Is the future of personalized therapy in triple-negative breast cancer based on molecular subtype?

Oncotarget

Volumn 6, Issue 15, 2015, Pages 12890-12908

  Du, Fanny Le ^a,b   Eckhardt, Bedrich L ^a   Lim, Bora ^a   Litton, Jennifer K ^a,c   Moulder, Stacy ^a   Meric Bernstam, Funda ^a   Gonzalez Angulo, Ana M ^a   Ueno, Naoto T ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b CENTRE EUGÈNE MARQUIS   (France)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Epithelial mesenchymal transition; Gene expression profiling; Immunotherapy; Targeted therapy; Triple negative breast cancer

Indexed keywords

ABIRATERONE ACETATE; ANASTROZOLE; ANDROGEN RECEPTOR; BICALUTAMIDE; BUPARLISIB; CARBOPLATIN; CETUXIMAB; CISPLATIN; DINACICLIB; ENTINOSTAT; ENZALUTAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERLOTINIB; EVEROLIMUS; GEFITINIB; GROWTH FACTOR; MPDL 3280A; N (6,7 DIHYDRO 6 OXO 5H DIBENZ[B,D]AZEPIN 7 YL) 2,2 DIMETHYL N' (2,2,3,3,3 PENTAFLUOROPROPYL)PROPANEDIAMIDE; OLAPARIB; ONARTUZUMAB; PANITUMUMAB; PEMBROLIZUMAB; PICTILISIB; SONIDEGIB; TAMOXIFEN; TIVANTINIB; TRAMETINIB; UNINDEXED DRUG; VELIPARIB; VISMODEGIB;

ANTIANGIOGENIC ACTIVITY; ARTICLE; BASAL LIKE TRIPLE NEGATIVE BREAST CANCER; CANCER CLASSIFICATION; CANCER STEM CELL; CELL CYCLE CHECKPOINT; DNA REPAIR; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; GENE MUTATION; HUMAN; IMMUNOMODULATION; IMMUNOMODULATORY TRIPLE NEGATIVE BREAST CANCER; LUMINAL APOCRINE TRIPLE NEGATIVE BREAST CANCER; MOLECULAR GENETICS; MOLECULARLY TARGETED THERAPY; PERSONALIZED MEDICINE; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN EXPRESSION; SYSTEMATIC REVIEW; TRIPLE NEGATIVE BREAST CANCER; FEMALE; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; PATHOLOGY; PROCEDURES; TRIPLE NEGATIVE BREAST NEOPLASMS;

FEMALE; GENE EXPRESSION PROFILING; HUMANS; MOLECULAR TARGETED THERAPY; PRECISION MEDICINE; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84931094433     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3849     Document Type: Article

References (103)

1. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V. Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype:a population-based study from the California cancer Registry. Cancer. 2007 May 1; 109:1721-8.
2. 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 Sep 2; 12:R68.
3. Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Lønning PE, Børresen-Dale AL. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001 Sep 11; 98:10869-74.
4. Burstein MD, Tsimelzon A, Poage GM, Covington KR, Contreras A, Fuqua S, Savage M, Osborne CK, Hilsenbeck SG, Chang JC, Mills GB, Lau CC, Brown PH. Comprehensive Genomic Analysis Identifies Novel Subtypes and Targets of Triple-negative Breast Cancer. Clin Cancer Res. 2014 Sep 10.
5. 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 Jul; 121:2750-67.
6. Lehmann BD, Pietenpol JA. Identification and use of biomarkers in treatment strategies for triple-negative breast cancer subtypes. J Pathol. 2014 Jan 1; 232:142-50.
7. Mayer IA, Abramson VG, Lehmann BD, Pietenpol JA. New Strategies for Triple-Negative Breast Cancer-Deciphering the Heterogeneity. Clin Cancer Res. 2014 Feb 15; 20:782-90.
8. Masuda H, Baggerly KA, Wang Y, Zhang Y, Gonzalez-Angulo AM, Meric-Bernstam F, Valero V, Lehmann BD, Pietenpol JA, Hortobagyi GN, Symmans WF, Ueno NT. Differential Response to Neoadjuvant Chemotherapy Among 7 Triple-Negative Breast Cancer Molecular Subtypes. Clin Cancer Res. 2013 Oct 1; 19:5533-40.
9. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, Akslen LA, Ragaz J, Gown AM, Gilks CB, van de Rijn M, Perou CM. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res. 2004 Aug 15; 10:5367-74.
10. Prat A, Adamo B, Cheang MCU, Anders CK, Carey LA, Perou CM. Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist. 2013; 18:123-33.
