1,1-Bis(3'-indolyl)-1-(p-biphenyl)methane inhibits basal-like breast cancer growth in athymic nude mice

Breast Cancer Research

Volumn 9, Issue 4, 2007, Pages

  Su, Yunpeng ^a   Vanderlaag, Kathryn ^b   Ireland, Courtney ^a   Ortiz, Janelle ^a   Grage, Henry ^c   Safe, Stephen ^b   Frankel, Arthur E ^a  

^a SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Plantacor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,1 BIS(3' INDOLYL) 1 (4 BIPHENYL)METHANE; 2 CHLORO 5 NITROBENZANILIDE; ACTIVATING TRANSCRIPTION FACTOR 3; ANTINEOPLASTIC AGENT; CAVEOLIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PLACEBO; PROTEIN P27; UNCLASSIFIED DRUG; 1,1-BIS(3'-INDOLYL)-1-(4-BIPHENYL)METHANE; CDKN1A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 1B; INDOLE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER INHIBITION; CANCER REGRESSION; CELL ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; CULTURE MEDIUM; DNA SYNTHESIS; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG MEGADOSE; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; NUDE MOUSE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; STRUCTURE ANALYSIS; SURVIVAL; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; EXPERIMENTAL NEOPLASM; IMMUNOBLOTTING; METABOLISM; MYOBLAST; NICK END LABELING; PATHOLOGY; SKELETAL MUSCLE; SURVIVAL RATE;

ANIMALS; ANTINEOPLASTIC AGENTS; CAVEOLIN 1; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; HUMANS; IMMUNOBLOTTING; IN SITU NICK-END LABELING; INDOLES; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, NUDE; MUSCLE, SKELETAL; MYOBLASTS; POLY(ADP-RIBOSE) POLYMERASES; PPAR GAMMA; SURVIVAL RATE; TUMOR CELLS, CULTURED;

EID: 36549011232     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr1761     Document Type: Article

References (67)

1. Smigal C Jemal A Ward E Cokkinides V Smith R Howe HL Thun M Trends in breast cancer by race and ethnicity: Update 2006 CA Cancer J Clin 2006, 56:168-183. 16737949
2. Carey LA Perou CM Livasy CA Dressler LG Cowan D Conway K Karaca G Troester MA Tse CK Edmiston S Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study JAMA 2006, 295:2492-2502. 10.1001/ jama.295.21.2492 16757721
3. Livasy CA Karaca G Nanda R Tretiakova MS Olopade OI Moore DT Perou CM Phenotypic evaluation of the basal-like subtype of invasive breast carcinoma Mod Pathol 2006, 19:264-271. 10.1038/modpathol.3800528 16341146
4. Turner NC Reis-Filho JS Russell AM Springall RJ Ryder K Steele D Savage K Gillett CE Schmitt FC Ashworth A BRCA1 dysfunction in sporadic basal-like breast cancer Oncogene 2007, 26:2126-2132. 10.1038/ sj.onc.1210014 17016441
5. Yehiely F Moyano JV Evans JR Nielsen TO Cryns VL Deconstructing the molecular portrait of basal-like breast cancer Trends Mol Med 2006, 12:537-544. 10.1016/j.molmed.2006.09.004 17011236
6. Caldon CE Daly RJ Sutherland RL Musgrove EA Cell cycle control in breast cancer cells J Cell Biochem 2006, 97:261-274. 10.1002/jcb.20690 16267837
7. Foulkes WD Brunet JS Stefansson IM Straume O Chappuis PO Begin LR Hamel N Goffin JR Wong N Trudel M The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer Cancer Res 2004, 64:830-835. 10.1158/0008-5472.CAN-03-2970 14871808
8. Sotgia F Williams TM Schubert W Medina F Minetti C Pestell RG Lisanti MP Caveolin-1 deficiency (-/-) conveys premalignant alterations in mammary epithelia, with abnormal lumen formation, growth factor independence, and cell invasiveness Am J Pathol 2006, 168:292-309. 1592656 16400031 10.2353/ajpath.2006.050429
