Metformin attenuates transforming growth factor beta (TGF-β) mediated oncogenesis in mesenchymal stem-like/claudin-low triple negative breast cancer

References

• Cheang MC, Voduc D, Bajdik C, Leung S, McKinney S, Chia SK, Perou CM, Nielsen TO. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 2008; 14(5):1368-76; PMID:18316557; http://dx.doi.org/10.1158/1078-0432.CCR-07-1658
   PubMed Web of Science ®Google Scholar
• Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med 2010; 363(20):1938-48; PMID:21067385; http://dx.doi.org/10.1056/NEJMra1001389
   PubMed Web of Science ®Google Scholar
• Lehmann BD, Pietenpol JA. Identification and use of biomarkers in treatment strategies for triple-negative breast cancer subtypes. J Pathol 2014; 232(2):142-50; PMID:24114677; http://dx.doi.org/10.1002/path.4280
   PubMed Web of Science ®Google Scholar
• Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121(7):2750-67; PMID:21633166; http://dx.doi.org/10.1172/JCI45014
   PubMed Web of Science ®Google Scholar
• Perou CM. Molecular stratification of triple-negative breast cancers. Oncologist 2010; 15 Supp l5:39-48; PMID:21138954; http://dx.doi.org/10.1634/theoncologist.2010-S5-39
   PubMed Web of Science ®Google Scholar
• Sabatier R, Finetti P, Guille A, Adelaide J, Chaffanet M, Viens P, Birnbaum D, Bertucci F. Claudin-low breast cancers: clinical, pathological, molecular and prognostic characterization. Mol Cancer 2014; 13:228; http://dx.doi.org/10.1186/1476-4598-13-228
   PubMed Web of Science ®Google Scholar
• Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X, Perou CM. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12(5):R68; PMID:20813035; http://dx.doi.org/10.1186/bcr2635
   PubMed Web of Science ®Google Scholar
• Cleator S, Heller W, Coombes RC. Triple-negative breast cancer: therapeutic options. Lancet Oncol 2007; 8(3):235-44; PMID:17329194; http://dx.doi.org/10.1016/S1470-2045(07)70074-8
   PubMed Web of Science ®Google Scholar
• Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, Harris CC, McLellan MD, Fulton RS, Fulton LL, et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010; 464(7291):999-1005; PMID:20393555; http://dx.doi.org/10.1038/nature08989
   PubMed Web of Science ®Google Scholar
• Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A 2001; 98(19):10869-74
   PubMed Web of Science ®Google Scholar
• Weigman VJ, Chao HH, Shabalin AA, He X, Parker JS, Nordgard SH, Grushko T, Huo D, Nwachukwu C, Nobel A, et al., Basal-like Breast cancer DNA copy number losses identify genes involved in genomic instability, response to therapy, and patient survival. Breast Cancer Res Treat 2011; 133(3):865-80.; PMID:22048815
   PubMed Web of Science ®Google Scholar
• Network TCGA. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490(7418):61-70; PMID:23000897; http://dx.doi.org/10.1038/nature11412
   PubMed Web of Science ®Google Scholar
• Massague J. TGFbeta in Cancer. Cell 2008; 134(2):215-30; PMID:18662538; http://dx.doi.org/10.1016/j.cell.2008.07.001
   PubMed Web of Science ®Google Scholar
• Blobe GC, Schiemann WP, Lodish HF. Role of transforming growth factor β in human disease. N Engl J Med 2000; 342(18):1350-8; PMID:10793168; http://dx.doi.org/10.1056/NEJM200005043421807
   PubMed Web of Science ®Google Scholar