11. Turner N, Tutt A, Ashworth A. Hallmarks of "BRCAness" in sporadic cancers. Nat Rev Cancer. 2004 Oct; 4:814-9.
12. Ossovskaya V, Wang Y, Budoff A, Xu Q, Lituev A, Potapova O, Vansant G, Monforte J, Daraselia N. Exploring molecular pathways of triple-negative breast cancer. Genes Cancer. 2011 Sep; 2:870-9.
13. Rouzier R, Perou CM, Symmans WF, Ibrahim N, Cristofanilli M, Anderson K, Hess KR, Stec J, Ayers M, Wagner P, Morandi P, Fan C, Rabiul I, Ross JS, Hortobagyi GN, Pusztai L. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res. 2005 Aug 15; 11:5678-85.
14. Silver DP, Richardson AL, Eklund AC, Wang ZC, Szallasi Z, Li Q, Juul N, Calogrias D, Buraimoh A, Fatima A, Gelman RS, Ryan PD, Tung NM, Nicolo AD, Ganesan S, Miron A, Colin C, Sgroi DC, Ellisen LW, Winer EP, Garber JE. Efficacy of Neoadjuvant Cisplatin in Triple-Negative Breast Cancer. J Clin Oncol. 2010 Mar 1; 28:1145-53.
15. Sikov WM, Berry DA, Perou CM, Singh B, Cirrincione C, Tolaney S, Kuzma CS. Impact of the addition of carboplatin (Cb) and/or bevacizumab (B) to neoadjuvant weekly paclitaxel (P) followed by dose-dense AC on pathologic complete response (pCR) rates in triple-negative breast cancer (TNBC):CALGB 40603 (Alliance). Cancer Res. 2014; in proceeding.
16. Von Minckwitz G, Schneeweiss A, Loibl S, Salat C, Denkert C, Rezai M, Blohmer JU, Jackisch C, Paepke S, Gerber B, Zahm DM, Kümmel S, Eidtmann H, Klare P, Huober J, Costa S, Tesch H, Hanusch C, Hilfrich J, Khandan F, Fasching PA, Sinn BV, Engels K, Mehta K, Nekljudova V, Untch M. Neoadjuvant carboplatin in patients with triple-negative and HER2-positive early breast cancer (GeparSixto; GBG 66): a randomised phase 2 trial. Lancet Oncol. 2014 Jun; 15:747-56.
17. Minckwitz GV, Hahnen E, Fasching PA, Hauke J, Schneeweiss A, Salat C, Rezai M, Blohmer JU, Zahm DM, Jackisch C, Gerber B, Klare P, Kummel S, Eidtmann H, Paepke S, Nekljudova V, Loibl S, Untch M, Schmutzler RK, Groups G, A-BS. Pathological complete response (pCR) rates after carboplatin-containing neoadjuvant chemotherapy in patients with germline BRCA (gBRCA) mutation and triple-negative breast cancer (TNBC): Results from GeparSixto. J Clin Oncol. 2014; 32:5s.
18. Isakoff SJ, He L, Mayer EL, Goss PE, Traina TA, Carey LA, Krag K, Liu MC, Rugo HS, Stearns V, Come SE, Ryan PD, Finkelstein DM, Hartman A-R, Garber JE, Timms K, Winer EP, Ellisen LW. Identification of biomarkers to predict response to single-agent platinum chemotherapy in metastatic triple-negative breast cancer (mTNBC): Correlative studies from TBCRC009. J Clin Oncol. 2014; 32:5s.
19. Tutt A, Ellis P, Kilburn L, Gilett C, Pinder S, Abraham J, Barrett S, Barrett-Lee P, Chan S, Cheang M, Dowsett M, Fox L, Gazinska P. TNT: A randomized phase III trial of carboplatin (C) compared with docetaxel (D) for patients with metastatic or recurrent locally advanced triple negative or BRCA1/2 breast cancer (CRUK/07/012). SABCS. 2014; abstract S3-01.
20. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, Giavara S, O'Connor MJ, Tutt AN, Zdzienicka MZ, Smith GCM, Ashworth A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly (ADP-ribose) polymerase inhibition. Cancer Res. 2006 Aug 15; 66:8109-15.
21. Fong PC, Boss DS, Yap TA, Tutt A, Wu P, Mergui-Roelvink M, Mortimer P, Swaisland H, Lau A, O'Connor MJ, Ashworth A, Carmichael J, Kaye SB, Schellens JHM, de Bono JS. Inhibition of poly (ADPribose) polymerase in tumors from BRCA mutation carriers. N Engl J Med. 2009 Jul 9; 361:123-34.
