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 Research and Treatment

Volumn 109, Issue 2, 2008, Pages 273-283

  Vanderlaag, Kathy ^a   Su, Yunpeng ^b   Frankel, Arthur E ^b   Grage, Henry ^c   Smith III, Roger ^a   Khan, Shaheen ^a   Safe, Stephen ^a,d  

^a TEXAS A AND M UNIVERSITY   (United States)

^b SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^c Plantacor   (United States)

^d TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

Author keywords

Breast cancer; C DIMs; ER negative; Growth inhibition; PPAR

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN D1; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; NONSTEROID ANTIINFLAMMATORY DRUG ACTIVATED GENE 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLACEBO; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CYTOTOXICITY; DOWN REGULATION; DRUG INHIBITION; FEMALE; GENE SEQUENCE; IN VITRO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PRIORITY JOURNAL; SYSTEMATIC REVIEW;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOKINES; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; HUMANS; INDOLES; MICE; MICE, NUDE; PPAR GAMMA; PROTEIN KINASES; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 43149087555     PISSN: 01676806     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10549-007-9648-y     Document Type: Article

References (47)

1. Desvergne B, Wahli W (1999) Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 20:649-688
2. Escher P, Wahli W (2000) Peroxisome proliferator-activated receptors: insight into multiple cellular functions. Mutat Res 448:121-138
3. Willson TM, Lambert MH, Kliewer SA (2001) Peroxisome proliferator- activated receptor g and metabolic disease. Annu Rev Biochem 70:341-367
4. Fajas L, Debril MB, Auwerx J (2001) Peroxisome proliferator-activated receptor-g: from adipogenesis to carcinogenesis. J Mol Endocrinol 27:1-9
5. Lee CH, Olson P, Evans RM (2003) Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144:2201-2207
6. Rosen ED, Spiegelman BM (2001) PPARg: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276:37731-37734
7. Ikezoe T, Miller CW, Kawano S, Heaney A, Williamson EA, Hisatake J, Green E, Hofmann W, Taguchi H, Koeffler HP (2001) Mutational analysis of the peroxisome proliferator-activated receptor g gene in human malignancies. Cancer Res 61:5307-5310
8. Posch MG, Zang C, Mueller W, Lass U, von DA, Elstner E (2004) Somatic mutations in peroxisome proliferator-activated receptor-g are rare events in human cancer cells. Med Sci Monit 10:BR250-BR254
9. Acton JJ III, Black RM, Jones AB, Moller DE, Colwell L, Doebber TW, Macnaul KL, Berger J, Wood HB (2005) Benzoyl 2-methyl indoles as selective PPARg modulators. Bioorg Med Chem Lett 15:357-362
10. Berger JP, Petro AE, Macnaul KL, Kelly LJ, Zhang BB, Richards K, Elbrecht A, Johnson BA, Zhou G, Doebber TW, Biswas C, Parikh M, Sharma N, Tanen MR, Thompson GM, Ventre J, Adams AD, Mosley R, Surwit RS, Moller DE (2003) Distinct properties and advantages of a novel peroxisome proliferator-activated protein g selective modulator. Mol Endocrinol 17:662-676
11. Koyama H, Miller DJ, Boueres JK, Desai RC, Jones AB, Berger JP, Macnaul KL, Kelly LJ, Doebber TW, Wu MS, Zhou G, Wang PR, Ippolito MC, Chao YS, Agrawal AK, Franklin R, Heck JV, Wright SD, Moller DE, Sahoo SP (2004) (2R)-2-ethylchromane-2-carboxylic acids: discovery of novel PPARa/g dual agonists as antihyperglycemic and hypolipidemic agents. J Med Chem 47:3255-3263
12. Liu K, Black RM, Acton III JJ, Mosley R, Debenham S, Abola R, Yang M, Tschirret-Guth R, Colwell L, Liu C, Wu M, Wang CF, Macnaul KL, McCann ME, Moller DE, Berger JP, Meinke PT, Jones AB, Wood HB (2005) Selective PPARg modulators with improved pharmacological profiles. Bioorg Med Chem Lett 15:2437-2440
13. Qin C, Morrow D, Stewart J, Spencer K, Porter W, Smith III R, Phillips T, Abdelrahim M, Samudio I, Safe S (2004) A new class of peroxisome proliferator-activated receptor g (PPARg) agonists that inhibit growth of breast cancer cells: 1,1-bis(3'-indolyl)-1-(p-substitutedphenyl)methanes. Mol Cancer Therap 3:247-259
14. Rieusset J, Touri F, Michalik L, Escher P, Desvergne B, Niesor E, Wahli W (2002) A new selective peroxisome proliferator-activated receptor g antagonist with antiobesity and antidiabetic activity. Mol Endocrinol 16:2628-2644
