Skip to main content
Top
Published in: BMC Cancer 1/2018

Open Access 01-12-2018 | Debate

Mechanisms of immune evasion in breast cancer

Authors: Joshua P. Bates, Roshanak Derakhshandeh, Laundette Jones, Tonya J. Webb

Published in: BMC Cancer | Issue 1/2018

Login to get access

Abstract

Tumors develop multiple mechanisms of immune evasion as they progress, with some cancer types being inherently better at ‘hiding’ than others. With an increased understanding of tumor immune surveillance, immunotherapy has emerged as a promising treatment strategy for breast cancer, despite historically being thought of as an immunologically silent neoplasm. Some types of cancer, such as melanoma, bladder, and renal cell carcinoma, have demonstrated a durable response to immunotherapeutic intervention, however, breast neoplasms have not shown the same efficacy. The causes of breast cancer’s immune silence derive from mechanisms that diminish immune recognition and others that promote strong immunosuppression. It is the mechanisms of immune evasion in breast cancers that are poorly defined. Thus, further characterization is critical for the development of better therapies. This brief review will seek to provide insight into the possible causes of weak immunogenicity and immune suppression mediated by breast cancers and highlight current immunotherapies being used to restore immune responses to breast cancer.
Literature
4.
6.
go back to reference Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J, Elkord E, Lichtor T, Decker WK, Whelan RL, Kumara HS. Immune evasion in cancer: mechanistic basis and therapeutic strategies. In: Seminars in Cancer biology: 2015: Elsevier; 2015. p. S185–98. Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J, Elkord E, Lichtor T, Decker WK, Whelan RL, Kumara HS. Immune evasion in cancer: mechanistic basis and therapeutic strategies. In: Seminars in Cancer biology: 2015: Elsevier; 2015. p. S185–98.
7.
go back to reference Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to Cancer. Annu Rev Immunol. 2011;29(1):235–71.PubMedCrossRef Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to Cancer. Annu Rev Immunol. 2011;29(1):235–71.PubMedCrossRef
8.
go back to reference van den Broek ME, Kagi D, Ossendorp F, Toes R, Vamvakas S, Lutz WK, Melief CJ, Zinkernagel RM, Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J Exp Med. 1996;184(5):1781–90.PubMedCrossRef van den Broek ME, Kagi D, Ossendorp F, Toes R, Vamvakas S, Lutz WK, Melief CJ, Zinkernagel RM, Hengartner H. Decreased tumor surveillance in perforin-deficient mice. J Exp Med. 1996;184(5):1781–90.PubMedCrossRef
10.
go back to reference Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410(6832):1107–11.PubMedCrossRef Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410(6832):1107–11.PubMedCrossRef
11.
go back to reference Teng MWL, Swann JB, Koebel CM, Schreiber RD, Smyth MJ. Immune-mediated dormancy: an equilibrium with cancer. J Leukoc Biol. 2008;84(4):988–93.PubMedCrossRef Teng MWL, Swann JB, Koebel CM, Schreiber RD, Smyth MJ. Immune-mediated dormancy: an equilibrium with cancer. J Leukoc Biol. 2008;84(4):988–93.PubMedCrossRef
12.
go back to reference Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol. 2006;90:51–81.PubMedCrossRef Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol. 2006;90:51–81.PubMedCrossRef
13.
go back to reference Harbeck N, Beckmann MW, Rody A, Schneeweiss A, Müller V, Fehm T, Marschner N, Gluz O, Schrader I, Heinrich G. HER2 dimerization inhibitor pertuzumab-mode of action and clinical data in breast cancer. Breast Care. 2013;8(1):49–55.PubMedPubMedCentralCrossRef Harbeck N, Beckmann MW, Rody A, Schneeweiss A, Müller V, Fehm T, Marschner N, Gluz O, Schrader I, Heinrich G. HER2 dimerization inhibitor pertuzumab-mode of action and clinical data in breast cancer. Breast Care. 2013;8(1):49–55.PubMedPubMedCentralCrossRef
14.
go back to reference Baselga J, Cortés J, Kim S-B, Im S-A, Hegg R, Im Y-H, Roman L, Pedrini JL, Pienkowski T, Knott A. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med. 2012;366(2):109–19.PubMedCrossRef Baselga J, Cortés J, Kim S-B, Im S-A, Hegg R, Im Y-H, Roman L, Pedrini JL, Pienkowski T, Knott A. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med. 2012;366(2):109–19.PubMedCrossRef
15.
go back to reference Gianni L, Pienkowski T, Im Y-H, Roman L, Tseng L-M, Liu M-C, Lluch A, Staroslawska E, de la Haba-Rodriguez J, Im S-A. Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. Lancet Oncol. 2012;13(1):25–32.PubMedCrossRef Gianni L, Pienkowski T, Im Y-H, Roman L, Tseng L-M, Liu M-C, Lluch A, Staroslawska E, de la Haba-Rodriguez J, Im S-A. Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. Lancet Oncol. 2012;13(1):25–32.PubMedCrossRef
16.
go back to reference Schneeweiss A, Chia S, Hickish T, Harvey V, Eniu A, Hegg R, Tausch C, Seo JH, Tsai Y-F, Ratnayake J. Pertuzumab plus trastuzumab in combination with standard neoadjuvant anthracycline-containing and anthracycline-free chemotherapy regimens in patients with HER2-positive early breast cancer: a randomized phase II cardiac safety study (TRYPHAENA). Ann Oncol. 2013;24(9):2278–84.PubMedCrossRef Schneeweiss A, Chia S, Hickish T, Harvey V, Eniu A, Hegg R, Tausch C, Seo JH, Tsai Y-F, Ratnayake J. Pertuzumab plus trastuzumab in combination with standard neoadjuvant anthracycline-containing and anthracycline-free chemotherapy regimens in patients with HER2-positive early breast cancer: a randomized phase II cardiac safety study (TRYPHAENA). Ann Oncol. 2013;24(9):2278–84.PubMedCrossRef
17.
