Breast cancer molecular subtypes: From TNBC to QNBC

American Journal of Cancer Research

Volumn 6, Issue 9, 2016, Pages 1864-1872

  Hon, Jane Date C ^a   Singh, Baljit ^b   Sahin, Aysegul ^c   Du, Gang ^b,d   Wang, Jinhua ^b,d   Wang, Vincent Y ^e   Deng, Fang Ming ^b,e   Zhang, David Y ^e   Monaco, Marie E ^b,d,f   Lee, Peng ^b,d,e,f  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^e Association of Chinese American Physicians   (United States)

^f DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

ACSL4; Breast cancer; QNBC; Quadruple negative; TNBC

Indexed keywords

EID: 84992187940     PISSN: None     EISSN: 21566976     Source Type: Journal    
DOI: None     Document Type: Review

References (61)

1. Siegel RL, Miller KD and Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015; 65: 5-29.
2. Kumar P and Aggarwal R. An overview of triple-negative breast cancer. Arch Gynecol Obstet 2016; 293: 247-69.
3. Polyak K. Heterogeneity in breast cancer. J Clin Invest 2011; 121: 3786-3788.
4. Barnard ME, Boeke CE and Tamimi RM. Established breast cancer risk factors and risk of intrinsic tumor subtypes. Biochim Biophys Acta 2015; 1856: 73-85.
5. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ; Panel members. Strategies for subtypes-dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol 2011; 22: 1736-1747.
6. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lonning PE, Brown PO, Borresen-Dale AL and Botstein D. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 2003; 100: 8418-8423.
7. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamen-schikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO and Botstein D. Molecular portraits of human breast tumours. Nature 2000; 406: 747-752.
8. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, Davies S, Fauron C, He X, Hu Z, Quackenbush JF, Stijleman IJ, Palazzo J, Marron JS, Nobel AB, Mardis E, Nielsen TO, Ellis MJ, Perou CM and Bernard PS. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009; 27: 1160-1167.
9. Murria R, Palanca S, de Juan I, Alenda C, Egoavil C, Segui FJ, Garcia-Casado Z, Juan MJ, Sanchez AB, Segura A, Santaballa A, Chirivella I, Llop M, Perez G, Barragan E, Salas D and Bolufer P. Immunohistochemical, genetic and epigenetic profiles of hereditary and triple negative breast cancers. Relevance in personalized medicine. Am J Cancer Res 2015; 5: 2330-2343.
10. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, Livasy C, Carey LA, Reynolds E, Dressler L, Nobel A, Parker J, Ewend MG, Sawyer LR, Wu J, Liu Y, Nanda R, Tretiakova M, Ruiz Orrico A, Dreher D, Palazzo JP, Perreard L, Nelson E, Mone M, Hansen H, Mullins M, Quackenbush JF, Ellis MJ, Olopade OI, Bernard PS and Perou CM. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006; 7: 96.
11. Choi YL, Oh E, Park S, Kim Y, Park YH, Song K, Cho EY, Hong YC, Choi JS, Lee JE, Kim JH, Nam SJ, Im YH, Yang JH and Shin YK. Triple-negative, basal-like, and quintuple-negative breast can cers: better prediction model for survival. BMC Cancer 2010; 10: 507.
12. Masuda H, Baggerly KA, Wang Y, Zhang Y, Gonzalez-Angulo AM, Meric-Bernstam F, Valero V, Lehmann BD, Pietenpol JA, Hortobagyi GN, Symmans WF and Ueno NT. Differential response to neoadjuvant chemotherapy among 7 triple-negative breast cancer molecular subtypes. Clin Cancer Res 2013; 19: 5533-5540.
13. Safarpour D and Tavassoli FA. A targetable androgen receptor-positive breast cancer subtype hidden among the triple-negative cancers. Arch Pathol Lab Med 2015; 139: 612-617.