22. Tutt A, Robson M, Garber JE, Domchek SM, Audeh MW, Weitzel JN, Friedlander M, Arun B, Loman N, Schmutzler RK, Wardley A, Mitchell G, Earl H, Wickens M, Carmichael J. Oral poly (ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and advanced breast cancer: a proof-ofconcept trial. The Lancet. 2010 Jul; 376:235-44.
23. O'Shaughnessy J, Schwartzberg LS, Danso MA, Rugo HS, Miller K, Yardley DA, Carlson RW. A randomized phase III study of iniparib (BSI-201) in combination with gemcitabine/carboplatin (G/C) in metastatic triple-negative breast cancer (TNBC). J Clin Oncol. 2011; 29:abstr 1007.
24. Mateo J, Ong M, Tan DSP, Gonzalez MA, de Bono JS. Appraising iniparib, the PARP inhibitor that never was-what must we learn? Nat Rev Clin Oncol. 2013 Oct 15; 10:688-96.
25. Shen Y, Rehman FL, Feng Y, Boshuizen J, Bajrami I, Elliott R, Wang B, Lord CJ, Post LE, Ashworth A. BMN 673, a Novel and Highly Potent PARP1/2 Inhibitor for the Treatment of Human Cancers with DNA Repair Deficiency. Clinical Cancer Research. 2013 Jul 23; 19:5003-15.
26. Rugo HS, Olopade O, DeMichele A, Van't Veer L, Buxton M, Hylton N, Yee D. Veliparib/carboplatin plus standard neoadjuvatn therapy for high risk breast cancer:First efficacy results from the I-SPY 2 TRIAL. Cancer Res. 2014; in proceeding.
27. Xia Q, Cai Y, Peng R, Wu G, Shi Y, Jiang W. The CDK1 inhibitor RO3306 improves the response of BRCAproficient breast cancer cells to PARP inhibition. Int J Oncol. 2014 Mar; 44:735-44.
28. Ueno NT. Targeting EGFR in Triple Negative Breast Cancer. Journal of Cancer. 2011; 2:324-8.
29. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002 Jun; 2:442-54.
30. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe J-P, Tong F, Speed T, Spellman PT, DeVries S, Lapuk A, Wang NJ, Kuo W-L, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, McCormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell. 2006 Dec; 10:515-27.
31. Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, Rimm DL, Wong H, Rodriguez A, Herschkowitz JI, Fan C, Zhang X, He X, Pavlick A, Gutierrez MC, Renshaw L, Larionov AA, Faratian D, Hilsenbeck SG, Perou CM, Lewis MT, Rosen JM, Chang JC. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci USA. 2009 Aug 18; 106:13820-5.
32. Khramtsov AI, Khramtsova GF, Tretiakova M, Huo D, Olopade OI, Goss KH. Wnt/beta-catenin pathway activation is enriched in basal-like breast cancers and predicts poor outcome. Am J Pathol. 2010 Jun; 176:2911-20.
33. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, Weinberg RA, Lander ES. Identification of Selective Inhibitors of Cancer Stem Cells by High-Throughput Screening. Cell. 2009 Aug 21; 138:645-59.
34. Chang J, Landis M, Schott A, Pavlick A, Dobrolecki L, Korkaya H, Zhang X, Froehlich A, Rodriguez A, Rimawi M, Wicha M, Lewis M, Hayes D. Targeting Intrinsically-Resistant Breast Cancer Stem Cells with Gamma-Secretase Inhibitors. Cancer Research. 2010; Feb 10; 69:48-48.
35. Wang K, Zhang Q, Li D, Ching K, Zhang C, Zheng X, Ozeck M, Shi S, Li X, Wang H, Rejto P, Christensen J, Olson P. PEST Domain Mutations in Notch Receptors Comprise an Oncogenic Driver Segment in Triple-Negative Breast Cancer Sensitive to a γ-Secretase Inhibitor. Clin Cancer Res. 2015 Mar 15; 21:1487-96.
36. Mueller KL, Madden JM, Zoratti GL, Kuperwasser C, List K, Boerner JL. Fibroblast-secreted hepatocyte growth factor mediates epidermal growth factor receptor tyrosine kinase inhibitor resistance in triple-negative breast cancers through paracrine activation of Met. Breast Cancer Res. 2012 Jul 12; 14:R104.
37. Zhang Y-W, Staal B, Essenburg C, Su Y, Kang L, West R, Kaufman D, Dekoning T, Eagleson B, Buchanan SG, Vande Woude GF. MET kinase inhibitor SGX523 synergizes with epidermal growth factor receptor inhibitor erlotinib in a hepatocyte growth factor-dependent fashion to suppress carcinoma growth. Cancer Res. 2010 Sep 1; 70:6880-90.