go back to reference Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh D-Y, Diéras V, Guardino E. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012;367(19):1783–91.PubMedPubMedCentralCrossRef Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh D-Y, Diéras V, Guardino E. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012;367(19):1783–91.PubMedPubMedCentralCrossRef
18.
go back to reference Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med. 2006;355(26):2733–43.PubMedCrossRef Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med. 2006;355(26):2733–43.PubMedCrossRef
19.
go back to reference Park JW, Liu MC, Yee D, Yau C, van’t Veer LJ, Symmans WF, Paoloni M, Perlmutter J, Hylton NM, Hogarth M. Adaptive randomization of neratinib in early breast cancer. N Engl J Med. 2016;375(1):11–22.PubMedPubMedCentralCrossRef Park JW, Liu MC, Yee D, Yau C, van’t Veer LJ, Symmans WF, Paoloni M, Perlmutter J, Hylton NM, Hogarth M. Adaptive randomization of neratinib in early breast cancer. N Engl J Med. 2016;375(1):11–22.PubMedPubMedCentralCrossRef
20.
go back to reference Onitilo AA, Engel JM, Greenlee RT, Mukesh BN. Breast Cancer subtypes based on ER/PR and Her2 expression: comparison of Clinicopathologic features and survival. Clin Med Res. 2009;7(1–2):4–13.PubMedPubMedCentralCrossRef Onitilo AA, Engel JM, Greenlee RT, Mukesh BN. Breast Cancer subtypes based on ER/PR and Her2 expression: comparison of Clinicopathologic features and survival. Clin Med Res. 2009;7(1–2):4–13.PubMedPubMedCentralCrossRef
21.
go back to reference Staaf J, Ringnér M, Vallon-Christersson J, Jönsson G, Bendahl P-O, Holm K, Arason A, Gunnarsson H, Hegardt C, Agnarsson BA. Identification of subtypes in human epidermal growth factor receptor 2–positive breast cancer reveals a gene signature prognostic of outcome. J Clin Oncol. 2010;28(11):1813–20.PubMedCrossRef Staaf J, Ringnér M, Vallon-Christersson J, Jönsson G, Bendahl P-O, Holm K, Arason A, Gunnarsson H, Hegardt C, Agnarsson BA. Identification of subtypes in human epidermal growth factor receptor 2–positive breast cancer reveals a gene signature prognostic of outcome. J Clin Oncol. 2010;28(11):1813–20.PubMedCrossRef
22.
go back to reference Teschendorff AE, Miremadi A, Pinder SE, Ellis IO, Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 2007;8(8):R157.PubMedPubMedCentralCrossRef Teschendorff AE, Miremadi A, Pinder SE, Ellis IO, Caldas C. An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 2007;8(8):R157.PubMedPubMedCentralCrossRef
23.
go back to reference 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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
24.
go back to reference Zakaria F, El-Mashad N, Mohamed D. Androgen receptor expression as a prognostic and predictive marker in triple-negative breast cancer patients. Alexandria J Med. 2016;52(2):131–40.CrossRef Zakaria F, El-Mashad N, Mohamed D. Androgen receptor expression as a prognostic and predictive marker in triple-negative breast cancer patients. Alexandria J Med. 2016;52(2):131–40.CrossRef
25.
go back to reference Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. Prognostic markers in triple-negative breast cancer. Cancer. 2007;109(1):25–32.PubMedCrossRef Rakha EA, El-Sayed ME, Green AR, Lee AH, Robertson JF, Ellis IO. Prognostic markers in triple-negative breast cancer. Cancer. 2007;109(1):25–32.PubMedCrossRef
26.
go back to reference Sutton LM, Cao D, Sarode V, Molberg KH, Torgbe K, Haley B, Peng Y. Decreased androgen receptor expression is associated with distant metastases in patients with androgen receptor–expressing triple-negative breast carcinoma. Am J Clin Pathol. 2012;138(4):511–6.PubMedCrossRef Sutton LM, Cao D, Sarode V, Molberg KH, Torgbe K, Haley B, Peng Y. Decreased androgen receptor expression is associated with distant metastases in patients with androgen receptor–expressing triple-negative breast carcinoma. Am J Clin Pathol. 2012;138(4):511–6.PubMedCrossRef
27.
go back to reference Pistelli M, Caramanti M, Biscotti T, Santinelli A, Pagliacci A, De Lisa M, Ballatore Z, Ridolfi F, Maccaroni E, Bracci R. Androgen receptor expression in early triple-negative breast cancer: clinical significance and prognostic associations. Cancers. 2014;6(3):1351–62.PubMedPubMedCentralCrossRef Pistelli M, Caramanti M, Biscotti T, Santinelli A, Pagliacci A, De Lisa M, Ballatore Z, Ridolfi F, Maccaroni E, Bracci R. Androgen receptor expression in early triple-negative breast cancer: clinical significance and prognostic associations. Cancers. 2014;6(3):1351–62.PubMedPubMedCentralCrossRef
28.
go back to reference Rampurwala M, Wisinski KB, O'Regan R. Role of the androgen receptor in triple-negative breast cancer. Clin Adv Hematol Oncol. 2016;14(3):186–93.PubMedPubMedCentral Rampurwala M, Wisinski KB, O'Regan R. Role of the androgen receptor in triple-negative breast cancer. Clin Adv Hematol Oncol. 2016;14(3):186–93.PubMedPubMedCentral
29.