14. Tsutsumi Y. Apocrine carcinoma as triple-negative breast cancer: novel definition of apocrine-type carcinoma as estrogen/progesterone receptor-negative and androgen receptor-positive invasive ductal carcinoma. Jpn J Clin Oncol 2012; 42: 375-386.
15. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y and Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011; 121: 2750-2767.
16. Prat A, Pineda E, Adamo B, Galvan P, Fernandez A, Gaba L, Diez M, Viladot M, Arance A and Munoz M. Clinical implications of the intrinsic molecular subtypes of breast cancer. Breast 2015; 24 Suppl 2: S26-35.
17. 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 and Perou CM. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res 2004; 10: 5367-5374.
18. Rakha EA, Elsheikh SE, Aleskandarany MA, Habashi HO, Green AR, Powe DG, El-Sayed ME, Benhasouna A, Brunet JS, Akslen LA, Evans AJ, Blamey R, Reis-Filho JS, Foulkes WD and Ellis IO. Triple-negative breast cancer: distinguishing between basal and nonbasal subtypes. Clin Cancer Res 2009; 15: 2302-2310.
19. Wahba HA and El-Hadaad HA. Current approaches in treatment of triple-negative breast cancer. Cancer Biol Med 2015; 12: 106-116.
20. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X and Perou CM. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010; 12: R68.
21. Ma CX, Luo J and Ellis MJ. Molecular profiling of triple negative breast cancer. Breast Dis 2010; 32: 73-84.
22. Burstein MD, Tsimelzon A, Poage GM, Covington KR, Contreras A, Fuqua SA, Savage MI, Osborne CK, Hilsenbeck SG, Chang JC, Mills GB, Lau CC and Brown PH. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res 2015; 21: 1688-1698.
23. Ono M, Tsuda H, Shimizu C, Yamamoto S, Shibata T, Yamamoto H, Hirata T, Yonemori K, Ando M, Tamura K, Katsumata N, Kinoshita T, Takiguchi Y, Tanzawa H and Fujiwara Y. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat 2012; 132: 793-805.
24. Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F, Perez EA, Thompson EA, Symmans WF, Richardson AL, Brock J, Criscitiello C, Bailey H, Ignatiadis M, Floris G, Sparano J, Kos Z, Nielsen T, Rimm DL, Allison KH, Reis-Filho JS, Loibl S, Sotiriou C, Viale G, Badve S, Adams S, Willard-Gallo K, Loi S; International TILs Working Group 2014. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol 2015; 26: 259-271.
25. Pruneri G, Vingiani A, Bagnardi V, Rotmensz N, De Rose A, Palazzo A, Colleoni AM, Goldhirsch A and Viale G. Clinical validity of tumor-infiltrating lymphocytes analysis in patients with triple-negative breast cancer. Ann Oncol 2016; 27: 249-256.
26. Ohtani H, Mori-Shiraishi K, Nakajima M and Ueki H. Defining lymphocyte-predominant breast cancer by the proportion of lymphocyte-rich stroma and its significance in routine histopathological diagnosis. Pathol Int 2015; 65: 644-651.
27. Jia LY, Shanmugam MK, Sethi G and Bishayee A. Potential role of targeted therapies in the treatment of triple-negative breast cancer. Anticancer Drugs 2016; 27: 147-155.
28. Safarpour D, Pakneshan S and Tavassoli FA. Androgen receptor (AR) expression in 400 breast carcinomas: is routine AR assessment justified? Am J Cancer Res 2014; 4: 353-368.
29. Giannos A, Filipits M, Zagouri F, Brandstetter A, Tsigginou A, Sotiropoulou M, Papaspyrou I, Sergentanis TN, Psaltopoulou T, Rodolakis A, Antsaklis A, Dimopoulos MA and Dimitrakakis C. Expression of ARs in triple negative breast cancer tumors: a potential prognostic factor? Onco Targets Ther 2015; 8: 1843-1847.