• Picon A, Gold LI, Wang J, Cohen A, Friedman E. A subset of metastatic human colon cancers expresses elevated levels of transforming growth factor beta1. Cancer Epidemiol Biomarkers Prev 1998; 7(6):497-504.; PMID:9641494
   PubMed Web of Science ®Google Scholar
• Meulmeester E, Ten Dijke P. The dynamic roles of TGF-β in cancer. J Pathol 2011; 223(2):205-18; PMID:20957627; http://dx.doi.org/10.1002/path.2785
   PubMed Web of Science ®Google Scholar
• Padua D, Massague J. Roles of TGFbeta in metastasis. Cell Res 2009; 19(1):89-102; PMID:19050696; http://dx.doi.org/10.1038/cr.2008.316
   PubMed Web of Science ®Google Scholar
• Wakefield LM, Roberts AB. TGF-β signaling: positive and negative effects on tumorigenesis. Curr Opin Genet Dev 2002; 12(1):22-9; PMID:11790550; http://dx.doi.org/10.1016/S0959-437X(01)00259-3
   PubMed Web of Science ®Google Scholar
• Derynck R, Akhurst RJ, Balmain A. TGF-β signaling in tumor suppression and cancer progression. Nat Genet 2001; 29(2):117-29; PMID:11586292; http://dx.doi.org/10.1038/ng1001-117
   PubMed Web of Science ®Google Scholar
• Massague J. TGF-β signal transduction. Annu Rev Biochem 1998; 67:753-91; PMID:9759503; http://dx.doi.org/10.1146/annurev.biochem.67.1.753
   PubMed Web of Science ®Google Scholar
• Bierie B, Stover DG, Abel TW, Chytil A, Gorska AE, Aakre M, Forrester E, Yang L, Wagner KU, Moses HL. Transforming growth factor-β regulates mammary carcinoma cell survival and interaction with the adjacent microenvironment. Cancer Res 2008; 68(6):1809-19; PMID:18339861; http://dx.doi.org/10.1158/0008-5472.CAN-07-5597
   PubMed Web of Science ®Google Scholar
• Moses HL. Serra R. Regulation of differentiation by TGF-β. Curr Opin Genetics Dev 1996; 6(5):581-6; PMID:8939725; http://dx.doi.org/10.1016/S0959-437X(96)80087-6
   PubMed Web of Science ®Google Scholar
• Muraoka-Cook RS, Dumont N, Arteaga CL. Dual role of transforming growth factor β in mammary tumorigenesis and metastatic progression. Clin Cancer Res 2005; 11(2 Pt 2):937s-43s.; PMID:15701890
   PubMed Web of Science ®Google Scholar
• Ganapathy V, Ge R, Grazioli A, Xie W, Banach-Petrosky W, Kang Y, Lonning S, McPherson J, Yingling JM, Biswas S, et al. Targeting the Transforming Growth Factor-β pathway inhibits human basal-like breast cancer metastasis. Mol Cancer 2010; 9:122; PMID:20504320; http://dx.doi.org/10.1186/1476-4598-9-122
   PubMed Web of Science ®Google Scholar
• Tan AR, Alexe G, Reiss M. Transforming growth factor-β signaling: emerging stem cell target in metastatic breast cancer? Breast Cancer Res Treat 2009; 115(3):453-95.; PMID:18841463
   PubMed Web of Science ®Google Scholar
• Bruna A, Darken RS, Rojo F, Ocaña A, Peñuelas S, Arias A, Paris R, Tortosa A, Mora J, Baselga J, et al. High TGFbeta-Smad activity confers poor prognosis in glioma patients and promotes cell proliferation depending on the methylation of the PDGF-B gene. Cancer Cell 2007; 11(2):147-60; PMID:17292826; http://dx.doi.org/10.1016/j.ccr.2006.11.023
   PubMed Web of Science ®Google Scholar
• Kjellman C, Olofsson SP, Hansson O, Von Schantz T, Lindvall M, Nilsson I, Salford LG, Sjögren HO, Widegren B. Expression of TGF-β isoforms, TGF-β receptors, and SMAD molecules at different stages of human glioma. Int J Cancer 2000; 89(3):251-8; PMID:10861501; http://dx.doi.org/10.1002/1097-0215(20000520)89:3<251::AID-IJC7>3.0.CO;2-5
   PubMed Web of Science ®Google Scholar
