Tumor infiltrating lymphocytes affect the outcome of patients with operable triple-negative breast cancer in combination with mutated amino acid classes

PLoS ONE

Volumn 11, Issue 9, 2016, Pages

  Kotoula, Vassiliki ^a   Lakis, Sotiris ^a   Vlachos, Ioannis S ^b,c   Giannoulatou, Eleni ^d,e   Zagouri, Flora ^f   Alexopoulou, Zoi ^g   Gogas, Helen ^f   Pectasides, Dimitrios ^h   Aravantinos, Gerasimos ⁱ   Efstratiou, Ioannis ^j   Pentheroudakis, George ^k   Papadopoulou, Kyriaki ^a   Chatzopoulos, Kyriakos ^a   Papakostas, Pavlos ^h   Sotiropoulou, Maria ^l   Nicolaou, Irene ^m   Razis, Evangelia ⁿ   Psyrri, Amanda ^o   Kosmidis, Paris ⁿ   Papadimitriou, Christos ^f   Fountzilas, George ^a   more..

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b INSTITUTE OF NANOSCIENCE AND NANOTECHNOLOGY   (Greece)

^c UNIVERSITY OF THESSALY   (Greece)

^d VICTOR CHANG CARDIAC RESEARCH INSTITUTE   (Australia)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f UNIVERSITY OF ATHENS   (Greece)

^g Health Data Specialists Ltd   (Greece)

^h HIPPOKRATION HOSPITAL   (Greece)

ⁱ AGII ANARGIRI CANCER HOSPITAL   (Greece)

^j PAPAGEORGIOU GENERAL HOSPITAL   (Greece)

^k UNIVERSITY HOSPITAL OF IOANNINA   (Greece)

^l ALEXANDRA HOSPITAL   (Greece)

^m Department of Histopathology Agii Anagriri Cancer Hospital   (Greece)

ⁿ HYGEIA HOSPITAL   (Greece)

^o NATIONAL AND KAPODISTRIAN UNIVERSITY OF ATHENS   (Greece)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; PROTEIN P53; PROTEIN PIK3CA; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER GRADING; CANCER SURVIVAL; DISEASE ASSOCIATION; FEMALE; GENE MUTATION; GENETIC CODE; HUMAN; HUMAN CELL; MAJOR CLINICAL STUDY; OUTCOME ASSESSMENT; PHENOTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; TRIPLE NEGATIVE BREAST CANCER; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VOLUME;

EID: 84991644022     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0163138     Document Type: Article

References (44)