30. Proverbs-Singh T, Feldman JL, Morris MJ, Autio KA and Traina TA. Targeting the androgen receptor in prostate and breast cancer: several new agents in development. Endocr Relat Cancer 2015; 22: R87-R106.
31. Chia K, O'Brien M, Brown M and Lim E. Targeting the androgen receptor in breast cancer. Curr Oncol Rep 2015; 17: 4.
32. Barton VN, D'Amato NC, Gordon MA, Chris-tenson JL, Elias A and Richer JK. Androgen Receptor Biology in Triple Negative Breast Cancer: a Case for Classification as AR+ or Quadruple Negative Disease. Horm Cancer 2015; 6: 206-213.
33. Choi JE, Kang SH, Lee SJ and Bae YK. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann Surg Oncol 2015; 22: 82-89.
34. McGhan LJ, McCullough AE, Protheroe CA, Dueck AC, Lee JJ, Nunez-Nateras R, Castle EP, Gray RJ, Wasif N, Goetz MP, Hawse JR, Henry TJ, Barrett MT, Cunliffe HE and Pockaj BA. Androgen receptor-positive triple negative breast cancer: a unique breast cancer subtype. Ann Surg Oncol 2014; 21: 361-367.
35. Mrklic I, Pogorelic Z, Capkun V and Tomic S. Expression of androgen receptors in triple negative breast carcinomas. Acta Histochem 2013; 115: 344-348.
36. Pistelli M, Caramanti M, Biscotti T, Santinelli A, Pagliacci A, De Lisa M, Ballatore Z, Ridolfi F, Maccaroni E, Bracci R, Berardi R, Battelli N and Cascinu S. Androgen receptor expression in early triple-negative breast cancer: clinical significance and prognostic associations. Cancers (Basel) 2014; 6: 1351-1362.
37. 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; Translational Breast Cancer Resear-ch Consortium (TBCRC 011). Phase II trial of bicalutamide in patients with androgen receptor-positive, estrogen receptor-negative metastatic Breast Cancer. Clin Cancer Res 2013; 19: 5505-5512.
38. Barton VN, D'Amato NC, Gordon MA, Lind HT, Spoelstra NS, Babbs BL, Heinz RE, Elias A, Jedlicka P, Jacobsen BM and 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; 14: 769-778.
39. McNamara KM, Yoda T, Miki Y, Chanplakorn N, Wongwaisayawan S, Incharoen P, Kongdan Y, Wang L, Takagi K, Mayu T, Nakamura Y, Suzuki T, Nemoto N, Miyashita M, Tamaki K, Ishida T, Ohuchi N and Sasano H. Androgenic pathway in triple negative invasive ductal tumors: its correlation with tumor cell proliferation. Cancer Sci 2013; 104: 639-646.
40. He J, Peng R, Yuan Z, Wang S, Peng J, Lin G, Jiang X and Qin T. Prognostic value of androgen receptor expression in operable triple-negative breast cancer: a retrospective analysis based on a tissue microarray. Med Oncol 2012; 29: 406-410.
41. Kim Y, Jae E and Yoon M. Influence of Androgen Receptor Expression on the Survival Outcomes in Breast Cancer: A Meta-Analysis. J Breast Cancer 2015; 18: 134-142.
42. Zhang H, Zhan Y, Liu X, Qi Y, Zhang G, Sartor O and Dong Y. Splicing variants of androgen receptor in prostate cancer. Am J Clin Exp Urol 2013; 1: 18-24.
43. Hu R, Isaacs WB and Luo J. A snapshot of the expression signature of androgen receptor splicing variants and their distinctive transcriptional activities. Prostate 2011; 71: 1656-1667.
44. Hickey TE, Irvine CM, Dvinge H, Tarulli GA, Hanson AR, Ryan NK, Pickering MA, Birrell SN, Hu DG, Mackenzie PI, Russell R, Caldas C, Raj GV, Dehm SM, Plymate SR, Bradley RK, Tilley WD and Selth LA. Expression of androgen receptor splice variants in clinical breast cancers. Oncotarget 2015; 6: 44728-44.