• Duffy MM, Ritter T, Ceredig R, Griffin MD. Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther 2011; 2(4):34; PMID:21861858; http://dx.doi.org/10.1186/scrt75
   PubMed Web of Science ®Google Scholar
• Li MO, Sanjabi S, Flavell RA. Transforming growth factor-β controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 2006; 25(3):455-71; PMID:16973386; http://dx.doi.org/10.1016/j.immuni.2006.07.011
   PubMed Web of Science ®Google Scholar
• Massague J. TGF-β signaling in development and disease. FEBS Lett 2012; 586(14):1833; PMID:22651913; http://dx.doi.org/10.1016/j.febslet.2012.05.030
   PubMed Web of Science ®Google Scholar
• Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012; 13(10):616-30; PMID:22992590; http://dx.doi.org/10.1038/nrm3434
   PubMed Web of Science ®Google Scholar
• Zarzynska JM. Two faces of TGF-beta1 in breast cancer. Mediators Inflamm 2014; 2014:141747; PMID:24891760; http://dx.doi.org/10.1155/2014/141747
   PubMed Web of Science ®Google Scholar
• Panis C, Herrera AC, Victorino VJ, Aranome AM, Cecchini R. Screening of circulating TGF-β levels and its clinicopathological significance in human breast cancer. Anticancer Res 2013; 33(2):737-42; PMID:23393376
   PubMed Web of Science ®Google Scholar
• Buijs JT, Stayrook KR, Guise TA. The role of TGF-β in bone metastasis: novel therapeutic perspectives. Bonekey Rep 2012; 1:96; PMID:23951484; http://dx.doi.org/10.1038/bonekey.2012.96
   PubMedGoogle Scholar
• Ikushima H, Miyazono K. TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 2010; 10(6):415-24; PMID:20495575; http://dx.doi.org/10.1038/nrc2853
   PubMed Web of Science ®Google Scholar
• Maier A, Peille AL, Vuaroqueaux V, Lahn M. Anti-tumor activity of the TGF-β receptor kinase inhibitor galunisertib (LY2157299 monohydrate) in patient-derived tumor xenografts. Cell Oncol (Dordr) 2015; 38(2):131-44; PMID:25573078; http://dx.doi.org/10.1007/s13402-014-0210-8
   PubMed Web of Science ®Google Scholar
• Goodwin PJ, Ligibel JA, Stambolic V. Metformin in breast cancer: time for action. J Clin Oncol 2009; 27(20):3271-3; PMID:19487373; http://dx.doi.org/10.1200/JCO.2009.22.1630
   PubMed Web of Science ®Google Scholar
• Iliopoulos D, Hirsch HA, Struhl K. Metformin decreases the dose of chemotherapy for prolonging tumor remission in mouse xenografts involving multiple cancer cell types. Cancer Res 2011; 71(9):3196-201; PMID:21415163; http://dx.doi.org/10.1158/0008-5472.CAN-10-3471
   PubMed Web of Science ®Google Scholar
• Jiralerspong S, Palla SL, Giordano SH, Meric-Bernstam F, Liedtke C, Barnett CM, Hsu L, Hung MC, Hortobagyi GN, Gonzalez-Angulo AM. Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. J Clin Oncol 2009; 27(20):3297-302; PMID:19487376; http://dx.doi.org/10.1200/JCO.2009.19.6410
   PubMed Web of Science ®Google Scholar
• Hirsch HA, Iliopoulos D, Tsichlis PN, Struhl K. Metformin selectively targets cancer stem cells, and acts together with chemotherapy to block tumor growth and prolong remission. Cancer Res 2009; 69(19):7507-11; PMID:19752085; http://dx.doi.org/10.1158/0008-5472.CAN-09-2994
   PubMed Web of Science ®Google Scholar
• Wahdan-Alaswad R, Fan Z, Edgerton SM, Liu B, Deng XS, Arnadottir SS, Richer JK, Anderson SM, Thor AD. Glucose promotes breast cancer aggression and reduces metformin efficacy. Cell Cycle 2013; 12(24):3759-69; PMID:24107633; http://dx.doi.org/10.4161/cc.26641
   PubMed Web of Science ®Google Scholar