38. Daniel B, Campone M, Dieras V, Ervin T, Yu W, Paton V, Xia Q, Peterson A. OT3-01-11: A Randomized, Phase II Multicenter, Double-Blind, Placebo-Controlled Trial Evaluating MetMAb and/or Bevacizumab in Combination with Weekly Paclitaxel in Patients with Metastatic Triple-Negative Breast Cancer. Cancer Research. 2011 Dec 15; 71:OT3-01-11-OT3-01-11.
39. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, Parker LM, Anderson KS, Harris LN, Garber JE, Richardson AL, Schnitt SJ, Nikolsky Y, Gelman RS, Polyak K. Molecular definition of breast tumor heterogeneity. Cancer Cell. 2007 Mar; 11:259-73.
40. Oettle H, Hilbig A, Seufferlein T, Luger T, Schmid RM, Von Wichert G, Schmaus S. Trabedersen (AP 12009) in the treatment of patients with advanced tumors: Completion of dose-escalation and first efficacy data. J Clin Oncol. 2010 28:abstr 2611.
41. Golicnik JP, Gazic B, Ovcaricek T, Matos E, Borstnar S. Prognostic value of routinely determined tumor infiltrating lymphocytes in triple-negative breast cancer. J Clin Oncol. 2014; 32:5s.
42. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, Chen H, Omeroglu G, Meterissian S, Omeroglu A, Hallett M, Park M. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med. 2008 May; 14:518-27.
43. Desmedt C, Haibe-Kains B, Wirapati P, Buyse M, Larsimont D, Bontempi G, Delorenzi M, Piccart M, Sotiriou C. Biological Processes Associated with Breast Cancer Clinical Outcome Depend on the Molecular Subtypes. Clin Cancer Res. 2008 Aug 15; 14:5158-65.
44. Bianchini G, Qi Y, Alvarez RH, Iwamoto T, Coutant C, Ibrahim NK, Valero V, Cristofanilli M, Green MC, Radvanyi L, Hatzis C, Hortobagyi GN, Andre F, Gianni L, Symmans WF, Pusztai L. Molecular Anatomy of Breast Cancer Stroma and Its Prognostic Value in Estrogen Receptor-Positive and-Negative Cancers. J Clin Oncol. 2010 Oct 1; 28:4316-23.
45. Denkert C, Loibl S, Noske A, Roller M, Müller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, Törne C von, Weichert W, Engels K, Solbach C, Schrader I, Dietel M, Minckwitz G von. Tumor-Associated Lymphocytes As an Independent Predictor of Response to Neoadjuvant Chemotherapy in Breast Cancer. J Clin Oncol. 2010 Jan 1; 28:105-13.
46. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD, Schem C, Fisch K, Darb-Esfahani S, Mehta K, Sotiriou C, Wienert S, Klare P, André F, Klauschen F, Blohmer J-U, Krappmann K, Schmidt M, Tesch H, Kümmel S, Sinn P, Jackisch C, Dietel M, Reimer T, Untch M, Loibl S. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without Carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol. 2015 Mar 20; 33:983-91.
47. Mittendorf EA, Philips AV, Meric-Bernstam F, Qiao N, Wu Y, Harrington S, Su X, Wang Y, Gonzalez-Angulo AM, Akcakanat A, Chawla A, Curran M, Hwu P, Sharma P, Litton JK, Molldrem JJ, Alatrash G. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res. 2014 Apr; 2:361-70.
48. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 2012 Jun 28; 366:2443-54.
49. Curigliano G, Viale G, Ghioni M, Jungbluth AA, Bagnardi V, Spagnoli GC, Neville AM, Nolè F, Rotmensz N, Goldhirsch A. Cancer-testis antigen expression in triple-negative breast cancer. Ann Oncol. 2011 Jan 1; 22:98-103.
50. Ju T, Cummings RD. A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase. Proc Natl Acad Sci USA. 2002 Dec 24; 99:16613-8.
51. Ademuyiwa FO, Bshara W, Attwood K, Morrison C, Edge SB, Karpf AR, James SA, Ambrosone CB, O'Connor TL, Levine EG, Miliotto A, Ritter E, Ritter G, Gnjatic S, Odunsi K. NY-ESO-1 cancer testis antigen demonstrates high immunogenicity in triple negative breast cancer. PLoS ONE. 2012; 7:e38783.