1. Carey L, Winer E, Viale G, Cameron D, Gianni L. Triple-negative breast cancer: disease entity or title of convenience? Nature reviews Clinical oncology. 2010; 7(12):683-92. Epub 2010/09/30. doi: 10.1038/nrclinonc.2010.154 PMID: 20877296.
2. Turner NC, Reis-Filho JS. Tackling the diversity of triple-negative breast cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2013; 19(23):6380-8. Epub 2013/12/04. doi: 10.1158/1078-0432.CCR-13-0915 PMID: 24298068.
3. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2009; 27(8):1160-7. Epub 2009/02/11. doi: 10.1200/JCO.2008.18.1370 PMID: 19204204; PubMed Central PMCID: PMC2667820.
4. Linn SC, Van 't Veer LJ. Clinical relevance of the triple-negative breast cancer concept: genetic basis and clinical utility of the concept. Eur J Cancer. 2009; 45 Suppl 1:11-26. Epub 2009/09/25. doi: 10.1016/S0959-8049(09)70012-7 PMID: 19775601.
5. Comprehensive molecular portraits of human breast tumours. Nature. 2012; 490(7418):61-70. Epub 2012/09/25. doi: 10.1038/nature11412 PMID: 23000897; PubMed Central PMCID: PMC3465532.
6. Shah SP, Roth A, Goya R, Oloumi A, Ha G, Zhao Y, et al. The clonal and mutational evolution spectrum of primary triple-negative breast cancers. Nature. 2012; 486(7403):395-9. Epub 2012/04/13. doi: 10.1038/nature10933 PMID: 22495314; PubMed Central PMCID: PMC3863681.
7. Stephens PJ, Tarpey PS, Davies H, Van Loo P, Greenman C, Wedge DC, et al. The landscape of cancer genes and mutational processes in breast cancer. Nature. 2012; 486(7403):400-4. doi: 10.1038/nature11017 PMID: 22722201; PubMed Central PMCID: PMC3428862.
8. Lips EH, Michaut M, Hoogstraat M, Mulder L, Besselink NJ, Koudijs MJ, et al. Next generation sequencing of triple negative breast cancer to find predictors for chemotherapy response. Breast cancer research: BCR. 2015; 17(1):134. doi: 10.1186/s13058-015-0642-8 PMID: 26433948; PubMed Central PMCID: PMC4592753.
9. Wang Y, Waters J, Leung ML, Unruh A, Roh W, Shi X, et al. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature. 2014; 512(7513):155-60. Epub 2014/08/01. doi: 10.1038/nature13600 PMID: 25079324; PubMed Central PMCID: PMC4158312.
10. Savas P, Salgado R, Denkert C, Sotiriou C, Darcy PK, Smyth MJ, et al. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nature reviews Clinical oncology. 2015. Epub 2015/12/17. doi: 10.1038/nrclinonc.2015.215 PMID: 26667975.
11. Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, et al. The evaluation of tumorinfiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO. 2015; 26(2):259-71. Epub 2014/09/13. doi: 10.1093/annonc/mdu450 PMID: 25214542.
12. Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, et al. Prognostic Value of Tumor-Infiltrating Lymphocytes in Triple-Negative Breast Cancers From Two Phase III Randomized Adjuvant Breast Cancer Trials: ECOG 2197 and ECOG 1199. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2014. doi: 10.1200/JCO.2013.55.0491 PMID: 25071121; PubMed Central PMCID: PMC4162494.
13. Kotoula V, Chatzopoulos K, Lakis S, Alexopoulou Z, Timotheadou E, Zagouri F, et al. Tumors with high-density tumor infiltrating lymphocytes constitute a favorable entity in breast cancer: a pooled analysis of four prospective adjuvant trials. Oncotarget. 2015. Epub 2015/10/28. doi: 10.18632/oncotarget.6231 PMID: 26506242.
14. Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO. 2014; 25(8):1544-50. Epub 2014/03/13. doi: 10.1093/annonc/mdu112 PMID: 24608200.
15. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02-98. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2013; 31(7):860-7. Epub 2013/01/24. doi: 10.1200/JCO.2011.41.0902 PMID: 23341518.
16. Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2010; 28(1):105-13. Epub 2009/11/18. doi: 10.1200/JCO.2009.23.7370 PMID: 19917869.
17. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, et al. 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. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2015; 33(9):983-91. Epub 2014/12/24. doi: 10.1200/JCO.2014.58.1967 PMID: 25534375.
18. Dieci MV, Criscitiello C, Goubar A, Viale G, Conte P, Guarneri V, et al. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO. 2014; 25(3):611-8. Epub 2014/01/10. doi: 10.1093/annonc/mdt556 PMID: 24401929; PubMed Central PMCID: PMC3933248.
19. Martin SD, Coukos G, Holt RA, Nelson BH. Targeting the undruggable: immunotherapy meets personalized oncology in the genomic era. Annals of oncology: official journal of the European Society for Medical Oncology / ESMO. 2015; 26(12):2367-74. Epub 2015/09/16. doi: 10.1093/annonc/mdv382 PMID: 26371284; PubMed Central PMCID: PMC4658541.
20. Gubin MM, Artyomov MN, Mardis ER, Schreiber RD. Tumor neoantigens: building a framework for personalized cancer immunotherapy. The Journal of clinical investigation. 2015; 125(9):3413-21. Epub 2015/08/11. doi: 10.1172/JCI80008 PMID: 26258412; PubMed Central PMCID: PMC4588307.
21. Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974; 185 (4154):862-4. PMID: 4843792. doi: 10.1126/science.185.4154.862
22. Robbins PF, El-Gamil M, Li YF, Kawakami Y, Loftus D, Appella E, et al. A mutated beta-catenin gene encodes a melanoma-specific antigen recognized by tumor infiltrating lymphocytes. The Journal of experimental medicine. 1996; 183(3):1185-92. Epub 1996/03/01. PMID: 8642260; PubMed Central PMCID: PMC2192326. doi: 10.1084/jem.183.3.1185
23. Chowell D, Krishna S, Becker PD, Cocita C, Shu J, Tan X, et al. TCR contact residue hydrophobicity is a hallmark of immunogenic CD8+ T cell epitopes. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112(14):E1754-62. Epub 2015/04/02. doi: 10.1073/pnas.1500973112 PMID: 25831525; PubMed Central PMCID: PMC4394253.
24. Kotoula V, Lyberopoulou A, Papadopoulou K, Charalambous E, Alexopoulou Z, Gakou C, et al. Evaluation of two highly-multiplexed custom panels for massively parallel semiconductor sequencing on paraffin DNA. PLOS ONE. 2015; 10(6):e0128818. Epub 2015/06/04. doi: 10.1371/journal.pone.0128818 PMID: 26039550; PubMed Central PMCID: PMC4454570.
25. Fountzilas G, Dafni U, Bobos M, Batistatou A, Kotoula V, Trihia H, et al. Differential response of immunohistochemically defined breast cancer subtypes to anthracycline-based adjuvant chemotherapy with or without paclitaxel. PLOS ONE. 2012; 7(6):e37946. Epub 2012/06/09. doi: 10.1371/journal.pone.0037946 PMID: 22679488; PubMed Central PMCID: PMC3367950.
26. Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2013; 31(31):3997-4013. doi: 10.1200/JCO.2013.50.9984 PMID: 24101045.
27. Badve S, Dabbs DJ, Schnitt SJ, Baehner FL, Decker T, Eusebi V, et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2011; 24(2):157-67. Epub 2010/11/16. doi: 10.1038/modpathol.2010.200 PMID: 21076464.
28. Thusberg J, Olatubosun A, Vihinen M. Performance of mutation pathogenicity prediction methods on missense variants. Human mutation. 2011; 32(4):358-68. Epub 2011/03/18. doi: 10.1002/humu.21445 PMID: 21412949.
29. Martelotto LG, Ng CK, De Filippo MR, Zhang Y, Piscuoglio S, Lim RS, et al. Benchmarking mutation effect prediction algorithms using functionally validated cancer-related missense mutations. Genome biology. 2014; 15(10):484. Epub 2014/10/29. doi: 10.1186/s13059-014-0484-1 PMID: 25348012; PubMed Central PMCID: PMC4232638.
30. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM, et al. REporting recommendations for tumor MARKer prognostic studies (REMARK). Breast cancer research and treatment. 2006; 100(2):229-35. doi: 10.1007/s10549-006-9242-8 PMID: 16932852.
31. McCullough AE, Dell'orto P, Reinholz MM, Gelber RD, Dueck AC, Russo L, et al. Central pathology laboratory review of HER2 and ER in early breast cancer: an ALTTO trial [BIG 2-06/NCCTG N063D (Alliance)] ring study. Breast cancer research and treatment. 2014; 143(3):485-92. Epub 2014/01/08. doi: 10.1007/s10549-013-2827-0 PMID: 24395109; PubMed Central PMCID: PMC4039190.