go back to reference Masuda H, Baggerly KA, Wang Y, Zhang Y, Gonzalez-Angulo AM, Meric-Bernstam F, Valero V, Lehmann BD, Pietenpol JA, Hortobagyi GN. Differential response to neoadjuvant chemotherapy among 7 triple-negative breast cancer molecular subtypes. Clin Cancer Res. 2013;19(19):5533–40.PubMedCrossRef Masuda H, Baggerly KA, Wang Y, Zhang Y, Gonzalez-Angulo AM, Meric-Bernstam F, Valero V, Lehmann BD, Pietenpol JA, Hortobagyi GN. Differential response to neoadjuvant chemotherapy among 7 triple-negative breast cancer molecular subtypes. Clin Cancer Res. 2013;19(19):5533–40.PubMedCrossRef
30.
go back to reference Choi JE, Kang SH, Lee SJ, Bae YK. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann Surg Oncol. 2015;22(1):82–9.PubMedCrossRef Choi JE, Kang SH, Lee SJ, Bae YK. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann Surg Oncol. 2015;22(1):82–9.PubMedCrossRef
31.
go back to reference Miller LD, Chou JA, Black MA, Chifman J, Alistar A, Putti T, Zhou X, Bedognetti D, Hendrickx W, Pullikuth A. Immunogenic subtypes of breast Cancer delineated by gene classifiers of immune responsiveness. Cancer immunology research. 2016;4(7):600–10.PubMedPubMedCentralCrossRef Miller LD, Chou JA, Black MA, Chifman J, Alistar A, Putti T, Zhou X, Bedognetti D, Hendrickx W, Pullikuth A. Immunogenic subtypes of breast Cancer delineated by gene classifiers of immune responsiveness. Cancer immunology research. 2016;4(7):600–10.PubMedPubMedCentralCrossRef
32.
go back to reference Denkert C. The immunogenicity of breast cancer—molecular subtypes matter. Ann Oncol. 2014;25(8):1453–5.PubMedCrossRef Denkert C. The immunogenicity of breast cancer—molecular subtypes matter. Ann Oncol. 2014;25(8):1453–5.PubMedCrossRef
34.
go back to reference Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539–45.PubMedCrossRef Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet. 2001;357(9255):539–45.PubMedCrossRef
35.
go back to reference Erreni M, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) and inflammation in colorectal cancer. Cancer Microenviron. 2011;4(2):141–54.PubMedCrossRef Erreni M, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) and inflammation in colorectal cancer. Cancer Microenviron. 2011;4(2):141–54.PubMedCrossRef
36.
go back to reference Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, Ojeifo J, Jiao X, Yeow W-S, Katiyar S. The canonical NF-κB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res. 2010;70(24):10464–73.PubMedPubMedCentralCrossRef Liu M, Sakamaki T, Casimiro MC, Willmarth NE, Quong AA, Ju X, Ojeifo J, Jiao X, Yeow W-S, Katiyar S. The canonical NF-κB pathway governs mammary tumorigenesis in transgenic mice and tumor stem cell expansion. Cancer Res. 2010;70(24):10464–73.PubMedPubMedCentralCrossRef
37.
go back to reference Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, Baumgartner KB, Gilliland FD, Sorensen BE, McTiernan A. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol. 2009;27(21):3437–44.PubMedPubMedCentralCrossRef Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, Baumgartner KB, Gilliland FD, Sorensen BE, McTiernan A. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol. 2009;27(21):3437–44.PubMedPubMedCentralCrossRef
38.
go back to reference Ammirante M, Luo J-L, Grivennikov S, Nedospasov S, Karin M. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature. 2010;464(7286):302–5.PubMedPubMedCentralCrossRef Ammirante M, Luo J-L, Grivennikov S, Nedospasov S, Karin M. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature. 2010;464(7286):302–5.PubMedPubMedCentralCrossRef
39.
go back to reference De Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24–37.PubMedCrossRef De Visser KE, Eichten A, Coussens LM. Paradoxical roles of the immune system during cancer development. Nat Rev Cancer. 2006;6(1):24–37.PubMedCrossRef
40.
go back to reference Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med. 2007;13(10):1211–8.PubMedCrossRef Soucek L, Lawlor ER, Soto D, Shchors K, Swigart LB, Evan GI. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat Med. 2007;13(10):1211–8.PubMedCrossRef
41.
go back to reference Stewart T, Tsai S-C, Grayson H, Henderson R, Opelz G. Incidence of de-novo breast cancer in women chronically immunosuppressed after organ transplantation. Lancet. 1995;346(8978):796–8.PubMedCrossRef Stewart T, Tsai S-C, Grayson H, Henderson R, Opelz G. Incidence of de-novo breast cancer in women chronically immunosuppressed after organ transplantation. Lancet. 1995;346(8978):796–8.PubMedCrossRef
42.
go back to reference Oluwole SF, Ali AO, Shafaee Z, Depaz HA. Breast cancer in women with HIV/AIDS: report of five cases with a review of the literature. J Surg Oncol. 2005;89(1):23–7.PubMedCrossRef Oluwole SF, Ali AO, Shafaee Z, Depaz HA. Breast cancer in women with HIV/AIDS: report of five cases with a review of the literature. J Surg Oncol. 2005;89(1):23–7.PubMedCrossRef
43.
go back to reference Harris RE, Chlebowski RT, Jackson RD, Frid DJ, Ascenseo JL, Anderson G, Loar A, Rodabough RJ, White E, McTiernan A. Breast Cancer and nonsteroidal anti-inflammatory drugs. Cancer Res. 2003;63(18):6096–101.PubMed Harris RE, Chlebowski RT, Jackson RD, Frid DJ, Ascenseo JL, Anderson G, Loar A, Rodabough RJ, White E, McTiernan A. Breast Cancer and nonsteroidal anti-inflammatory drugs. Cancer Res. 2003;63(18):6096–101.PubMed
44.