52. Tessari A, Paolini B, Mariani L, Pilla L, Carcangiu ML, Moliterni A, Braud FGD, Cresta S. Expression of PD-L1 and NY-ESO-1 in early and advanced triple-negative breast cancer. J Clin Oncol. 2014; 32:5s.
53. Ulloa-Montoya F, Louahed J, Dizier B, Gruselle O, Spiessens B, Lehmann FF, Suciu S, Kruit WHJ, Eggermont AMM, Vansteenkiste J, Brichard VG. Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J Clin Oncol. 2013 Jul 1; 31:2388-95.
54. Farmer P, Bonnefoi H, Becette V, Tubiana-Hulin M, Fumoleau P, Larsimont D, MacGrogan G, Bergh J, Cameron D, Goldstein D, Duss S, Nicoulaz A-L, Brisken C, Fiche M, Delorenzi M, Iggo R. Identification of molecular apocrine breast tumours by microarray analysis. Oncogene. 2005 May 9; 24:4660-71.
55. Gonzalez-Angulo AM, Stemke-Hale K, Palla SL, Carey M, Agarwal R, Meric-Berstam F, Traina TA, Hudis C, Hortobagyi GN, Gerald WL, Mills GB, Hennessy BT. Androgen receptor levels and association with PIK3CA mutations and prognosis in breast cancer. Clin Cancer Res. 2009 Apr 1; 15:2472-8.
56. Park S, Koo J, Park HS, Kim J-H, Choi S-Y, Lee JH, Park B-W, Lee KS. Expression of androgen receptors in primary breast cancer. Annals of Oncology. 2009 Nov 3; 21:488-92.
57. McNamara KM, Yoda T, Takagi K, Miki Y, Suzuki T, Sasano H. Androgen receptor in triple negative breast cancer. J Steroid Biochem Mol Biol. 2013 Jan; 133:66-76.
58. Gucalp A, Tolaney S, Isakoff SJ, Ingle JN, Liu MC, Carey LA, Blackwell K, Rugo H, Nabell L, Forero A, Stearns V, Doane AS, Danso M, Moynahan ME, Momen LF, Gonzalez JM, Akhtar A, Giri DD, Patil S, Feigin KN, Hudis CA, Traina TA. Phase II Trial of Bicalutamide in Patients with Androgen Receptor-Positive, Estrogen Receptor-Negative Metastatic Breast Cancer. Clin Cancer Res. 2013 Oct 1; 19:5505-12.
59. Cochrane DR, Bernales S, Jacobsen BM, Cittelly DM, Howe EN, D'Amato NC, Spoelstra NS, Edgerton SM, Jean A, Guerrero J, Gómez F, Medicherla S, Alfaro IE, McCullagh E, Jedlicka P, Torkko KC, Thor AD, Elias AD, Protter AA, Richer JK. Role of the androgen receptor in breast cancer and preclinical analysis of enzalutamide. Breast Cancer Res. 2014; 16:R7.
60. Traina TA, O'Shaughnessy J, Nanda R, Schwartzberg L, Abramson VG, Cortes J, Peterson A, Tudor IC, Blaney M, Steinberg J, Kelly CM, Trudeau M, Awada A, Winer EP, Hudis C, Schmid P, Yardley DA. Stage 1 results from MDV3100-11: A 2-stage study of enzalutamide (ENZA), an androgen receptor (AR) inhibitor, in advanced AR+ triple-negative breast cancer (TNBC). SABCS. 2014; abstract P5-19-09.
61. Overmoyer B, Sanz-Altamira P, Taylor RP, Hancock ML, Dalton JT, Johnston MA, Steiner MS. Enobosarm: A targeted therapy for metastatic, androgen receptor positive, breast cancer. J Clin Oncol. 2014; 32:5s.
62. Barton VN, D'Amato NC, Gordon MA, Lind HT, Spoelstra NS, Babbs BL, Heinz RE, Elias A, Jedlicka P, Jacobsen BM, Richer JK. Multiple Molecular Subtypes of Triple-Negative Breast Cancer Critically Rely on Androgen Receptor and Respond to Enzalutamide In Vivo. Mol Cancer Ther. 2015 Feb 23.
63. Tate CR, Rhodes LV, Segar HC, Driver JL, Pounder FN, Burow ME, Collins-Burow BM. Targeting triple-negative breast cancer cells with the histone deacetylase inhibitor panobinostat. Breast Cancer Res. 2012; 14:R79.
64. Sabnis GJ, Goloubeva O, Chumsri S, Nguyen N, Sukumar S, Brodie AMH. Functional activation of the estrogen receptor-α and aromatase by the HDAC inhibitor entinostat sensitizes ER-negative tumors to letrozole. Cancer Res. 2011 Mar 1; 71:1893-903.