32. Kriegsmann M, Endris V, Wolf T, Pfarr N, Stenzinger A, Loibl S, et al. Mutational profiles in triple-negative breast cancer defined by ultradeep multigene sequencing show high rates of PI3K pathway alterations and clinically relevant entity subgroup specific differences. Oncotarget. 2014; 5(20):9952-65. Epub 2014/10/10. doi: 10.18632/oncotarget.2481 PMID: 25296970; PubMed Central PMCID: PMC4259450.
33. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C. Emerging landscape of oncogenic signatures across human cancers. Nature genetics. 2013; 45(10):1127-33. Epub 2013/09/28. doi: 10.1038/ng.2762 PMID: 24071851; PubMed Central PMCID: PMC4320046.
34. Banerjee S, Wei Z, Tan F, Peck KN, Shih N, Feldman M, et al. Distinct microbiological signatures associated with triple negative breast cancer. Scientific reports. 2015; 5:15162. Epub 2015/10/16. doi: 10.1038/srep15162 PMID: 26469225; PubMed Central PMCID: PMC4606812.
35. Kumai T, Ishibashi K, Oikawa K, Matsuda Y, Aoki N, Kimura S, et al. Induction of tumor-reactive T helper responses by a posttranslational modified epitope from tumor protein p53. Cancer immunology, immunotherapy: CII. 2014; 63(5):469-78. Epub 2014/03/19. doi: 10.1007/s00262-014-1533-z PMID: 24633296.
36. Met O, Balslev E, Flyger H, Svane IM. High immunogenic potential of p53 mRNA-transfected dendritic cells in patients with primary breast cancer. Breast cancer research and treatment. 2011; 125(2):395-406. Epub 2010/03/26. doi: 10.1007/s10549-010-0844-9 PMID: 20336365.
37. Strub C, Alies C, Lougarre A, Ladurantie C, Czaplicki J, Fournier D. Mutation of exposed hydrophobic amino acids to arginine to increase protein stability. BMC biochemistry. 2004; 5:9. Epub 2004/07/15. doi: 10.1186/1471-2091-5-9 PMID: 15251041; PubMed Central PMCID: PMC479692.
38. Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015; 348 (6230):69-74. Epub 2015/04/04. doi: 10.1126/science.aaa4971 PMID: 25838375.
39. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 2011; 331(6024):1565-70. Epub 2011/03/26. doi: 10.1126/science.1203486 PMID: 21436444.
40. Loi S, Dushyanthen S, Beavis PA, Salgado R, Denkert C, Savas P, et al. RAS/MAPK Activation Is Associated with Reduced Tumor-Infiltrating Lymphocytes in Triple-Negative Breast Cancer: Therapeutic Cooperation Between MEK and PD-1/PD-L1 Immune Checkpoint Inhibitors. Clinical cancer research: an official journal of the American Association for Cancer Research. 2015. Epub 2015/10/31. doi: 10.1158/1078-0432.CCR-15-1125 PMID: 26515496.
41. Cheang MC, Martin M, Nielsen TO, Prat A, Voduc D, Rodriguez-Lescure A, et al. Defining breast cancer intrinsic subtypes by quantitative receptor expression. The oncologist. 2015; 20(5):474-82. Epub 2015/04/25. doi: 10.1634/theoncologist.2014-0372 PMID: 25908555; PubMed Central PMCID: PMC4425383.
42. Bao L, Cardiff RD, Steinbach P, Messer KS, Ellies LG. Multipotent luminal mammary cancer stem cells model tumor heterogeneity. Breast cancer research: BCR. 2015; 17(1):137. Epub 2015/10/16. doi: 10.1186/s13058-015-0615-y PMID: 26467658; PubMed Central PMCID: PMC4606989.
43. Ng CK, Martelotto LG, Gauthier A, Wen HC, Piscuoglio S, Lim RS, et al. Intra-tumor genetic heterogeneity and alternative driver genetic alterations in breast cancers with heterogeneous HER2 gene amplification. Genome biology. 2015; 16:107. Epub 2015/05/23. doi: 10.1186/s13059-015-0657-6 PMID: 25994018; PubMed Central PMCID: PMC4440518.
44. Ng CK, Schultheis AM, Bidard FC, Weigelt B, Reis-Filho JS. Breast cancer genomics from microarrays to massively parallel sequencing: paradigms and new insights. Journal of the National Cancer Institute. 2015; 107(5). Epub 2015/02/26. doi: 10.1093/jnci/djv015 PMID: 25713166.