go back to reference Hoption Cann SA, van Netten JP, van Netten C. Dr William Coley and tumour regression: a place in history or in the future. Postgrad Med J. 2003;79(938):672–80.PubMedPubMedCentral Hoption Cann SA, van Netten JP, van Netten C. Dr William Coley and tumour regression: a place in history or in the future. Postgrad Med J. 2003;79(938):672–80.PubMedPubMedCentral
46.
go back to reference Mamessier E, Sylvain A, Thibult M-L, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest. 2011;121(9):3609–22.PubMedPubMedCentralCrossRef Mamessier E, Sylvain A, Thibult M-L, Houvenaeghel G, Jacquemier J, Castellano R, Gonçalves A, André P, Romagné F, Thibault G. Human breast cancer cells enhance self tolerance by promoting evasion from NK cell antitumor immunity. J Clin Invest. 2011;121(9):3609–22.PubMedPubMedCentralCrossRef
47.
go back to reference Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28(1):105–13.PubMedCrossRef Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28(1):105–13.PubMedCrossRef
48.
go back to reference Denkert C, Von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD. 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;33(9):983–91.PubMedCrossRef Denkert C, Von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD. 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;33(9):983–91.PubMedCrossRef
49.
go back to reference Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen P-L, Bono P, Kataja V, Desmedt C. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014;25(8):1544–50.PubMedCrossRef Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen P-L, Bono P, Kataja V, Desmedt C. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014;25(8):1544–50.PubMedCrossRef
50.
go back to reference Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, Martino S, Wang M, Jones VE, Saphner TJ. 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. J Clin Oncol. 2014;32(27):2959–66.PubMedPubMedCentralCrossRef Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, Martino S, Wang M, Jones VE, Saphner TJ. 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. J Clin Oncol. 2014;32(27):2959–66.PubMedPubMedCentralCrossRef
51.
go back to reference Pruneri G, Gray KP, Vingiani A, Viale G, Curigliano G, Criscitiello C, Láng I, Ruhstaller T, Gianni L, Goldhirsch A, et al. Tumor-infiltrating lymphocytes (TILs) are a powerful prognostic marker in patients with triple-negative breast cancer enrolled in the IBCSG phase III randomized clinical trial 22-00. Breast Cancer Res Treat. 2016;158(2):323–31.PubMedPubMedCentralCrossRef Pruneri G, Gray KP, Vingiani A, Viale G, Curigliano G, Criscitiello C, Láng I, Ruhstaller T, Gianni L, Goldhirsch A, et al. Tumor-infiltrating lymphocytes (TILs) are a powerful prognostic marker in patients with triple-negative breast cancer enrolled in the IBCSG phase III randomized clinical trial 22-00. Breast Cancer Res Treat. 2016;158(2):323–31.PubMedPubMedCentralCrossRef
52.
go back to reference Kroemer G, Senovilla L, Galluzzi L, André F, Zitvogel L. Natural and therapy-induced immunosurveillance in breast cancer. Nat Med. 2015;21(10):1128–38.PubMedCrossRef Kroemer G, Senovilla L, Galluzzi L, André F, Zitvogel L. Natural and therapy-induced immunosurveillance in breast cancer. Nat Med. 2015;21(10):1128–38.PubMedCrossRef
53.
go back to reference Yu X, Zhang Z, Wang Z, Wu P, Qiu F, Huang J. Prognostic and predictive value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. Clin Transl Oncol. 2015:1–10. Yu X, Zhang Z, Wang Z, Wu P, Qiu F, Huang J. Prognostic and predictive value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. Clin Transl Oncol. 2015:1–10.
54.
go back to reference Miyashita M, Sasano H, Tamaki K, Hirakawa H, Takahashi Y, Nakagawa S, Watanabe G, Tada H, Suzuki A, Ohuchi N. Prognostic significance of tumor-infiltrating CD8+ and FOXP3+ lymphocytes in residual tumors and alterations in these parameters after neoadjuvant chemotherapy in triple-negative breast cancer: a retrospective multicenter study. Breast Cancer Res. 2015;17(1):1–13.CrossRef Miyashita M, Sasano H, Tamaki K, Hirakawa H, Takahashi Y, Nakagawa S, Watanabe G, Tada H, Suzuki A, Ohuchi N. Prognostic significance of tumor-infiltrating CD8+ and FOXP3+ lymphocytes in residual tumors and alterations in these parameters after neoadjuvant chemotherapy in triple-negative breast cancer: a retrospective multicenter study. Breast Cancer Res. 2015;17(1):1–13.CrossRef
55.
go back to reference Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, Ellis IO, Green AR. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol. 2011;29(15):1949–55.PubMedCrossRef Mahmoud SM, Paish EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, Ellis IO, Green AR. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol. 2011;29(15):1949–55.PubMedCrossRef
56.
go back to reference Iwamoto M, Shinohara H, Miyamoto A, Okuzawa M, Mabuchi H, Nohara T, Gon G, Toyoda M, Tanigawa N. Prognostic value of tumor-infiltrating dendritic cells expressing CD83 in human breast carcinomas. Int J Cancer. 2003;104(1):92–7.PubMedCrossRef Iwamoto M, Shinohara H, Miyamoto A, Okuzawa M, Mabuchi H, Nohara T, Gon G, Toyoda M, Tanigawa N. Prognostic value of tumor-infiltrating dendritic cells expressing CD83 in human breast carcinomas. Int J Cancer. 2003;104(1):92–7.PubMedCrossRef
57.
