosine kinase inhibitor-resistant Chinese non-small cell lung cancer. Pathol. Oncol. Res. 2009.
40. Engelman J.A., Zejnullahu K., Mitsudomi T., Song Y., Hyland C., Park J.O., Lindeman N., Gale C.M., Zhao X., Christensen J., Kosaka T., Holmes A.J., Rogers A.M., Cappuzzo F., Mok T., Lee C., Johnson B.E., Cantley L.C., Janne P.A. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007, 316:1039-1043.
41. Khwaja F.S., Wynne S., Posey I., Djakiew D. 3,3'-Diindolylmethane induction of p75NTR-dependent cell death via the p38 mitogen-activated protein kinase pathway in prostate cancer cells. Cancer Prev. Res. (Phila Pa) 2009, 2:566-571.
42. Vivar O.I., Lin C.L., Firestone G.L., Bjeldanes L.F. 3,3'-Diindolylmethane induces a G(1) arrest in human prostate cancer cells irrespective of androgen receptor and p53 status. Biochem. Pharmacol. 2009, 78:469-476.
43. Cai X.M., Tao B.B., Wang L.Y., Liang Y.L., Jin J.W., Yang Y., Hu Y.L., Zha X.L. Protein phosphatase activity of PTEN inhibited the invasion of glioma cells with epidermal growth factor receptor mutation type III expression. Int. J. Cancer 2005, 117:905-912.
44. Choe G., Park J.K., Jouben-Steele L., Kremen T.J., Liau L.M., Vinters H.V., Cloughesy T.F., Mischel P.S. Active matrix metalloproteinase 9 expression is associated with primary glioblastoma subtype. Clin. Cancer Res. 2002, 8:2894-2901.
45. Damstrup L., Wandahl P.M., Bastholm L., Elling F., Skovgaard P.H. Epidermal growth factor receptor mutation type III transfected into a small cell lung cancer cell line is predominantly localized at the cell surface and enhances the malignant phenotype. Int. J. Cancer 2002, 97:7-14.
46. Lal A., Glazer C.A., Martinson H.M., Friedman H.S., Archer G.E., Sampson J.H., Riggins G.J. Mutant epidermal growth factor receptor up-regulates molecular effectors of tumor invasion. Cancer Res. 2002, 62:3335-3339.
47. Yu H., Gong X., Luo X., Han W., Hong G., Singh B., Tang C.K. Co-expression of EGFRvIII with ErbB-2 enhances tumorigenesis: EGFRvIII mediated constitutively activated and sustained signaling pathways, whereas EGF-induced a transient effect on EGFR-mediated signaling pathways. Cancer Biol. Ther. 2008, 7.
48. Han W., Zhang T., Yu H., Foulke J.G., Tang C.K. Hypophosphorylation of residue Y1045 leads to defective downregulation of EGFRvIII. Cancer Biol. Ther. 2006, 5:1361-1368.
49. Karamouzis M.V., Konstantinopoulos P.A., Papavassiliou A.G. Targeting MET as a strategy to overcome crosstalk-related resistance to EGFR inhibitors. Lancet Oncol. 2009, 10:709-717.
50. Lal B., Goodwin C.R., Sang Y., Foss C.A., Cornet K., Muzamil S., Pomper M.G., Kim J., Laterra J. EGFRvIII and c-Met pathway inhibitors synergize against PTEN-null/EGFRvIII+glioblastoma xenografts. Mol. Cancer Ther. 2009, 8:1751-1760.
51. Kinkade C.W., Castillo-Martin M., Puzio-Kuter A., Yan J., Foster T.H., Gao H., Sun Y., Ouyang X., Gerald W.L., Cordon-Cardo C., bate-Shen C. Targeting AKT/mTOR and ERK MAPK signaling inhibits hormone-refractory prostate cancer in a preclinical mouse model. J. Clin. Invest. 2008, 118:3051-3064.
52. Frey M.R., Dise R.S., Edelblum K.L., Polk D.B. p38 Kinase regulates epidermal growth factor receptor downregulation and cellular migration. EMBO J. 2006, 25:5683-5692.
53. Vergarajauregui S., San M.A., Puertollano R. Activation of p38 mitogen-activated protein kinase promotes epidermal growth factor receptor internalization. Traffic 2006, 7:686-698.
54. Hsu E.L., Chen N., Westbrook A., Wang F., Zhang R., Taylor R.T., Hankinson O. CXCR4 and CXCL12 down-regulation: a novel mechanism for the chemoprotection of 3,3'-diindolylmethane for breast and ovarian cancers. Cancer Lett. 2008, 265:113-123.