65. Cancer Genome Atlas Network . Comprehensive molecular portraits of human breast tumours. Nature. 2012 Oct 4; 490:61-70.
66. Paik S, Kim C, Wolmark N. HER2 status and benefit from adjuvant trastuzumab in breast cancer. N Engl J Med. 2008 Mar 27; 358:1409-11.
67. Mittendorf EA, Schneble EJ, Perez SA, Symanowski JT, Patil R, Vreeland TJ, Berry JS, Trappey AF, Clifton GT, Hofe E von, Ardavanis A, Ponniah S, Shumway NM, Papamichail M, Peoples GE. Primary analysis of the prospective, randomized, single-blinded phase II trial of AE37 vaccine versus GM-CSF alone administered in the adjuvant setting to high-risk breast cancer patients. J Clin Oncol. 2014; 32:5s.
68. Schneble EJ, Perez SA, Berry JS, Trappey AF, Vreeland T, Hale DF, Sears AK, Clifton GT, Hofe E von, Ardavanis A, Shumway NM, Ponniah S, Papamichail M, Peoples GE, Mittendorf EA. Comparison of recurrent and nonrecurrent breast cancer patients undergoing AE37 peptide vaccine therapy. J Clin Oncol. 2014; 32:5s.
69. Masuda H, Zhang D, Bartholomeusz C, Doihara H, Hortobagyi GN, Ueno NT. Role of epidermal growth factor receptor in breast cancer. Breast Cancer Res Treat. 2012 Nov; 136:331-45.
70. Baselga J, Gómez P, Greil R, Braga S, Climent MA, Wardley AM, Kaufman B, Stemmer SM, Pêgo A, Chan A, Goeminne J-C, Graas M-P, Kennedy MJ, Gil EMC, Schneeweiss A, Zubel A, Groos J, Melezínková H, Awada A. Randomized Phase II Study of the Anti-Epidermal Growth Factor Receptor Monoclonal Antibody Cetuximab With Cisplatin Versus Cisplatin Alone in Patients With Metastatic Triple-Negative Breast Cancer. J Clin Oncol. 2013 Jul 10; 31:2586-92.
71. Nabholtz J, Weber B, Mouret-Reynier M, Gligorov J, Coudert BP, Vanlemmens L, Petit T. Panitumumab in combination with FEC 100 (5-fluorouracil, epidoxorubicin, cyclophosphamide) followed by docetaxel (T) in patients with operable, triple-negative breast cancer (TNBC):Preliminary results of a multicenter neoadjuvant pilot phase II study. J Clin Oncol. 2011; 29:abstr 11574.
72. Carey LA, Rugo HS, Marcom PK, Mayer EL, Esteva FJ, Ma CX, Liu MC, Storniolo AM, Rimawi MF, Forero-Torres A, Wolff AC, Hobday TJ, Ivanova A, Chiu W-K, Ferraro M, Burrows E, Bernard PS, Hoadley KA, Perou CM, Winer EP. TBCRC 001: randomized phase II study of cetuximab in combination with carboplatin in stage IV triple-negative breast cancer. J Clin Oncol. 2012 Jul 20; 30:2615-23.
73. Sharpe R, Pearson A, Herrera-Abreu MT, Johnson D, Mackay A, Welti JC, Natrajan R, Reynolds AR, Reis-Filho JS, Ashworth A, Turner NC. FGFR signaling promotes the growth of triple-negative and basal-like breast cancer cell lines both in vitro and in vivo. Clin Cancer Res. 2011 Aug 15; 17:5275-86.
74. Bane AL, Pinnaduwage D, Colby S, Bull SB, O'Malley FP, Andrulis IL. Expression profiling of familial breast cancers demonstrates higher expression of FGFR2 in BRCA2-associated tumors. Breast Cancer Res Treat. 2009 Sep 1; 117:183-91.
75. André F, Bachelot T, Campone M, Dalenc F, Perez-Garcia JM, Hurvitz SA, Turner N, Rugo H, Smith JW, Deudon S, Shi M, Zhang Y, Kay A, Porta DG, Yovine A, Baselga J. Targeting FGFR with Dovitinib (TKI258):Preclinical and Clinical Data in Breast Cancer. Clin Cancer Res. 2013 Jul 1; 19:3693-702.
76. Guagnano V, Kauffmann A, Wöhrle S, Stamm C, Ito M, Barys L, Pornon A. FGFR Genetic Alterations Predict for Sensitivity to NVP-BGJ398, a Selective Pan-FGFR Inhibitor. Cancer Discov. 2012; 2:1118-33.