• Wahdan-Alaswad RS, Cochrane DR, Spoelstra NS, Howe EN, Edgerton SM, Anderson SM, Thor AD, Richer JK. Metformin-induced killing of triple-negative breast cancer cells is mediated by reduction in fatty acid synthase via miRNA-193b. Horm Cancer 2014; 5(6):374-89; PMID:25213330; http://dx.doi.org/10.1007/s12672-014-0188-8
   PubMed Web of Science ®Google Scholar
• Alimova IN, Liu B, Fan Z, Edgerton SM, Dillon T, Lind SE, Thor AD. Metformin inhibits breast cancer cell growth, colony formation and induces cell cycle arrest in vitro. Cell Cycle 2009; 8(6):909-15; PMID:19221498; http://dx.doi.org/10.4161/cc.8.6.7933
   PubMed Web of Science ®Google Scholar
• Liu B, Fan Z, Edgerton SM, Deng XS, Alimova IN, Lind SE, Thor AD. Metformin induces unique biological and molecular responses in triple negative breast cancer cells. Cell Cycle 2009; 8(13):2031-40; PMID:19440038; http://dx.doi.org/10.4161/cc.8.13.8814
   PubMed Web of Science ®Google Scholar
• Liu B, Fan Z, Edgerton SM, Yang X, Lind SE, Thor AD. Potent anti-proliferative effects of metformin on trastuzumab-resistant breast cancer cells via inhibition of erbB2/IGF-1 receptor interactions. Cell Cycle 2011; 10(17):2959-66; PMID:21862872; http://dx.doi.org/10.4161/cc.10.17.16359
   PubMed Web of Science ®Google Scholar
• Dalal BI, Keown PA, Greenberg AH. Immunocytochemical localization of secreted transforming growth factor-β 1 to the advancing edges of primary tumors and to lymph node metastases of human mammary carcinoma. Am J Pathol 1993; 143(2):381-9.; PMID:8393616
   PubMed Web of Science ®Google Scholar
• Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27(8):1160-7; PMID:19204204; http://dx.doi.org/10.1200/JCO.2008.18.1370
   PubMed Web of Science ®Google Scholar
• Harrell JC, Prat A, Parker JS, Fan C, He X, Carey L, Anders C, Ewend M, Perou CM. Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res Treat 2012; 132(2):523-35; PMID:21671017; http://dx.doi.org/10.1007/s10549-011-1619-7
   PubMed Web of Science ®Google Scholar
• Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe JP, Tong F, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10(6):515-27; PMID:17157791; http://dx.doi.org/10.1016/j.ccr.2006.10.008
   PubMed Web of Science ®Google Scholar
• Gupta GP, Perk J, Acharyya S, de Candia P, Mittal V, Todorova-Manova K, Gerald WL, Brogi E, Benezra R, Massagué J. ID genes mediate tumor reinitiation during breast cancer lung metastasis. Proc Natl Acad Sci U S A 2007; 104(49):19506-11
   PubMed Web of Science ®Google Scholar
• Kang Y, Chen CR, Massague J. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 2003; 11(4):915-26; http://dx.doi.org/10.1016/S1097-2765(03)00109-6
   PubMed Web of Science ®Google Scholar
• Scheel TK, Gottwein JM, Carlsen TH, Li YP, Jensen TB, Spengler U, Weis N, Bukh J. Efficient culture adaptation of hepatitis C virus recombinants with genotype-specific core-NS2 by using previously identified mutations. J Virol 2011; 85(6):2891-906; PMID:21177811; http://dx.doi.org/10.1128/JVI.01605-10
   PubMed Web of Science ®Google Scholar
• Gumireddy K, Li A, Kossenkov AV, Cai KQ, Liu Q, Yan J, Xu H, Showe L, Zhang L, Huang Q. ID1 promotes breast cancer metastasis by S100A9 regulation. Mol Cancer Res 2014; 12(9):1334-43; PMID:24948111; http://dx.doi.org/10.1158/1541-7786.MCR-14-0049
   PubMed Web of Science ®Google Scholar