9. Williams TM Sotgia F Lee H Hassan G Di Vizio D Bonuccelli G Capozza F Mercier I Rui H Pestell RG Stromal and epithelial caveolin-1 both confer a protective effect against mammary hyperplasia and tumorigenesis: caveolin-1 antagonizes cyclin D1 function in mammary epithelial cells Am J Pathol 2006, 169:1784-1801. 1780215 17071600 10.2353/ajpath.2006.060590
10. Savage K Lambros MB Robertson D Jones RL Jones C Mackay A James M Hornick JL Pereira EM Milanezi F Caveolin 1 is overexpressed and amplified in a subset of basal-like and metaplastic breast carcinomas: A morphologic, ultrastructural, immunohistochemical, and in situ hybridization analysis Clin Cancer Res 2007, 13:90-101. 10.1158/ 1078-0432.CCR-06-1371 17200343
11. Williams TM Lisanti MP Caveolin-1 in oncogenic transformation, cancer, and metastasis Am J Physiol Cell Physiol 2005, 288:C494-C506. 10.1152/ ajpcell.00458.2004 15692148
12. Rumi MA Ishihara S Kazumori H Kadowaki Y Kinoshita Y Can PPAR gamma ligands be used in cancer therapy? Curr Med Chem Anticancer Agents 2004, 4:465-477. 10.2174/1568011043352678 15579013
13. Ikezoe T Miller CW Kawano S Heaney A Williamson EA Hisatake J Green E Hofmann W Taguchi H Koeffler HP Mutational analysis of the peroxisome proliferator-activated receptor gamma gene in human malignancies Cancer Res 2001, 61:5307-5310. 11431375
14. Posch MG Zang C Mueller W Lass U von Deimling A Elstner E Somatic mutations in peroxisome proliferator-activated receptor-gamma are rare events in human cancer cells Med Sci Monit 2004, 10:BR250-BR254. 15277984
15. Jiang WG Douglas-Jones A Mansel RE Expression of peroxisome-proliferator activated receptor-gamma (PPARgamma) and the PPARgamma co-activator, PGC-1, in human breast cancer correlates with clinical outcomes Int J Cancer 2003, 106:752-757. 10.1002/ijc.11302 12866036
16. Lapillonne H Konopleva M Tsao T Gold D McQueen T Sutherland RL Madden T Andreeff M Activation of peroxisome proliferator-activated receptor gamma 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 2003, 63:5926-5939. 14522919
17. Suzuki T Hayashi S Miki Y Nakamura Y Moriya T Sugawara A Ishida T Ohuchi N Sasano H Peroxisome proliferator-activated receptor gamma in human breast carcinoma: A modulator of estrogenic actions Endocr Relat Cancer 2006, 13:233-250. 10.1677/erc.1.01075 16601291
18. Llaverias G Vazquez-Carrera M Sanchez RM Noe V Ciudad CJ Laguna JC Alegret M Rosiglitazone upregulates caveolin-1 expression in THP-1 cells through a PPAR-dependent mechanism J Lipid Res 2004, 45:2015-2024. 10.1194/jlr.M400049-JLR200 15314095
19. Demetri GD Fletcher CD Mueller E Sarraf P Naujoks R Campbell N Spiegelman BM Singer S Induction of solid tumor differentiation by the peroxisome proliferator-activated receptor-gamma ligand troglitazone in patients with liposarcoma Proc Natl Acad Sci USA 1999, 96:3951-3956. 22401 10097144 10.1073/pnas.96.7.3951
20. Mueller E Smith M Sarraf P Kroll T Aiyer A Kaufman DS Oh W Demetri G Figg WD Zhou XP Effects of ligand activation of peroxisome proliferator-activated receptor gamma in human prostate cancer Proc Natl Acad Sci USA 2000, 97:10990-10995. 27136 10984506 10.1073/pnas.180329197
21. Grau R Punzon C Fresno M Iniguez MA Peroxisome-proliferator-activated receptor alpha agonists inhibit cyclo-oxygenase 2 and vascular endothelial growth factor transcriptional activation in human colorectal carcinoma cells via inhibition of activator protein-1 Biochem J 2006, 395:81-88. 1409694 16343055 10.1042/BJ20050964
22. Grabacka M Plonka PM Urbanska K Reiss K Peroxisome proliferator-activated receptor alpha activation decreases metastatic potential of melanoma cells in vitro via down-regulation of Akt Clin Cancer Res 2006, 12:3028-3036. 10.1158/1078-0432.CCR-05-2556 16707598