go back to reference Brown JR, Wimberly H, Lannin DR, Nixon C, Rimm DL, Bossuyt V. Multiplexed quantitative analysis of CD3, CD8, and CD20 predicts response to neoadjuvant chemotherapy in breast cancer. Clin Cancer Res. 2014;20(23):5995–6005.PubMedPubMedCentralCrossRef Brown JR, Wimberly H, Lannin DR, Nixon C, Rimm DL, Bossuyt V. Multiplexed quantitative analysis of CD3, CD8, and CD20 predicts response to neoadjuvant chemotherapy in breast cancer. Clin Cancer Res. 2014;20(23):5995–6005.PubMedPubMedCentralCrossRef
58.
go back to reference Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–92.PubMedPubMedCentralCrossRef Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G. CD4+ follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–92.PubMedPubMedCentralCrossRef
59.
go back to reference Lutz ER, Wu AA, Bigelow E, Sharma R, Mo G, Soares K, Solt S, Dorman A, Wamwea A, Yager A, et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol Res. 2014;2(7):616–31.PubMedPubMedCentralCrossRef Lutz ER, Wu AA, Bigelow E, Sharma R, Mo G, Soares K, Solt S, Dorman A, Wamwea A, Yager A, et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol Res. 2014;2(7):616–31.PubMedPubMedCentralCrossRef
60.
go back to reference Lee HJ, Kim JY, Park IA, Song IH, Yu JH, Ahn J-H, Gong G. Prognostic significance of tumor-infiltrating lymphocytes and the tertiary lymphoid structures in HER2-positive breast Cancer treated with adjuvant Trastuzumab. Am J Clin Pathol. 2015;144(2):278–88.PubMedCrossRef Lee HJ, Kim JY, Park IA, Song IH, Yu JH, Ahn J-H, Gong G. Prognostic significance of tumor-infiltrating lymphocytes and the tertiary lymphoid structures in HER2-positive breast Cancer treated with adjuvant Trastuzumab. Am J Clin Pathol. 2015;144(2):278–88.PubMedCrossRef
61.
go back to reference Loi S, Dushyanthen S, Beavis PA, Salgado R, Denkert C, Savas P, Combs S, Rimm DL, Giltnane JM, Estrada MV. 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. Clin Cancer Res. 2016;22(6):1499–509.PubMedCrossRef Loi S, Dushyanthen S, Beavis PA, Salgado R, Denkert C, Savas P, Combs S, Rimm DL, Giltnane JM, Estrada MV. 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. Clin Cancer Res. 2016;22(6):1499–509.PubMedCrossRef
62.
go back to reference Lake RA, Robinson BW. Immunotherapy and chemotherapy—a practical partnership. Nat Rev Cancer. 2005;5(5):397–405.PubMedCrossRef Lake RA, Robinson BW. Immunotherapy and chemotherapy—a practical partnership. Nat Rev Cancer. 2005;5(5):397–405.PubMedCrossRef
63.
go back to reference Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med. 2005;202(12):1691.PubMedPubMedCentralCrossRef Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, Schmitt E, Hamai A, Hervas-Stubbs S, Obeid M, et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med. 2005;202(12):1691.PubMedPubMedCentralCrossRef
64.
go back to reference Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini J-L, Castedo M, Mignot G, Panaretakis T, Casares N, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13(1):54–61.PubMedCrossRef Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini J-L, Castedo M, Mignot G, Panaretakis T, Casares N, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13(1):54–61.PubMedCrossRef
65.
go back to reference Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P. Toll-like receptor 4–dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050–9.PubMedCrossRef Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P. Toll-like receptor 4–dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med. 2007;13(9):1050–9.PubMedCrossRef
66.
go back to reference Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51–72.PubMedCrossRef Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51–72.PubMedCrossRef
67.
go back to reference Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, Špíšek R. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res. 2011;71(14):4821–33.PubMedCrossRef Fucikova J, Kralikova P, Fialova A, Brtnicky T, Rob L, Bartunkova J, Špíšek R. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res. 2011;71(14):4821–33.PubMedCrossRef
68.
go back to reference Yeo B, Kotsori K, Mohammed K, Walsh G, Smith I. Long-term outcome of HER2 positive metastatic breast cancer patients treated with first-line trastuzumab. Breast. 2015;24(6):751–7.PubMedCrossRef Yeo B, Kotsori K, Mohammed K, Walsh G, Smith I. Long-term outcome of HER2 positive metastatic breast cancer patients treated with first-line trastuzumab. Breast. 2015;24(6):751–7.PubMedCrossRef
69.
go back to reference Nahta R, Yu D, Hung MC, Hortobagyi GN, Esteva FJ. Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol. 2006;3(5):269–80.PubMedCrossRef Nahta R, Yu D, Hung MC, Hortobagyi GN, Esteva FJ. Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol. 2006;3(5):269–80.PubMedCrossRef
70.
go back to reference Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med. 2000;6(4):443–6.PubMedCrossRef Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med. 2000;6(4):443–6.PubMedCrossRef
71.
go back to reference Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, Laccabue D, Zerbini A, Camisa R, Bisagni G. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu–positive metastatic breast cancer. J Clin Oncol. 2008;26(11):1789–96.PubMedCrossRef Musolino A, Naldi N, Bortesi B, Pezzuolo D, Capelletti M, Missale G, Laccabue D, Zerbini A, Camisa R, Bisagni G. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu–positive metastatic breast cancer. J Clin Oncol. 2008;26(11):1789–96.PubMedCrossRef
72.
go back to reference Baron JM, Boster BL, Barnett CM. Ado-trastuzumab emtansine (T-DM1): a novel antibody-drug conjugate for the treatment of HER2-positive metastatic breast cancer. J Oncol Pharm Pract. 2014; 1078155214527144 Baron JM, Boster BL, Barnett CM. Ado-trastuzumab emtansine (T-DM1): a novel antibody-drug conjugate for the treatment of HER2-positive metastatic breast cancer. J Oncol Pharm Pract. 2014; 1078155214527144
73.