• Stankic M, Pavlovic S, Chin Y, Brogi E, Padua D, Norton L, Massagué J, Benezra R. TGF-β-Id1 signaling opposes Twist1 and promotes metastatic colonization via a mesenchymal-to-epithelial transition. Cell Rep 2013; 5(5):1228-42; PMID:24332369; http://dx.doi.org/10.1016/j.celrep.2013.11.014
   PubMed Web of Science ®Google Scholar
• Farina AR, Coppa A, Tiberio A, Tacconelli A, Turco A, Colletta G, Gulino A, Mackay AR. Transforming growth factor-beta1 enhances the invasiveness of human MDA-MB-231 breast cancer cells by up-regulating urokinase activity. Int J Cancer 1998; 75(5):721-30; PMID:9495240; http://dx.doi.org/10.1002/(SICI)1097-0215(19980302)75:5<721::AID-IJC10>3.0.CO;2-9
   PubMed Web of Science ®Google Scholar
• Kalkhoven E, Kwakkenbos-Isbrücker L, Mummery CL, de Laat SW, van den Eijnden-van Raaij AJ, van der Saag PT, van der Burg B. The role of TGF-β production in growth inhibition of breast-tumor cells by progestins. Int J Cancer 1995; 61(1):80-6; PMID:7705937; http://dx.doi.org/10.1002/ijc.2910610114
   PubMed Web of Science ®Google Scholar
• Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res 2010; 70(2):440-6; PMID:20068163; http://dx.doi.org/10.1158/0008-5472.CAN-09-1947
   PubMed Web of Science ®Google Scholar
• Pang MF, Georgoudaki AM, Lambut L, Johansson J, Tabor V, Hagikura K, Jin Y, Jansson M, Alexander JS, Nelson CM, et al. TGF-beta1-induced EMT promotes targeted migration of breast cancer cells through the lymphatic system by the activation of CCR7/CCL21-mediated chemotaxis. Oncogene 2015; 35(6):748-60
   PubMed Web of Science ®Google Scholar
• Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J, Menendez JA. Metformin against TGFbeta-induced epithelial-to-mesenchymal transition (EMT): from cancer stem cells to aging-associated fibrosis. Cell Cycle 2010; 9(22):4461-8; PMID:21088486; http://dx.doi.org/10.4161/cc.9.22.14048
   PubMed Web of Science ®Google Scholar
• Qu C, Zhang W, Zheng G, Zhang Z, Yin J, He Z. Metformin reverses multidrug resistance and epithelial-mesenchymal transition (EMT) via activating AMP-activated protein kinase (AMPK) in human breast cancer cells. Mol Cell Biochem 2014; 386(1–2):63-71; http://dx.doi.org/10.1007/s11010-013-1839-8
   PubMed Web of Science ®Google Scholar
• Bierie B, Moses HL. Transforming growth factor β (TGF-β) and inflammation in cancer. Cytokine Growth Factor Rev 2010; 21(1):49-59; PMID:20018551; http://dx.doi.org/10.1016/j.cytogfr.2009.11.008
   PubMed Web of Science ®Google Scholar
• Pickup M, Novitskiy S, Moses HL. The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 2013; 13(11):788-99; PMID:24132110; http://dx.doi.org/10.1038/nrc3603
   PubMed Web of Science ®Google Scholar
• Harrell JC, Dye WW, Allred DC, Jedlicka P, Spoelstra NS, Sartorius CA, Horwitz KB. Estrogen receptor positive breast cancer metastasis: altered hormonal sensitivity and tumor aggressiveness in lymphatic vessels and lymph nodes. Cancer Res 2006; 66(18):9308-15; http://dx.doi.org/10.1158/0008-5472.CAN-06-1769
   PubMed Web of Science ®Google Scholar
• Harrell JC, Pfefferle AD, Zalles N, Prat A, Fan C, Khramtsov A, Olopade OI, Troester MA, Dudley AC, Perou CM. Endothelial-like properties of claudin-low breast cancer cells promote tumor vascular permeability and metastasis. Clin Exp Metastasis 2014; 31(1):33-45; PMID:23975155; http://dx.doi.org/10.1007/s10585-013-9607-4
   PubMed Web of Science ®Google Scholar