23. Grabacka M Placha W Plonka PM Pajak S Urbanska K Laidler P Slominski A Inhibition of melanoma metastases by fenofibrate Arch Dermatol Res 2004, 296:54-58. 10.1007/s00403-004-0479-y 15278363
24. Suchanek KM May FJ Robinson JA Lee WJ Holman NA Monteith GR Roberts-Thomson SJ Peroxisome proliferator-activated receptor alpha in the human breast cancer cell lines MCF-7 and MDA-MB-231 Mol Carcinog 2002, 34:165-171. 10.1002/mc.10061 12203367
25. Qin C Morrow D Stewart J Spencer K Porter W Smith R III 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. 15026545
26. Chintharlapalli S Papineni S Safe S 1,1-Bis(3'-indolyl)-1-(p-substituted phenyl)methanes inhibit colon cancer cell and tumor growth through PPARgamma-dependent and PPARgamma-independent pathways Mol Cancer Ther 2006, 5:1362-1370. 10.1158/1535-7163.MCT-06-0002 16731770
27. Chintharlapalli S Papineni S Safe S 1,1-bis(3'-indolyl)-1-(p-substitutedphenyl)methanes inhibit growth, induce apoptosis, and decrease the androgen receptor in LNCaP prostate cancer cells through peroxisome proliferator-activated receptor gamma-independent pathways Mol Pharmacol 2007, 71:558-569. 10.1124/ mol.106.028696 17093136
28. Chintharlapalli S Papineni S Baek SJ Liu S Safe S 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 nonsteroidal anti-inflammatory drug-activated gene-1 Mol Pharmacol 2005, 68:1782-1792. 16155208
29. Chintharlapalli S Smith R III Samudio I Zhang W Safe S 1,1-Bis(3'-indolyl)-1-(p-substitutedphenyl)methanes induce peroxisome proliferator-activated receptor gamma-mediated growth inhibition, transactivation, and differentiation markers in colon cancer cells Cancer Res 2004, 64:5994-6001. 10.1158/0008-5472.CAN-04-0399 15342379
30. Hong J Samudio I Liu S Abdelrahim M Safe S Peroxisome proliferator-activated receptor gamma-dependent activation of p21 in Panc-28 pancreatic cancer cells involves Sp1 and Sp4 proteins Endocrinology 2004, 145:5774-5785. 10.1210/en.2004-0686 15345676
31. Abdelrahim M Newman K Vanderlaag K Samudio I Safe S 3,3'-diindolylmethane (DIM) and its derivatives induce apoptosis in pancreatic cancer cells through endoplasmic reticulum stress-dependent upregulation of DR5 Carcinogenesis 2006, 27:717-728. 10.1093/carcin/ bgi270 16332727
32. Kassouf W Chintharlapalli S Abdelrahim M Nelkin G Safe S Kamat AM Inhibition of bladder tumor growth by 1,1-bis(3'-indolyl)-1-(p-substitutedphenyl)methanes: A new class of peroxisome proliferator-activated receptor gamma agonists Cancer Res 2006, 66:412-418. 10.1158/0008-5472.CAN-05-2755 16397256
33. Lei P Abdelrahim M Safe S 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 2006, 5:2324-2336. 10.1158/1535-7163.MCT-06-0184 16985067
34. Kamal A Ali QA Syntheses of some substituted di-indolyl-methanes in aqueous medium at room temperature Tetrahedron 1963, 19:513-520. 10.1016/ S0040-4020(01)98540-0
35. Su Y Ortiz J Liu S Bugge TH Singh R Leppla SH Frankel AE Systematic urokinase-activated anthrax toxin therapy produces regressions of subcutaneous human non-small cell lung tumor in athymic nude mice Cancer Res 2007, 67:3329-3336. 10.1158/0008-5472.CAN-06-4642 17409442
36. Su Y Bakker T Harris J Tsang C Brown GD Wormald MR Gordon S Dwek RA Rudd PM Martinez-Pomares L Glycosylation influences the lectin activities of the macrophage mannose receptor J Biol Chem 2005, 280:32811-32820. 10.1074/jbc.M503457200 15983039
37. Cameron IL Sun LZ Short N Hardman WE Williams CD Therapeutic electromagnetic field (TEMF) and gamma irradiation on human breast cancer xenograft growth, angiogenesis and metastasis Cancer Cell Int 2005, 5:23. 1190196 16045802 10.1186/1475-2867-5-23