77. Werner H, Bruchim I. IGF-1 and BRCA1 signalling pathways in familial cancer. The Lancet Oncology. 2012 Dec; 13:e537-e544.
78. Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer. 2012 Mar; 12:159-69.
79. Sangai T, Akcakanat A, Chen H, Tarco E, Wu Y, Do K-A, Miller TW, Arteaga CL, Mills GB, Gonzalez-Angulo AM, Meric-Bernstam F. Biomarkers of response to Akt inhibitor MK-2206 in breast cancer. Clin Cancer Res. 2012 Oct 15; 18:5816-28.
80. Bendell JC, Rodon J, Burris HA, de Jonge M, Verweij J, Birle D, Demanse D, De Buck SS, Ru QC, Peters M, Goldbrunner M, Baselga J. Phase, I, dose-escalation study of BKM120, an oral pan-Class I PI3K inhibitor, in patients with advanced solid tumors. J Clin Oncol. 2012 Jan 20; 30:282-90.
81. Juric D, Infante J, Krop I, Kurkjian C, Patel M, Graham R, Wilson T. Evaluation of Tolerability and Anti-Tumor Activity of GDC-0032, a PI3K Inhibitor with Enhanced Activity Against PIK3CA Mutant Tumors, Administered to Patients with Advanced Solid Tumors. Eur J Cancer. 2013; 49:S168-168.
82. Burris H, Rodon J, Sharma S, Herbst RS, Tabernero J, Infante JR, Silva A. First-in-human phase I study of the oral PI3K inhibitor BEZ235 in patients (pts) with advanced solid tumors. J Clin Oncol. 2010; 28:abstr 3005.
83. Hoeflich KP, O'Brien C, Boyd Z, Cavet G, Guerrero S, Jung K, Januario T, Savage H, Punnoose E, Truong T, Zhou W, Berry L, Murray L, Amler L, Belvin M, Friedman LS, Lackner MR. In vivo Antitumor Activity of MEK and Phosphatidylinositol 3-Kinase Inhibitors in Basal-Like Breast Cancer Models. Clin Cancer Res. 2009 Jul 15; 15:4649-64.
84. Bayliss J, Hilger A, Vishnu P, Diehl K, El-Ashry D. Reversal of the estrogen receptor negative phenotype in breast cancer and restoration of antiestrogen response. Clin Cancer Res. 2007 Dec 1; 13:7029-36.
85. Cameron D, Brown J, Dent R, Jackisch C, Mackey J, Pivot X, Steger GG, Suter TM, Toi M, Parmar M, Laeufle R, Im Y-H, Romieu G, Harvey V, Lipatov O, Pienkowski T, Cottu P, Chan A, Im S-A, Hall PS, Bubuteishvili-Pacaud L, Henschel V, Deurloo RJ, Pallaud C, Bell R. Adjuvant bevacizumab-containing therapy in triple-negative breast cancer (BEATRICE): primary results of a randomised, phase 3 trial. The Lancet Oncology. 2013 Sep; 14:933-42.
86. O'Shaughnessy J, Romieu G, Diéras V, Byrtek M, Duenne AA, Miles D. Meta-Analysis of Patients with Triple-Negative Breast Cancer (TNBC) from Three Randomized Trials of First-Line Bevacizumab (BV) and Chemotherapy Treatment for Metastatic Breast Cancer (MBC). Cancer Res. 2010; 70:abstr P6-12-03.
87. Hu Z, Fan C, Livasy C, He X, Oh DS, Ewend MG, Carey LA, Subramanian S, West R, Ikpatt F, Olopade OI, van de Rijn M, Perou CM. A compact VEGF signature associated with distant metastases and poor outcomes. BMC Med. 2009; 7:9.
88. Bender RJ, Mac Gabhann F. Expression of VEGF and Semaphorin Genes Define Subgroups of Triple Negative Breast Cancer. PLoS, ONE. 2013 May 8; 8:e61788.
89. Glénisson M, Vacher S, Callens C, Susini A, Cizeron-Clairac G, Le Scodan R, Meseure D, Lerebours F, Spyratos F, Lidereau R, Bièche I. Identification of new candidate therapeutic target genes in triple-negative breast cancer. Genes Cancer. 2012 Jan; 3:63-70.
90. Shangary S, Wang S. Small-Molecule Inhibitors of the MDM2-p53 Protein-Protein Interaction to Reactivate p53 Function: A Novel Approach for Cancer Therapy. Annu Rev Pharmacol Toxicol. 2009; 49:223-41.