45. Wu X, Li Y, Wang J, Wen X, Marcus MT, Daniels G, Zhang DY, Ye F, Wang LH, Du X, Adams S, Singh B, Zavadil J, Lee P and Monaco ME. Long chain fatty Acyl-CoA synthetase 4 is a biomarker for and mediator of hormone resistance in human breast cancer. PLoS One 2013; 8: e77060.
46. Sung YK, Park MK, Hong SH, Hwang SY, Kwack MH, Kim JC and Kim MK. Regulation of cell growth by fatty acid-CoA ligase 4 in human hepatocellular carcinoma cells. Exp Mol Med 2007; 39: 477-482.
47. Cao Y, Dave KB, Doan TP and Prescott SM. Fatty acid CoA ligase 4 is up-regulated in colon adenocarcinoma. Cancer Res 2001; 61: 8429-8434.
48. Maloberti PM, Duarte AB, Orlando UD, Pasqualini ME, Solano AR, Lopez-Otin C and Podesta EJ. Functional interaction between acyl-CoA synthetase 4, lipooxygenases and cyclooxygenase-2 in the aggressive phenotype of breast cancer cells. PLoS One 2010; 5: e15540.
49. Monaco ME, Creighton CJ, Lee P, Zou X, Topham MK and Stafforini DM. Expression of Long-chain Fatty Acyl-CoA Synthetase 4 in Breast and Prostate Cancers Is Associated with Sex Steroid Hormone Receptor Negativity. Transl Oncol 2010; 3: 91-98.
50. Orlando UD, Garona J, Ripoll GV, Maloberti PM, Solano AR, Avagnina A, Gomez DE, Alonso DF and Podesta EJ. The functional interaction between Acyl-CoA synthetase 4, 5-lipooxygenase and cyclooxygenase-2 controls tumor growth: a novel therapeutic target. PLoS One 2012; 7: e40794.
51. Orlando UD, Castillo AF, Dattilo MA, Solano AR, Maloberti PM and Podesta EJ. Acyl-CoA synthetase-4, a new regulator of mTOR and a potential therapeutic target for enhanced estrogen receptor function in receptor-positive and-negative breast cancer. Oncotarget 2015; 6: 42632-50.
52. Laplante M and Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149: 274-293.
53. Alayev A, Salamon RS, Berger SM, Schwartz NS, Cuesta R, Snyder RB and Holz MK. mTORC1 directly phosphorylates and activates ERalpha upon estrogen stimulation. Oncogene 2015; [Epub ahead of print].
54. Sun YJ, Wang XK and Li BJ. S-phase kinase-associated protein 2 expression interference inhibits breast cancer cell proliferation. Genet Mol Res 2015; 14: 9244-9252.
55. Signoretti S, Di Marcotullio L, Richardson A, Ramaswamy S, Isaac B, Rue M, Monti F, Loda M and Pagano M. Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J Clin Invest 2002; 110: 633-641.
56. Yang C, Nan H, Ma J, Jiang L, Guo Q, Han L, Zhang Y, Nan K and Guo H. High Skp2/Low p57(Kip2) Expression is Associated with Poor Prognosis in Human Breast Carcinoma. Breast Cancer (Auckl) 2015; 9: 13-21.
57. Wu L, Grigoryan AV, Li Y, Hao B, Pagano M and Cardozo TJ. Specific small molecule inhibitors of Skp2-mediated p27 degradation. Chem Biol 2012; 19: 1515-1524.
58. Shi P, Zhang Y, Tong X, Yang Y and Shao Z. Dihydrotestosterone induces p27 degradation via direct binding with SKP2 in ovarian and breast cancer. Int J Mol Med 2011; 28: 109-114.
59. Freres P, Wenric S, Boukerroucha M, Fasquelle C, Thiry J, Bovy N, Struman I, Geurts P, Collignon J, Schroeder H, Kridelka F, Lifrange E, Jossa V, Bours V, Josse C and Jerusalem G. Circulating microRNA-based screening tool for breast cancer. Oncotarget 2016; 7: 5416-28.
60. Mathe A, Scott RJ and Avery-Kiejda KA. MiRNAs and Other Epigenetic Changes as Biomarkers in Triple Negative Breast Cancer. Int J Mol Sci 2015; 16: 28347-28376.
61. Ouyang M, Li Y, Ye S, Ma J, Lu L, Lv W, Chang G, Li X, Li Q, Wang S and Wang W. MicroRNA profiling implies new markers of chemoresistance of triple-negative breast cancer. PLoS One 2014; 9: e96228.