38. Hoke EM Maylock CA Shacter E Desferal inhibits breast tumor growth and does not interfere with the tumoricidal activity of doxorubicin Free Radic Biol Med 2005, 39:403-411. 10.1016/j.freeradbiomed.2005.03.029 15993339
39. Moody TW Leyton J Chan D Brenneman DC Fridkin M Gelber E Levy A Gozes I VIP receptor antagonists and chemotherapeutic drugs inhibit the growth of breast cancer cells Breast Cancer Res Treat 2001, 68:55-64. 10.1023/ A:1017994722130 11678309
40. Yee LD Williams N Wen P Young DC Lester J Johnson MV Farrar WB Walker MJ Povoski SP Suster S Pilot study of rosiglitazone therapy in women with breast cancer: Effects of short-term therapy on tumor tissue and serum markers Clin Cancer Res 2007, 13:246-252. 10.1158/1078-0432.CCR-06-1947 17200362
41. Elstner E Muller C Koshizuka K Williamson EA Park D Asou H Shintaku P Said JW Heber D Koeffler HP Ligands for peroxisome proliferator-activated receptorgamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice Proc Natl Acad Sci USA 1998, 95:8806-8811. 21158 9671760 10.1073/pnas.95.15.8806
42. Clay CE Namen AM Atsumi G Willingham MC High KP Kute TE Trimboli AJ Fonteh AN Dawson PA Chilton FH Influence of J series prostaglandins on apoptosis and tumorigenesis of breast cancer cells Carcinogenesis 1999, 20:1905-1911. 10.1093/carcin/20.10.1905 10506103
43. Clay CE Monjazeb A Thorburn J Chilton FH High KP 15-Deoxy-delta12,14-prostaglandin J2-induced apoptosis does not require PPARgamma in breast cancer cells J Lipid Res 2002, 43:1818-1828. 10.1194/ jlr.M200224-JLR200 12401880
44. Clay CE Atsumi GI High KP Chilton FH Early de novo gene expression is required for 15-deoxy-Delta 12,14-prostaglandin J2-induced apoptosis in breast cancer cells J Biol Chem 2001, 276:47131-47135. 10.1074/ jbc.C100339200 11668172
45. Belletti B Nicoloso MS Schiappacassi M Chimienti E Berton S Lovat F Colombatti A Baldassarre G p27(kip1) functional regulation in human cancer: A potential target for therapeutic designs Curr Med Chem 2005, 12:1589-1605. 10.2174/0929867054367149 16022660
46. Alkarain A Jordan R Slingerland J p27 deregulation in breast cancer: prognostic significance and implications for therapy J Mammary Gland Biol Neoplasia 2004, 9:67-80. 10.1023/B:JOMG.0000023589.00994.5e 15082919
47. Chappuis PO Kapusta L Begin LR Wong N Brunet JS Narod SA Slingerland J Foulkes WD Germline BRCA1/2 mutations and p27(Kip1) protein levels independently predict outcome after breast cancer J Clin Oncol 2000, 18:4045-4052. 11118465
48. Vanderlaag K Su Y Frankel AE Grage H Smith R 3rd 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 2007. 17624585
49. Sloan EK Stanley KL Anderson RL Caveolin-1 inhibits breast cancer growth and metastasis Oncogene 2004, 23:7893-7897. 10.1038/sj.onc.1208062 15334058
50. Burgermeister E Tencer L Liscovitch M Peroxisome proliferator-activated receptor-gamma upregulates caveolin-1 and caveolin-2 expression in human carcinoma cells Oncogene 2003, 22:3888-3900. 10.1038/sj.onc.1206625 12813462
51. Einbond LS Su T Wu HA Friedman R Wang X Jiang B Hagan T Kennelly EJ Kronenberg F Weinstein IB Gene expression analysis of the mechanisms whereby black cohosh inhibits human breast cancer cell growth Anticancer Res 2007, 27:697-712. 17465192
52. Lu D Wolfgang CD Hai T Activating transcription factor 3, a stress-inducible gene, suppresses Ras-stimulated tumorigenesis J Biol Chem 2006, 281:10473-10481. 10.1074/jbc.M509278200 16469745
53. Stearns ME Kim G Garcia F Wang M Interleukin-10 induced activating transcription factor 3 transcriptional suppression of matrix metalloproteinase-2 gene expression in human prostate CPTX-1532 cells Mol Cancer Res 2004, 2:403-416. 15280448