91. Perez R, Schally AV, Popovics P, Cai R, Sha W, Rincon R, Rick FG. Antagonistic analogs of growth hormone-releasing hormone increase the efficacy of treatment of triple negative breast cancer in nude mice with doxorubicin; A preclinical study. Oncoscience. 2014; 1:665-73.
92. Zardavas D, Baselga J, Piccart M. Emerging targeted agents in metastatic breast cancer. Nat Rev Clin Oncol. 2013 Apr; 10:191-210.
93. Ibrahim YH, García-García C, Serra V, He L, Torres-Lockhart K, Prat A, Anton P, Cozar P, Guzmán M, Grueso J, Rodríguez O, Calvo MT, Aura C, Díez O, Rubio IT, Pérez J, Rodón J, Cortés J, Ellisen LW, Scaltriti M, Baselga J. PI3K inhibition impairs BRCA1/2 expression and sensitizes BRCA-proficient triple-negative breast cancer to PARP inhibition. Cancer Discov. 2012 Nov; 2:1036-47.
94. Gonzalez-Angulo AM, Ferrer-Lozano J, Stemke-Hale K, Sahin A, Liu S, Barrera JA, Burgues O, Lluch AM, Chen H, Hortobagyi GN, Mills GB, Meric-Bernstam F. PI3K Pathway Mutations and PTEN Levels in Primary and Metastatic Breast Cancer. Molecular Cancer Therapeutics. 2011 Apr 13; 10:1093-101.
95. Le Du F, Ueno NT, Gonzalez-Angulo AM. Breast Cancer Biomarkers: Utility in Clinical Practice. Current Breast Cancer Reports. 2013; 1-9.
96. Ocaña A, Montero JC, Pandiella A. Achilles' heel of triple negative cancer. Oncoscience. 2014; 1:763-4.
97. Hatzis C, Pusztai L, Valero V, Booser DJ, Esserman L, Lluch A, Vidaurre T, Holmes F, Souchon E, Wang H, Martin M, Cotrina J, Gomez H, Hubbard R, Chacón JI, Ferrer-Lozano J, Dyer R, Buxton M, Gong Y, Wu Y, Ibrahim N, Andreopoulou E, Ueno NT, Hunt K, Yang W, Nazario A, DeMichele A, O'Shaughnessy J, Hortobagyi GN, Symmans WF. A genomic predictor of response and survival following taxane-anthracycline chemotherapy for invasive breast cancer. JAMA. 2011 May 11; 305:1873-81.
98. Peintinger F, Kuerer HM, Anderson K, Boughey JC, Meric-Bernstam F, Singletary SE, Hunt KK, Whitman GJ, Stephens T, Buzdar AU, Green MC, Symmans WF. Accuracy of the combination of mammography and sonography in predicting tumor response in breast cancer patients after neoadjuvant chemotherapy. Ann Surg Oncol. 2006 Nov; 13:1443-9.
99. Dent RA, Lindeman GJ, Clemons M, Wildiers H, Chan A, McCarthy NJ, Singer CF, Lowe ES, Watkins CL, Carmichael J. Phase I trial of the oral PARP inhibitor olaparib in combination with paclitaxel for first- or secondline treatment of patients with metastatic triple-negative breast cancer. Breast Cancer Res. 2013; 15:R88.
100. Tolaney SM, Guo H, Barry WT, Larrabee K, Brock JE, Wagle N, Allen EMV, Paweletz C, Ivanova E, Janne PA, Overmoyer B, Wright JJ, Shapiro G, Winer EP, Krop IE. A phase II study of tivantinib (ARQ-197) for metastatic triple-negative breast cancer. J Clin Oncol. 2014; 32:5s.
101. Nanda R, Chow LQM, Dees C, Berger R, Gupta S, Geva R, Pusztai L, Dolled-Filhart M, Emancipator K, Gonzalez E, Houp J, Pathiraja K, Karantza V. A phase IB of pembrolizumab (MK-3475) in patients with advanced triple-negative breast cancer. SABCS. 2014; abstract S1-09.
102. Emens L, Braiteh F, Cassier P, DeLord J-P, Eder JP, Shen X, Xiao X, Wang Y, Hegde PS, Chen DS, Krop I. Inhibition of PD-L1 by MPDL3280A leads to clinical activity in patients with metastatic triple-negative breast cancer. SABCS. 2014; abstract PD1-6.
103. Curigliano G, Pivot X, Cortés J, Elias A, Cesari R, Khosravan R, Collier M, Huang X, Cataruozolo PE, Kern KA, Goldhirsch A. Randomized phase II study of sunitinib versus standard of care for patients with previously treated advanced triple-negative breast cancer. Breast. 2013 Oct; 22:650-6.