go back to reference Milani A, Sangiolo D, Montemurro F, Aglietta M, Valabrega G. Active immunotherapy in HER2 overexpressing breast cancer: current status and future perspectives. Ann Oncol. 2013;24(7):1740–8.PubMedCrossRef Milani A, Sangiolo D, Montemurro F, Aglietta M, Valabrega G. Active immunotherapy in HER2 overexpressing breast cancer: current status and future perspectives. Ann Oncol. 2013;24(7):1740–8.PubMedCrossRef
74.
go back to reference Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008;8(1):59–73.PubMedCrossRef Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008;8(1):59–73.PubMedCrossRef
75.
go back to reference Hossain DMS, Panda AK, Manna A, Mohanty S, Bhattacharjee P, Bhattacharyya S, Saha T, Chakraborty S, Kar RK, Das T. FoxP3 acts as a cotranscription factor with STAT3 in tumor-induced regulatory T cells. Immunity. 2013;39(6):1057–69.PubMedCrossRef Hossain DMS, Panda AK, Manna A, Mohanty S, Bhattacharjee P, Bhattacharyya S, Saha T, Chakraborty S, Kar RK, Das T. FoxP3 acts as a cotranscription factor with STAT3 in tumor-induced regulatory T cells. Immunity. 2013;39(6):1057–69.PubMedCrossRef
76.
go back to reference Ladoire S, Arnould L, Apetoh L, Coudert B, Martin F, Chauffert B, Fumoleau P, Ghiringhelli F. Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clin Cancer Res. 2008;14(8):2413–20.PubMedCrossRef Ladoire S, Arnould L, Apetoh L, Coudert B, Martin F, Chauffert B, Fumoleau P, Ghiringhelli F. Pathologic complete response to neoadjuvant chemotherapy of breast carcinoma is associated with the disappearance of tumor-infiltrating foxp3+ regulatory T cells. Clin Cancer Res. 2008;14(8):2413–20.PubMedCrossRef
77.
go back to reference Lutsiak MC, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4+ 25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood. 2005;105(7):2862–8.PubMedCrossRef Lutsiak MC, Semnani RT, De Pascalis R, Kashmiri SV, Schlom J, Sabzevari H. Inhibition of CD4+ 25+ T regulatory cell function implicated in enhanced immune response by low-dose cyclophosphamide. Blood. 2005;105(7):2862–8.PubMedCrossRef
78.
go back to reference Ladoire S, Mignot G, Dabakuyo S, Arnould L, Apetoh L, Rébé C, Coudert B, Martin F, Bizollon MH, Vanoli A. In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival. J Pathol. 2011;224(3):389–400.PubMedCrossRef Ladoire S, Mignot G, Dabakuyo S, Arnould L, Apetoh L, Rébé C, Coudert B, Martin F, Bizollon MH, Vanoli A. In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival. J Pathol. 2011;224(3):389–400.PubMedCrossRef
79.
go back to reference Bezu L, Gomes-da-Silva LC, Dewitte H, Breckpot K, Fucikova J, Spisek R, Galluzzi L, Kepp O, Kroemer G. Combinatorial strategies for the induction of immunogenic cell death. Front Immunol. 2015;6:187.PubMedPubMedCentral Bezu L, Gomes-da-Silva LC, Dewitte H, Breckpot K, Fucikova J, Spisek R, Galluzzi L, Kepp O, Kroemer G. Combinatorial strategies for the induction of immunogenic cell death. Front Immunol. 2015;6:187.PubMedPubMedCentral
80.
go back to reference Gebremeskel S, Johnston B. Concepts and mechanisms underlying chemotherapy induced immunogenic cell death: Impact on clinical studies and considerations for combined therapies. Oncotarget. 2015;6:41600–41619. Gebremeskel S, Johnston B. Concepts and mechanisms underlying chemotherapy induced immunogenic cell death: Impact on clinical studies and considerations for combined therapies. Oncotarget. 2015;6:41600–41619.
81.
go back to reference Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, Vermaelen K, Panaretakis T, Mignot G, Ullrich E. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1β–dependent adaptive immunity against tumors. Nat Med. 2009;15(10):1170–8.PubMedCrossRef Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C, Vermaelen K, Panaretakis T, Mignot G, Ullrich E. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1β–dependent adaptive immunity against tumors. Nat Med. 2009;15(10):1170–8.PubMedCrossRef
82.
go back to reference DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer discovery. 2011;1(1):54–67.PubMedPubMedCentralCrossRef DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, Gallagher WM, Wadhwani N, Keil SD, Junaid SA. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer discovery. 2011;1(1):54–67.PubMedPubMedCentralCrossRef
83.
go back to reference Zhang B, Bowerman NA, Salama JK, Schmidt H, Spiotto MT, Schietinger A, Yu P, Fu Y-X, Weichselbaum RR, Rowley DA. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med. 2007;204(1):49–55.PubMedPubMedCentralCrossRef Zhang B, Bowerman NA, Salama JK, Schmidt H, Spiotto MT, Schietinger A, Yu P, Fu Y-X, Weichselbaum RR, Rowley DA. Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med. 2007;204(1):49–55.PubMedPubMedCentralCrossRef
84.
go back to reference Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, de Ru AH, Neijssen J. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006;203(5):1259–71.PubMedPubMedCentralCrossRef Reits EA, Hodge JW, Herberts CA, Groothuis TA, Chakraborty M, Wansley EK, Camphausen K, Luiten RM, de Ru AH, Neijssen J. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006;203(5):1259–71.PubMedPubMedCentralCrossRef
85.