15. Schopfer FJ, Lin Y, Baker PR, Cui T, Garcia-Barrio M, Zhang J, Chen K, Chen YE, Freeman BA (2005) Nitrolinoleic acid: an endogenous peroxisome proliferator-activated receptor g ligand. Proc Natl Acad Sci USA 102:2340-2345
16. Suh N, Wang Y, Honda T, Gribble GW, Dmitrovsky E, Hickey WF, Maue RA, Place AE, Porter DM, Spinella MJ, Williams CR, Wu G, Dannenberg AJ, Flanders KC, Letterio JJ, Mangelsdorf DJ, Nathan CF, Nguyen L, Porter WW, Ren RF, Roberts AB, Roche NS, Subbaramaiah K, Sporn MB (1999) A novel synthetic oleanane triterpenoid, 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid, with potent differentiating, antiproliferative, and anti-inflammatory activity. Cancer Res 59:336-341
17. Chintharlapalli S, Papineni S, Konopleva M, Andreef M, Samudio I, Safe S (2005c) 2-Cyano-3,12-dioxoolean-1,9-dien-28-oic acid and related compounds inhibit growth of colon cancer cells through peroxisome proliferator-activated receptor g-dependent and -independent pathways. Mol Pharmacol 68:119-128
18. Ikeda T, Sporn M, Honda T, Gribble GW, Kufe D (2003) The novel triterpenoid CDDO and its derivatives induce apoptosis by disruption of intracellular redox balance. Cancer Res 63:5551-5558
19. Ito Y, Pandey P, Place A, Sporn MB, Gribble GW, Honda T, Kharbanda S, Kufe D (2000) The novel triterpenoid 2-cyano-3,12-dioxoolean-1,9-dien-28-oic acid induces apoptosis of human myeloid leukemia cells by a caspase-8-dependent mechanism. Cell Growth Differ 11:261-267
20. Konopleva M, Tsao T, Estrov Z, Lee RM, Wang RY, Jackson CE, McQueen T, Monaco G, Munsell M, Belmont J, Kantarjian H, Sporn MB, Andreeff M (2004b) The synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces caspase-dependent and -independent apoptosis in acute myelogenous leukemia. Cancer Res 64:7927-7935
21. Konopleva M, Elstner E, McQueen TJ, Tsao T, Sudarikov A, Hu W, Schober WD, Wang RY, Chism D, Kornblau SM, Younes A, Collins SJ, Koeffler HP, Andreeff M (2004a) Peroxisome proliferator-activated receptor g and retinoid X receptor ligands are potent inducers of differentiation and apoptosis in leukemias. Mol Cancer Ther 3:1249-1262
22. Lapillonne H, Konopleva M, Tsao T, Gold D, McQueen T, Sutherland RL, Madden T, Andreeff M (2003) Activation of peroxisome proliferator-activated receptor g by a novel synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien- 28-oic acid induces growth arrest and apoptosis in breast cancer cells. Cancer Res 63:5926-5939
23. Samudio I, Konopleva M, Hail Jr N, Shi YX, McQueen T, Hsu T, Evans R, Honda T, Gribble GW, Sporn M, Gilbert HF, Safe S, Andreeff M (2005) 2-Cyano-3,12 dioxooleana-1,9 diene-28-imidazolide (CDDO-Im) directly targets mitochondrial glutathione to induce apoptosis in pancreatic cancer. J Biol Chem 280:36273-36282
24. Abdelrahim M, Newman K, Vanderlaag K, Samudio I, Safe S (2006) 3,3'-Diindolylmethane (DIM) and derivatives induce apoptosis in pancreatic cancer cells through endoplasmic reticulum stress-dependent upregulation of DR5. Carcinogenesis 27:717-728
25. Chintharlapalli S, Smith III R, Samudio I, Zhang W, Safe S (2004) 1,1-Bis(3'-indolyl)-1-(p-substitutedphenyl)methanes induce peroxisome proliferator-activated receptor g-mediated growth inhibition, transactivation and differentiation markers in colon cancer cells. Cancer Res 64:5994-6001
26. Chintharlapalli S, Papineni S, Baek SJ, Liu S, Safe S (2005b) 1,1-Bis(3'-indolyl)-1-(p-substitutedphenyl)methanes are peroxisome proliferator-activated receptor gamma agonists but decrease HCT-116 colon cancer cell survival through receptor-independent activation of early growth response-1 and NAG-1. Mol Pharmacol 68:1782-1792
27. Chintharlapalli S, Burghardt R, Papineni S, Ramaiah S, Yoon K, Safe S (2005a) Activation of Nur77 by selected 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes induces apoptosis through nuclear pathways. J Biol Chem 280:24903-24914
28. Chintharlapalli S, Papineni S, Safe S (2006) 1,1-Bis(3'-indolyl)-1-(p- substituted phenyl)methanes inhibit colon cancer cell and tumor growth through PPARg-dependent and PPARg-independent pathways. Mol Cancer Ther 5:1362-1370
29. Contractor R, Samudio I, Estrov Z, Harris D, McCubrey JA, Safe S, Andreeff M, Konopleva M (2005) A novel ring-substituted diindolylmethane 1,1-bis[3'-(5-methoxyindolyl)]-1-(p-t-butylphenyl)methane inhibits ERK activation and induces apoptosis in acute myeloid leukemia. Cancer Res 65:2890-2898