54. Lee SH Kim JS Yamaguchi K Eling TE Baek SJ Indole-3-carbinol and 3,3'-diindolylmethane induce expression of NAG-1 in a p53-independent manner Biochem Biophys Res Commun 2005, 328:63-69. 10.1016/ j.bbrc.2004.12.138 15670751
55. Bottone FG Jr Moon Y Kim JS Alston-Mills B Ishibashi M Eling TE The anti-invasive activity of cyclooxygenase inhibitors is regulated by the transcription factor ATF3 (activating transcription factor 3) Mol Cancer Ther 2005, 4:693-703. 10.1158/1535-7163.MCT-04-0337 15897233
56. Li PX Wong J Ayed A Ngo D Brade AM Arrowsmith C Austin RC Klamut HJ Placental transforming growth factor-beta is a downstream mediator of the growth arrest and apoptotic response of tumor cells to DNA damage and p53 overexpression J Biol Chem 2000, 275:20127-20135. 10.1074/ jbc.M909580199 10777512
57. Tan M Wang Y Guan K Sun Y PTGF-beta, a type beta transforming growth factor (TGF-beta) superfamily member, is a p53 target gene that inhibits tumor cell growth via TGF-beta signaling pathway Proc Natl Acad Sci USA 2000, 97:109-114. 26624 10618379 10.1073/pnas.97.1.109
58. Lei X Bandyopadhyay A Le T Sun L Autocrine TGFbeta supports growth and survival of human breast cancer MDA-MB-231 cells Oncogene 2002, 21:7514-7523. 10.1038/sj.onc.1205966 12386814
59. Hiraga T Myoui A Choi ME Yoshikawa H Yoneda T Stimulation of cyclooxygenase-2 expression by bone-derived transforming growth factor-beta enhances bone metastases in breast cancer Cancer Res 2006, 66:2067-2073. 10.1158/0008-5472.CAN-05-2012 16489006
60. Martin TA Parr C Davies G Watkins G Lane J Matsumoto K Nakamura T Mansel RE Jiang WG Growth and angiogenesis of human breast cancer in a nude mouse tumour model is reduced by NK4, a HGF/SF antagonist Carcinogenesis 2003, 24:1317-1323. 10.1093/carcin/bgg072 12807719
61. Singer CF Kronsteiner N Hudelist G Marton E Walter I Kubista M Czerwenka K Schreiber M Seifert M Kubista E Interleukin 1 system and sex steroid receptor expression in human breast cancer: Interleukin 1alpha protein secretion is correlated with malignant phenotype Clin Cancer Res 2003, 9:4877-4883. 14581361
62. Hjortoe GM Petersen LC Albrektsen T Sorensen BB Norby PL Mandal SK Pendurthi UR Rao LV Tissue factor-factor VIIa-specific up-regulation of IL-8 expression in MDA-MB-231 cells is mediated by PAR-2 and results in increased cell migration Blood 2004, 103:3029-3037. 10.1182/ blood-2003-10-3417 15070680
63. Calabro P Samudio I Safe SH Willerson JT Yeh ET Inhibition of tumor-necrosis-factor-alpha induced endothelial cell activation by a new class of PPAR-gamma agonists. An in vitro study showing receptor-independent effects J Vasc Res 2005, 42:509-516. 10.1159/ 000088260 16155367
64. Elstner E Muller C Koshizuka K Williamson EA Park D Asou H Shintaku P Said JW Heber D Koeffler HP Ligands for peroxisome proliferator-activated receptorgamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice Proc Natl Acad Sci USA 1998, 95:8806-8811. 21158 9671760 10.1073/pnas.95.15.8806
65. Gerhold DL Liu F Jiang G Li Z Xu J Lu M Sachs JR Bagchi A Fridman A Holder DJ Gene expression profile of adipocyte differentiation and its regulation by peroxisome proliferator-activated receptor-gamma agonists Endocrinology 2002, 143:2106-2118. 10.1210/en.143.6.2106 12021175
66. Schadinger SE Bucher NL Schreiber BM Farmer SR PPARgamma2 regulates lipogenesis and lipid accumulation in steatotic hepatocytes Am J Physiol Endocrinol Metab 2005, 288:E1195-E1205. 10.1152/ajpendo.00513.2004 15644454
67. Dobrian AD The complex role of PPARgamma in renal dysfunction in obesity: Managing a Janus-faced receptor Vascul Pharmacol 2006, 45:36-45. 10.1016/j.vph.2006.01.017 16716756