go back to reference Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, Allison JP, Formenti SC. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res. 2005;11(2):728–34.PubMed Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, Allison JP, Formenti SC. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res. 2005;11(2):728–34.PubMed
86.
go back to reference Golden EB, Demaria S, Schiff PB, Chachoua A, Formenti SC. An abscopal response to radiation and ipilimumab in a patient with metastatic non–small cell lung cancer. Cancer Immunology Research. 2013;1(6):365–72.PubMedPubMedCentralCrossRef Golden EB, Demaria S, Schiff PB, Chachoua A, Formenti SC. An abscopal response to radiation and ipilimumab in a patient with metastatic non–small cell lung cancer. Cancer Immunology Research. 2013;1(6):365–72.PubMedPubMedCentralCrossRef
87.
go back to reference Golden E, Chachoua A, Fenton-Kerimian M, Demaria S, Formenti S. Abscopal responses in metastatic non-small cell lung cancer (NSCLC) patients treated on a phase 2 study of combined radiation therapy and ipilimumab: evidence for the in situ vaccination hypothesis of radiation. Int J Rad Oncol Biol Phys. 2015;93(3):S66–7.CrossRef Golden E, Chachoua A, Fenton-Kerimian M, Demaria S, Formenti S. Abscopal responses in metastatic non-small cell lung cancer (NSCLC) patients treated on a phase 2 study of combined radiation therapy and ipilimumab: evidence for the in situ vaccination hypothesis of radiation. Int J Rad Oncol Biol Phys. 2015;93(3):S66–7.CrossRef
88.
go back to reference Shiao SL, Ruffell B, DeNardo DG, Faddegon BA, Park CC, Coussens LM. TH2-polarized CD4+ T cells and macrophages limit efficacy of radiotherapy. Cancer. 2015;3(5):518. Shiao SL, Ruffell B, DeNardo DG, Faddegon BA, Park CC, Coussens LM. TH2-polarized CD4+ T cells and macrophages limit efficacy of radiotherapy. Cancer. 2015;3(5):518.
89.
go back to reference Greenup R, Buchanan A, Lorizio W, Rhoads K, Chan S, Leedom T, King R, McLennan J, Crawford B, Marcom PK. Prevalence of BRCA mutations among women with triple-negative breast cancer (TNBC) in a genetic counseling cohort. Ann Surg Oncol. 2013;20(10):3254–8.PubMedCrossRef Greenup R, Buchanan A, Lorizio W, Rhoads K, Chan S, Leedom T, King R, McLennan J, Crawford B, Marcom PK. Prevalence of BRCA mutations among women with triple-negative breast cancer (TNBC) in a genetic counseling cohort. Ann Surg Oncol. 2013;20(10):3254–8.PubMedCrossRef
90.
go back to reference Brown SD, Warren RL, Gibb EA, Martin SD, Spinelli JJ, Nelson BH, Holt RA. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014;24(5):743–50.PubMedPubMedCentralCrossRef Brown SD, Warren RL, Gibb EA, Martin SD, Spinelli JJ, Nelson BH, Holt RA. Neo-antigens predicted by tumor genome meta-analysis correlate with increased patient survival. Genome Res. 2014;24(5):743–50.PubMedPubMedCentralCrossRef
91.
go back to reference Lu Y-C, Robbins PF. Cancer immunotherapy targeting neoantigens. In: Seminars in immunology: 2016: Elsevier; 2016. p. 22–7. Lu Y-C, Robbins PF. Cancer immunotherapy targeting neoantigens. In: Seminars in immunology: 2016: Elsevier; 2016. p. 22–7.
92.
go back to reference Helleday T, Bryant HE, Schultz N. Poly (ADP-ribose) polymerase (PARP-1) in homologous recombination and as a target for cancer therapy. Cell Cycle. 2005;4(9):1176–8.PubMedCrossRef Helleday T, Bryant HE, Schultz N. Poly (ADP-ribose) polymerase (PARP-1) in homologous recombination and as a target for cancer therapy. Cell Cycle. 2005;4(9):1176–8.PubMedCrossRef
94.
go back to reference Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, Scott C, Meier W, Shapira-Frommer R, Safra T. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med. 2012;366(15):1382–92.PubMedCrossRef Ledermann J, Harter P, Gourley C, Friedlander M, Vergote I, Rustin G, Scott C, Meier W, Shapira-Frommer R, Safra T. Olaparib maintenance therapy in platinum-sensitive relapsed ovarian cancer. N Engl J Med. 2012;366(15):1382–92.PubMedCrossRef
95.
go back to reference Jiang T, Shi W, Wali VB, Pongor LS, Li C, Lau R, Győrffy B, Lifton RP, Symmans WF, Pusztai L. Predictors of Chemosensitivity in triple negative breast Cancer: an integrated genomic analysis. PLoS Med. 2016;13(12):e1002193.PubMedPubMedCentralCrossRef Jiang T, Shi W, Wali VB, Pongor LS, Li C, Lau R, Győrffy B, Lifton RP, Symmans WF, Pusztai L. Predictors of Chemosensitivity in triple negative breast Cancer: an integrated genomic analysis. PLoS Med. 2016;13(12):e1002193.PubMedPubMedCentralCrossRef
97.
go back to reference Dhanasekaran R, Venkatesh SK, Torbenson MS, Roberts LR. Clinical implications of basic research in hepatocellular carcinoma. J Hepatol. 2016;64(3):736–45.PubMedCrossRef Dhanasekaran R, Venkatesh SK, Torbenson MS, Roberts LR. Clinical implications of basic research in hepatocellular carcinoma. J Hepatol. 2016;64(3):736–45.PubMedCrossRef
98.