30. Hong J, Samudio I, Liu S, Abdelrahim M, Safe S (2004) Peroxisome proliferator-activated receptor g-dependent activation of p21 in Panc-28 pancreatic cancer cells involves Sp1 and Sp4 proteins. Endocrinology 145:5774-5785
31. Kassouf W, Chintharlapalli S, Abdelrahim M, Nelkin G, Safe S, Kamat AM (2006) Inhibition of bladder tumor growth by 1,1-bis(3'-indolyl)-1-(p- substitutedphenyl)methanes: a new class of peroxisome proliferator-activated receptor g agonists. Cancer Res 66:412-418
32. Lei P, Abdelrahim M, Safe S (2006) 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes inhibit ovarian cancer cell growth through peroxisome proliferator-activated receptor-dependent and independent pathways. Mol Cancer Ther 5:2324-2336
33. Baek SJ, Wilson LC, Hsi LC, Eling TE (2003) Troglitazone, a peroxisome proliferator-activated receptor g (PPARg) ligand, selectively induces the early growth response-1 gene independently of PPARg. A novel mechanism for its anti-tumorigenic activity. J Biol Chem 278:5845-5853
34. Baek SJ, Kim KS, Nixon JB, Wilson LC, Eling TE (2001) Cyclooxygenase inhibitors regulate the expression of a TGF-b superfamily member that has proapoptotic and antitumorigenic activities. Mol Pharmacol 59:901-908
35. Baek SJ, Kim JS, Nixon JB, DiAugustine RP, Eling TE (2004) Expression of NAG-1, a transforming growth factor-b superfamily member, by troglitazone requires the early growth response gene EGR-1. J Biol Chem 279:6883-6892
36. Lee SH, Kim JS, Yamaguchi K, Eling TE, Baek SJ (2005) Indole-3-carbinol and 3,3'-diindolylmethane induce expression of NAG-1 in a p53-independent manner. Biochem Biophys Res Commun 328:63-69
37. Shim M, Eling TE (2005) Protein kinase C-dependent regulation of NAG-1/placental bone morphogenic protein/MIC-1 expression in LNCaP prostate carcinoma cells. J Biol Chem 280:18636-18642
38. Vanderlaag K, Samudio I, Burghardt R, Barhoumi R, Safe S (2006) 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 236:198-212
39. Clay CE, Namen AM, Atsumi G, Willingham MC, High KP, Kute TE, Trimboli AJ, Fonteh AN, Dawson PA, Chilton FH (1999) Influence of J series prostaglandins on apoptosis and tumorigenesis of breast cancer cells. Carcinogenesis 20:1905-1911
40. Clay CE, Monjazeb A, Thorburn J, Chilton FH, High KP (2002) 15-Deoxy-D(12,14)-prostaglandin J2-induced apoptosis does not require PPARg in breast cancer cells. J Lipid Res 43:1818-1828
41. Hyer ML, Croxton R, Krajewska M, Krajewski S, Kress CL, Lu M, Suh N, Sporn MB, Cryns VL, Zapata JM, Reed JC (2005) Synthetic triterpenoids cooperate with tumor necrosis factor-related apoptosis-inducing ligand to induce apoptosis of breast cancer cells. Cancer Res 65:4799-4808
42. Konopleva M, Zhang W, Shi YX, McQueen T, Tsao T, Abdelrahim M, Munsell MF, Johansen M, Yu D, Madden T, Safe SH, Hung MC, Andreeff M (2006) Synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid induces growth arrest in HER2-overexpressing breast cancer cells. Mol Cancer Ther 5:317-328
43. Patel L, Pass I, Coxon P, Downes CP, Smith SA, Macphee CH (2001) Tumor suppressor and anti-inflammatory actions of PPARg agonists are mediated via upregulation of PTEN. Curr Biol 11:764-768
44. Pignatelli M, Cortes-Canteli M, Lai C, Santos A, Perez-Castillo A (2001) The peroxisome proliferator-activated receptor g is an inhibitor of ErbBs activity in human breast cancer cells. J Cell Sci 114:4117-4126
45. Qin C, Burghardt R, Smith R, Wormke M, Stewart J, Safe S (2003) Peroxisome proliferator-activated receptor g (PPARg) agonists induce proteasome-dependent degradation of cyclin D1 and estrogen receptor a in MCF-7 breast cancer cells. Cancer Res 63:958-964
46. Wang CG, Fu MF, D'Amico M, Albanese C, Zhou JN, Brownlee M, Lisanti MP, Chatterjee VKK, Lazar MA, Pestell RG (2001) Inhibition of cellular proliferation through IkB kinase-independent and peroxisome proliferator-activated receptor g-dependent repression of cyclin D1. Mol Cell Biol 21:3057-3070
47. Lu M, Kwan T, Yu C, Chen F, Freedman B, Schafer JM, Lee EJ, Jameson JL, Jordan VC, Cryns VL (2005) Peroxisome proliferator-activated receptor g agonists promote TRAIL-induced apoptosis by reducing survivin levels via cyclin D3 repression and cell cycle arrest. J Biol Chem 280:6742-6751