go back to reference Kodumudi KN, Siegel J, Weber AM, Scott E, Sarnaik AA, Pilon-Thomas S. Immune checkpoint blockade to improve tumor infiltrating lymphocytes for adoptive cell therapy. PLoS One. 2016;11(4):e0153053.PubMedPubMedCentralCrossRef Kodumudi KN, Siegel J, Weber AM, Scott E, Sarnaik AA, Pilon-Thomas S. Immune checkpoint blockade to improve tumor infiltrating lymphocytes for adoptive cell therapy. PLoS One. 2016;11(4):e0153053.PubMedPubMedCentralCrossRef
100.
go back to reference Mittendorf EA, Philips AV, Meric-Bernstam F, Qiao N, Wu Y, Harrington S, Su X, Wang Y, Gonzalez-Angulo AM, Akcakanat A, et al. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res. 2014;2(4):361–70.PubMedPubMedCentralCrossRef Mittendorf EA, Philips AV, Meric-Bernstam F, Qiao N, Wu Y, Harrington S, Su X, Wang Y, Gonzalez-Angulo AM, Akcakanat A, et al. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res. 2014;2(4):361–70.PubMedPubMedCentralCrossRef
101.
go back to reference Vonderheide RH, LoRusso PM, Khalil M, Gartner EM, Khaira D, Soulieres D, Dorazio P, Trosko JA, Rüter J, Mariani GL. Tremelimumab in combination with exemestane in patients with advanced breast cancer and treatment-associated modulation of inducible costimulator expression on patient T cells. Clin Cancer Res. 2010;16(13):3485–94.PubMedCrossRef Vonderheide RH, LoRusso PM, Khalil M, Gartner EM, Khaira D, Soulieres D, Dorazio P, Trosko JA, Rüter J, Mariani GL. Tremelimumab in combination with exemestane in patients with advanced breast cancer and treatment-associated modulation of inducible costimulator expression on patient T cells. Clin Cancer Res. 2010;16(13):3485–94.PubMedCrossRef
102.
go back to reference Yu H, Yang J, Jiao S, Li Y, Zhang W, Wang J. Cytotoxic T lymphocyte antigen 4 expression in human breast cancer: implications for prognosis. Cancer Immunol Immunother. 2015;64(7):853–60.PubMedPubMedCentralCrossRef Yu H, Yang J, Jiao S, Li Y, Zhang W, Wang J. Cytotoxic T lymphocyte antigen 4 expression in human breast cancer: implications for prognosis. Cancer Immunol Immunother. 2015;64(7):853–60.PubMedPubMedCentralCrossRef
103.
go back to reference Sabel MS, Arora A, Su G, Chang AE. Adoptive immunotherapy of breast cancer with lymph node cells primed by cryoablation of the primary tumor. Cryobiology. 2006;53(3):360–6.PubMedCrossRef Sabel MS, Arora A, Su G, Chang AE. Adoptive immunotherapy of breast cancer with lymph node cells primed by cryoablation of the primary tumor. Cryobiology. 2006;53(3):360–6.PubMedCrossRef
104.
go back to reference Wang Z-X, Cao J-X, Wang M, Li D, Cui Y-X, Zhang X-Y, Liu J-L, Li J-L. Adoptive cellular immunotherapy for the treatment of patients with breast cancer: a meta-analysis. Cytotherapy. 2014;16(7):934–45.PubMedCrossRef Wang Z-X, Cao J-X, Wang M, Li D, Cui Y-X, Zhang X-Y, Liu J-L, Li J-L. Adoptive cellular immunotherapy for the treatment of patients with breast cancer: a meta-analysis. Cytotherapy. 2014;16(7):934–45.PubMedCrossRef
105.
go back to reference Wang K, Xu J, Zhang T, Xue D. Tumor-infiltrating lymphocytes in breast cancer predict the response to chemotherapy and survival outcome: a meta-analysis. Oncotarget. 2016;7(28):44288.PubMedPubMedCentral Wang K, Xu J, Zhang T, Xue D. Tumor-infiltrating lymphocytes in breast cancer predict the response to chemotherapy and survival outcome: a meta-analysis. Oncotarget. 2016;7(28):44288.PubMedPubMedCentral
106.
go back to reference Karyampudi L, Lamichhane P, Scheid AD, Kalli KR, Shreeder B, Krempski JW, Behrens MD, Knutson KL. Accumulation of memory precursor CD8 T cells in regressing tumors following combination therapy with vaccine and anti-PD-1 antibody. Cancer Res. 2014;74(11):2974–85.PubMedPubMedCentralCrossRef Karyampudi L, Lamichhane P, Scheid AD, Kalli KR, Shreeder B, Krempski JW, Behrens MD, Knutson KL. Accumulation of memory precursor CD8 T cells in regressing tumors following combination therapy with vaccine and anti-PD-1 antibody. Cancer Res. 2014;74(11):2974–85.PubMedPubMedCentralCrossRef
107.
go back to reference Jaini R, Rayman P, Cohen PA, Finke JH, Tuohy VK. Combination of sunitinib with anti-tumor vaccination inhibits T cell priming and requires careful scheduling to achieve productive immunotherapy. Int J Cancer. 2014;134(7):1695–705.PubMedCrossRef Jaini R, Rayman P, Cohen PA, Finke JH, Tuohy VK. Combination of sunitinib with anti-tumor vaccination inhibits T cell priming and requires careful scheduling to achieve productive immunotherapy. Int J Cancer. 2014;134(7):1695–705.PubMedCrossRef
Metadata
Title
Mechanisms of immune evasion in breast cancer
Authors
Joshua P. Bates
Roshanak Derakhshandeh
Laundette Jones
Tonya J. Webb
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2018
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-018-4441-3

Other articles of this Issue 1/2018

BMC Cancer 1/2018 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine