The Tumor Immune Microenvironment in Breast Cancer Progression
DOI:
https://doi.org/10.2340/1651-226X.2024.33008Keywords:
Breast cancer, tumor immune microenvironment, subtypes, progressionAbstract
Background: The tumor microenvironment significantly influences breast cancer development, progression, and metastasis. Various immune cell populations, including T cells, B cells, NK cells, and myeloid cells exhibit diverse functions in different breast cancer subtypes, contributing to both anti-tumor and pro-tumor activities.
Purpose: This review provides an overview of the predominant immune cell populations in breast cancer subtypes, elucidating their suppressive and prognostic effects. We aim to outline the role of the immune microenvironment from normal breast tissue to invasive cancer and distant metastasis.
Methods: A comprehensive literature review was conducted to analyze the involvement of immune cells throughout breast cancer progression.
Results: In breast cancer, tumors exhibit increased immune cell infiltration compared to normal tissue. Variations exist across subtypes, with higher levels observed in triple-negative and HER2+ tumors are linked to better survival. In contrast, ER+ tumors display lower immune infiltration, associated with poorer outcomes. Furthermore, metastatic sites commonly exhibit a more immunosuppressive microenvironment.
Conclusion: Understanding the complex interaction between tumor and immune cells during breast cancer progression is essential for future research and the development of immune-based strategies. This comprehensive understanding may pave the way for more effective treatment approaches and improved patients outcomes.
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References
Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Ann Rev Immunol. 2004;22:329–60.
https://doi.org/10.1146/annurev.immunol.22.012703.104803 DOI: https://doi.org/10.1146/annurev.immunol.22.012703.104803
Goff SL, Danforth DN. The role of immune cells in breast tissue and immunotherapy for the treatment of breast cancer. Clin Breast Cancer. 2021;21(1):e63–73.
https://doi.org/10.1016/j.clbc.2020.06.011 DOI: https://doi.org/10.1016/j.clbc.2020.06.011
Ogony J, Hoskin TL, Stallings-Mann M, et al. Immune cells are increased in normal breast tissues of BRCA1/2 mutation carriers. Breast Cancer Res Treat. 2023;197(2):277–85.
https://doi.org/10.1007/s10549-022-06786-y DOI: https://doi.org/10.1007/s10549-022-06786-y
Degnim AC, Brahmbhatt RD, Radisky DC, et al. Immune cell quantitation in normal breast tissue lobules with and without lobulitis. Breast Cancer Res Treat. 2014;144(3):539–49.
https://doi.org/10.1007/s10549-014-2896-8 DOI: https://doi.org/10.1007/s10549-014-2896-8
Ferguson DJ. Intraepithelial lymphocytes and macrophages in the normal breast. Virchows Arch A Pathol Anat Histopathol. 1985;407(4):369–78.
https://doi.org/10.1007/BF00709984 DOI: https://doi.org/10.1007/BF00709984
Azizi E, Carr AJ, Plitas G, et al. Single-cell map of diverse immune phenotypes in the breast tumor microenvironment. Cell. 2018;174(5):1293–308.e36.
https://doi.org/10.1016/j.cell.2018.05.060 DOI: https://doi.org/10.1016/j.cell.2018.05.060
Kumar T, Nee K, Wei R, et al. A spatially resolved single-cell genomic atlas of the adult human breast. Nature. 2023;620(7972):181–91.
https://doi.org/10.1038/s41586-023-06252-9 DOI: https://doi.org/10.1038/s41586-023-06252-9
Oertelt-Prigione S. Immunology and the menstrual cycle. Autoimmunity Rev. 2012;11(6):A486–92.
https://doi.org/10.1016/j.autrev.2011.11.023 DOI: https://doi.org/10.1016/j.autrev.2011.11.023
Zirbes A, Joseph J, Lopez JC, et al. Changes in immune cell types with age in breast are consistent with a decline in immune surveillance and increased immunosuppression. J Mammary Gland Biol Neoplasia. 2021;26(3):247–61.
https://doi.org/10.1007/s10911-021-09495-2 DOI: https://doi.org/10.1007/s10911-021-09495-2
Ménard S, Tomasic G, Casalini P, et al. Lymphoid infiltration as a prognostic variable for early-onset breast carcinomas. Clin Cancer Res. 1997;3(5):817–9.
Loi S, Sirtaine N, Piette 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. JCO. 2013;31(7):860–7.
https://doi.org/10.1200/JCO.2011.41.0902 DOI: https://doi.org/10.1200/JCO.2011.41.0902
Mahmoud SMA, Paish EC, Powe DG, et al. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. JCO. 2011;29(15):1949–55.
https://doi.org/10.1200/JCO.2010.30.5037 DOI: https://doi.org/10.1200/JCO.2010.30.5037
Denkert C, Von Minckwitz G, Darb-Esfahani S, et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 2018;19(1):40–50.
https://doi.org/10.1016/S1470-2045(17)30904-X DOI: https://doi.org/10.1016/S1470-2045(17)30904-X
Buisseret L, Garaud S, de Wind A, et al. Tumor-infiltrating lymphocyte composition, organization and PD-1/ PD-L1 expression are linked in breast cancer. OncoImmunology. 2017;6(1):e1257452.
https://doi.org/10.1080/2162402X.2016.1257452 DOI: https://doi.org/10.1080/2162402X.2016.1257452
Zhang Q, Wu S. Tertiary lymphoid structures are critical for cancer prognosis and therapeutic response. Front Immunol [Internet]. 2023 [cited 01-12-2023];13. Available from: https://www.frontiersin.org/articles/10.3389/fimmu.2022.1063711 DOI: https://doi.org/10.3389/fimmu.2022.1063711
Garaud S, Buisseret L, Solinas C, et al. Tumor-infiltrating B cells signal functional humoral immune responses in breast cancer. JCI Insight [Internet]. 2019 [cited 10-11-2021];4(18). Available from: https://insight.jci.org/articles/view/129641 DOI: https://doi.org/10.1172/jci.insight.129641
Harris RJ, Cheung A, Ng JCF, et al. Tumor-infiltrating B lymphocyte profiling identifies IgG-biased, clonally expanded prognostic phenotypes in triple-negative breast cancer. Cancer Res. 2021;81(16):4290–304.
https://doi.org/10.1158/0008-5472.CAN-20-3773 DOI: https://doi.org/10.1158/0008-5472.CAN-20-3773
Khaja ASS, Toor SM, El Salhat H, et al. Preferential accumulation of regulatory T cells with highly immunosuppressive characteristics in breast tumor microenvironment. Oncotarget. 2017;8(20):33159–71.
https://doi.org/10.18632/oncotarget.16565 DOI: https://doi.org/10.18632/oncotarget.16565
Saleh R, Elkord E. FoxP3+ T regulatory cells in cancer: prognostic biomarkers and therapeutic targets. Cancer Lett. 2020;490:174–85.
https://doi.org/10.1016/j.canlet.2020.07.022 DOI: https://doi.org/10.1016/j.canlet.2020.07.022
Toffoli EC, Sheikhi A, Höppner YD, et al. Natural killer cells and anti-cancer therapies: reciprocal effects on immune function and therapeutic response. Cancers (Basel). 2021;13(4):711.
https://doi.org/10.3390/cancers13040711 DOI: https://doi.org/10.3390/cancers13040711
Campbell KS, Hasegawa J. Natural killer cell biology: an update and future directions. J Allergy Clin Immunol. 2013;132(3):536–44.
https://doi.org/10.1016/j.jaci.2013.07.006 DOI: https://doi.org/10.1016/j.jaci.2013.07.006
Albrecht AE, Hartmann BW, Scholten C, Huber JC, Kalinowska W, Zielinski CC. Effect of estrogen replacement therapy on natural killer cell activity in postmenopausal women. Maturitas. 1996;25(3).
https://doi.org/10.1016/S0378-5122(96)01063-8 DOI: https://doi.org/10.1016/S0378-5122(96)01063-8
Scanlan JM, Werner JJ, Legg RL, Laudenslager ML. Natural killer cell activity is reduced in association with oral contraceptive use. Psychoneuroendocrinology. 1995;20(3):281–7.
https://doi.org/10.1016/0306-4530(94)00059-J DOI: https://doi.org/10.1016/0306-4530(94)00059-J
Bouzidi L, Triki H, Charfi S, et al. Prognostic value of natural killer cells besides tumor-infiltrating lymphocytes in breast cancer tissues. Clin Breast Cancer. 2021;21(6):e738–47.
https://doi.org/10.1016/j.clbc.2021.02.003 DOI: https://doi.org/10.1016/j.clbc.2021.02.003
Loi S, Michiels S, Salgado R, 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. Ann Oncol. 2014;25(8):1544–50.
https://doi.org/10.1093/annonc/mdu112 DOI: https://doi.org/10.1093/annonc/mdu112
Hu Q, Hong Y, Qi P, et al. Atlas of breast cancer infiltrated B-lymphocytes revealed by paired single-cell RNA-sequencing and antigen receptor profiling. Nat Commun. 2021;12(1):2186.
https://doi.org/10.1038/s41467-021-22300-2 DOI: https://doi.org/10.1038/s41467-021-22300-2
Takenaka M, Seki N, Toh U, et al. FOXP3 expression in tumor cells and tumor-infiltrating lymphocytes is associated with breast cancer prognosis. Mol Clin Oncol. 2013;1(4):625–32.
https://doi.org/10.3892/mco.2013.107 DOI: https://doi.org/10.3892/mco.2013.107
Glajcar A, Szpor J, Hodorowicz-Zaniewska D, Tyrak KE, Okoń K. The composition of T cell infiltrates varies in primary invasive breast cancer of different molecular subtypes as well as according to tumor size and nodal status. Virchows Arch. 2019;475(1):13–23.
https://doi.org/10.1007/s00428-019-02568-y DOI: https://doi.org/10.1007/s00428-019-02568-y
Ono M, Tsuda H, Shimizu C, et al. Tumor-infiltrating lymphocytes are correlated with response to neoadjuvant chemotherapy in triple-negative breast cancer. Breast Cancer Res Treat. 2012;132(3):793–805.
https://doi.org/10.1007/s10549-011-1554-7 DOI: https://doi.org/10.1007/s10549-011-1554-7
Liu F, Lang R, Zhao J, et al. CD8+ cytotoxic T cell and FOXP3+ regulatory T cell infiltration in relation to breast cancer survival and molecular subtypes. Breast Cancer Res Treat. 2011;130(2):645–55.
https://doi.org/10.1007/s10549-011-1647-3 DOI: https://doi.org/10.1007/s10549-011-1647-3
Ali HR, Provenzano E, Dawson SJ, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12 439 patients. Ann Oncol. 2014;25(8):1536–43.
https://doi.org/10.1093/annonc/mdu191 DOI: https://doi.org/10.1093/annonc/mdu191
Salemme V, Centonze G, Cavallo F, Defilippi P, Conti L. The crosstalk between tumor cells and the immune microenvironment in breast cancer: implications for immunotherapy. Front Oncol. 2021;11:289.
https://doi.org/10.3389/fonc.2021.610303 DOI: https://doi.org/10.3389/fonc.2021.610303
Levi I, Amsalem H, Nissan A, et al. Characterization of tumor infiltrating natural killer cell subset. Oncotarget. 2015;6(15):13835–43.
https://doi.org/10.18632/oncotarget.3453 DOI: https://doi.org/10.18632/oncotarget.3453
Lapeyre-Prost A, Terme M, Pernot S, et al. Chapter seven – immunomodulatory activity of VEGF in cancer. In: Galluzzi L, editor. International review of cell and molecular biology [Internet]. Academic Press; 2017 [cited 14-11-2021]. p. 295–342. Available from: https://www.sciencedirect.com/science/article/pii/S1937644816301022 DOI: https://doi.org/10.1016/bs.ircmb.2016.09.007
Kiaei SZF, Nouralishahi A, Ghasemirad M, et al. Advances in natural killer cell therapies for breast cancer. Immunol Cell Biol [Internet]. [cited 21-08-2023];n/a(n/a). Available from: https://onlinelibrary.wiley.com/doi/abs/10.1111/imcb.12658
Fernandez-Martinez A, Pascual T, Singh B, et al. Prognostic and predictive value of immune-related gene expression signatures vs tumor-infiltrating lymphocytes in early-stage ERBB2/HER2-positive breast cancer: a correlative analysis of the CALGB 40601 and PAMELA trials. JAMA Oncol. 2023;9(4):490–9.
https://doi.org/10.1001/jamaoncol.2022.6288 DOI: https://doi.org/10.1001/jamaoncol.2022.6288
Wculek SK, Cueto FJ, Mujal AM, Melero I, Krummel MF, Sancho D. Dendritic cells in cancer immunology and immunotherapy. Nat Rev Immunol. 2020;20(1):7–24.
https://doi.org/10.1038/s41577-019-0210-z DOI: https://doi.org/10.1038/s41577-019-0210-z
Greene TT, Jo Y, Zuniga EI. Infection and cancer suppress pDC derived IFN-I. Curr Opin Immunol. 2020;66:114–22.
https://doi.org/10.1016/j.coi.2020.08.001 DOI: https://doi.org/10.1016/j.coi.2020.08.001
Paek SH, Kim HG, Lee JW, et al. Circulating plasmacytoid and myeloid dendritic cells in breast cancer patients: a pilot study. J Breast Cancer. 2019;22(1):29–37.
https://doi.org/10.4048/jbc.2019.22.e15 DOI: https://doi.org/10.4048/jbc.2019.22.e15
Kini Bailur J, Gueckel B, Pawelec G. Prognostic impact of high levels of circulating plasmacytoid dendritic cells in breast cancer. J Transl Med. 2016;14(1):151.
https://doi.org/10.1186/s12967-016-0905-x DOI: https://doi.org/10.1186/s12967-016-0905-x
Treilleux I, Blay JY, Bendriss-Vermare N, et al. Dendritic cell infiltration and prognosis of early stage breast cancer. Clin Cancer Res. 2004;10(22):7466–74.
https://doi.org/10.1158/1078-0432.CCR-04-0684 DOI: https://doi.org/10.1158/1078-0432.CCR-04-0684
Szpor J, Streb J, Glajcar A, et al. Dendritic cells are associated with prognosis and survival in breast cancer. Diagnostics (Basel). 2021;11(4):702.
https://doi.org/10.3390/diagnostics11040702 DOI: https://doi.org/10.3390/diagnostics11040702
Ma Y, Shurin GV, Peiyuan Z, Shurin MR. Dendritic cells in the cancer microenvironment. J Cancer. 2013;4(1):36–44.
https://doi.org/10.7150/jca.5046 DOI: https://doi.org/10.7150/jca.5046
Wilson BE, Gorrini C, Cescon DW. Breast cancer immune microenvironment: from pre-clinical models to clinical therapies. Breast Cancer Res Treat. 2021;191:257–267.
https://doi.org/10.1007/s10549-021-06431-0 DOI: https://doi.org/10.1007/s10549-021-06431-0
Markowitz J, Wesolowski R, Papenfuss T, Brooks TR, Carson WE. Myeloid-derived suppressor cells in breast cancer. Breast Cancer Res Treat. 2013;140(1):13–21.
https://doi.org/10.1007/s10549-013-2618-7 DOI: https://doi.org/10.1007/s10549-013-2618-7
Wang PF, Song SY, Wang TJ, et al. Prognostic role of pretreatment circulating MDSCs in patients with solid malignancies: a meta-analysis of 40 studies. OncoImmunology. 2018;7(10):e1494113.
https://doi.org/10.1080/2162402X.2018.1494113 DOI: https://doi.org/10.1080/2162402X.2018.1494113
Kumar S, Wilkes DW, Samuel N, et al. ΔNp63-driven recruitment of myeloid-derived suppressor cells promotes metastasis in triple-negative breast cancer. J Clin Invest. 2018;128(11):5095–109.
https://doi.org/10.1172/JCI99673 DOI: https://doi.org/10.1172/JCI99673
Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin–cyclophosphamide chemotherapy. Cancer Immunol Immunother. 2009;58(1):49–59.
https://doi.org/10.1007/s00262-008-0523-4 DOI: https://doi.org/10.1007/s00262-008-0523-4
Bingle L, Brown NJ, Lewis CE. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J Pathol. 2002;196(3):254–65.
https://doi.org/10.1002/path.1027 DOI: https://doi.org/10.1002/path.1027
Mahmoud SMA, Lee AHS, Paish EC, Macmillan RD, Ellis IO, Green AR. Tumour-infiltrating macrophages and clinical outcome in breast cancer. J Clin Pathol. 2012;65(2):159–63.
https://doi.org/10.1136/jclinpath-2011-200355 DOI: https://doi.org/10.1136/jclinpath-2011-200355
Zhang Y, Cheng S, Zhang M, et al. High-infiltration of tumor-associated macrophages predicts unfavorable clinical outcome for node-negative breast cancer. PLoS One. 2013;8(9):e76147.
https://doi.org/10.1371/journal.pone.0076147 DOI: https://doi.org/10.1371/journal.pone.0076147
Tiainen S, Tumelius R, Rilla K, et al. High numbers of macrophages, especially M2-like (CD163-positive), correlate with hyaluronan accumulation and poor outcome in breast cancer. Histopathology. 2015;66(6):873–83.
https://doi.org/10.1111/his.12607 DOI: https://doi.org/10.1111/his.12607
Cox TR, Gartland A, Erler JT. The pre-metastatic niche: is metastasis random? Bonekey Rep. 2012;1:80.
https://doi.org/10.1038/bonekey.2012.80 DOI: https://doi.org/10.1038/bonekey.2012.80
Paget S. The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev. 1989;8(2):98–101.
Liu Y, Cao X. Characteristics and significance of the pre-metastatic niche. Cancer Cell. 2016;30(5):668–81.
https://doi.org/10.1016/j.ccell.2016.09.011 DOI: https://doi.org/10.1016/j.ccell.2016.09.011
Liao N, Li C, Cao L, et al. Single-cell profile of tumor and immune cells in primary breast cancer, sentinel lymph node, and metastatic lymph node. Breast Cancer. 2023;30(1):77–87.
https://doi.org/10.1007/s12282-022-01400-x DOI: https://doi.org/10.1007/s12282-022-01400-x
Moshina N, Sebuødegård S, Lee CI, et al. Automated volumetric analysis of mammographic density in a screening setting: worse outcomes for women with dense breasts. Radiology. 2018;288(2):343–52.
https://doi.org/10.1148/radiol.2018172972 DOI: https://doi.org/10.1148/radiol.2018172972
Rye IH, Huse K, Josefsson SE, et al. Breast cancer metastasis: immune profiling of lymph nodes reveals exhaustion of effector T cells and immunosuppression. Mol Oncol. 2022;16(1):88–103.
https://doi.org/10.1002/1878-0261.13047 DOI: https://doi.org/10.1002/1878-0261.13047
Kohrt HE, Nouri N, Nowels K, Johnson D, Holmes S, Lee PP. Profile of immune cells in axillary lymph nodes predicts disease-free survival in breast cancer. PLoS Med. 2005;2(9):e284.
https://doi.org/10.1371/journal.pmed.0020284 DOI: https://doi.org/10.1371/journal.pmed.0020284
Núñez NG, Tosello Boari J, Ramos RN, et al. Tumor invasion in draining lymph nodes is associated with Treg accumulation in breast cancer patients. Nat Commun. 2020;11:3272.
https://doi.org/10.1038/s41467-020-17046-2 DOI: https://doi.org/10.1038/s41467-020-17046-2
van Pul KM, Vuylsteke RJCLM, van de Ven R, et al. Selectively hampered activation of lymph node-resident dendritic cells precedes profound T cell suppression and metastatic spread in the breast cancer sentinel lymph node. J Immunother Cancer. 2019;7:133.
https://doi.org/10.1186/s40425-019-0605-1 DOI: https://doi.org/10.1186/s40425-019-0605-1
Mansfield AS, Heikkila P, von Smitten K, Vakkila J, Leidenius M. The presence of sinusoidal CD163+ macrophages in lymph nodes is associated with favorable nodal status in patients with breast cancer. Virchows Arch. 2012;461(6):639–46.
https://doi.org/10.1007/s00428-012-1338-4 DOI: https://doi.org/10.1007/s00428-012-1338-4
DeSantis CE, Ma J, Gaudet MM, et al. Breast cancer statistics, 2019. CA: A Cancer J Clin. 2019;69(6):438–51.
https://doi.org/10.3322/caac.21583 DOI: https://doi.org/10.3322/caac.21583
van Uden DJP, van Maaren MC, Strobbe LJA, et al. Metastatic behavior and overall survival according to breast cancer subtypes in stage IV inflammatory breast cancer. Breast Cancer Res. 2019;21(1):113.
https://doi.org/10.1186/s13058-019-1201-5 DOI: https://doi.org/10.1186/s13058-019-1201-5
Manders K, van de Poll-Franse LV, Creemers GJ, et al. Clinical management of women with metastatic breast cancer: a descriptive study according to age group. BMC Cancer. 2006;6:179.
https://doi.org/10.1186/1471-2407-6-179 DOI: https://doi.org/10.1186/1471-2407-6-179
Molnár IA, Molnár BÁ, Vízkeleti L, et al. Breast carcinoma subtypes show different patterns of metastatic behavior. Virchows Arch. 2017;470(3):275–83.
https://doi.org/10.1007/s00428-017-2065-7 DOI: https://doi.org/10.1007/s00428-017-2065-7
Gerratana L, Fanotto V, Bonotto M, et al. Pattern of metastasis and outcome in patients with breast cancer. Clin Exp Metastasis. 2015;32(2):125–33.
https://doi.org/10.1007/s10585-015-9697-2 DOI: https://doi.org/10.1007/s10585-015-9697-2
Dieci MV, Tsvetkova V, Orvieto E, et al. Immune characterization of breast cancer metastases: prognostic implications. Breast Cancer Res. 2018;20:62.
https://doi.org/10.1186/s13058-018-1003-1 DOI: https://doi.org/10.1186/s13058-018-1003-1
Suva LJ, Washam C, Nicholas RW, Griffin RJ. Bone metastasis: mechanisms and therapeutic opportunities. Nat Rev Endocrinol. 2011;7(4):208–18.
https://doi.org/10.1038/nrendo.2010.227 DOI: https://doi.org/10.1038/nrendo.2010.227
Tivari S, Lu H, Dasgupta T, De Lorenzo MS, Wieder R. Reawakening of dormant estrogen-dependent human breast cancer cells by bone marrow stroma secretory senescence. Cell Commun Signa. 2018;16(1):48.
https://doi.org/10.1186/s12964-018-0259-5 DOI: https://doi.org/10.1186/s12964-018-0259-5
Walker ND, Patel J, Munoz JL, et al. The bone marrow niche in support of breast cancer dormancy. Cancer Lett. 2016;380(1):263–71.
https://doi.org/10.1016/j.canlet.2015.10.033 DOI: https://doi.org/10.1016/j.canlet.2015.10.033
Lee H, Na KJ, Choi H. Differences in tumor immune microenvironment in metastatic sites of breast cancer. Front Oncol. 2021;11:722.
https://doi.org/10.3389/fonc.2021.649004 DOI: https://doi.org/10.3389/fonc.2021.649004
Terceiro LEL, Edechi CA, Ikeogu NM, et al. The breast tumor microenvironment: a key player in metastatic spread. Cancers. 2021;13(19):4798.
https://doi.org/10.3390/cancers13194798 DOI: https://doi.org/10.3390/cancers13194798
Kersten K, Coffelt SB, Hoogstraat M, et al. Mammary tumor-derived CCL2 enhances pro-metastatic systemic inflammation through upregulation of IL1β in tumor-associated macrophages. OncoImmunology. 2017;6(8):e1334744.
https://doi.org/10.1080/2162402X.2017.1334744 DOI: https://doi.org/10.1080/2162402X.2017.1334744
Yan CY, Zhao ML, Wei YN, Zhao XH. Mechanisms of drug resistance in breast cancer liver metastases: dilemmas and opportunities. Mol Ther – Oncolytics. 2023;28:212–29.
https://doi.org/10.1016/j.omto.2023.02.001 DOI: https://doi.org/10.1016/j.omto.2023.02.001
Tsilimigras DI, Brodt P, Clavien PA, et al. Liver metastases. Nat Rev Dis Primers. 2021;7(1):1–23.
https://doi.org/10.1038/s41572-021-00261-6 DOI: https://doi.org/10.1038/s41572-021-00261-6
Heitz F, Harter P, Lueck HJ, et al. Triple-negative and HER2-overexpressing breast cancers exhibit an elevated risk and an earlier occurrence of cerebral metastases. Eur J Cancer. 2009;45(16):2792–8.
https://doi.org/10.1016/j.ejca.2009.06.027 DOI: https://doi.org/10.1016/j.ejca.2009.06.027
Aversa C, Rossi V, Geuna E, et al. Metastatic breast cancer subtypes and central nervous system metastases. Breast. 2014;23(5):623–8.
https://doi.org/10.1016/j.breast.2014.06.009 DOI: https://doi.org/10.1016/j.breast.2014.06.009
Kim YJ, Kim JS, Kim IA. Molecular subtype predicts incidence and prognosis of brain metastasis from breast cancer in SEER database. J Cancer Res Clin Oncol. 2018;144(9):1803–16.
https://doi.org/10.1007/s00432-018-2697-2 DOI: https://doi.org/10.1007/s00432-018-2697-2
Kennecke H, Yerushalmi R, Woods R, et al. Metastatic behavior of breast cancer subtypes. JCO. 2010;28(20):3271–7.
https://doi.org/10.1200/JCO.2009.25.9820 DOI: https://doi.org/10.1200/JCO.2009.25.9820
Lu W, Xie H, Yuan C, Li J, Li Z, Wu A. Genomic landscape of the immune microenvironments of brain metastases in breast cancer. J Transl Med. 2020;18(1):327.
https://doi.org/10.1186/s12967-020-02503-9 DOI: https://doi.org/10.1186/s12967-020-02503-9
Berghoff AS, Lassmann H, Preusser M, Höftberger R. Characterization of the inflammatory response to solid cancer metastases in the human brain. Clin Exp Metastasis. 2013;30(1):69–81.
https://doi.org/10.1007/s10585-012-9510-4 DOI: https://doi.org/10.1007/s10585-012-9510-4
Noh MG, Kim SS, Kim YJ, et al. Evolution of the tumor microenvironment toward immune-suppressive seclusion during brain metastasis of breast cancer: implications for targeted therapy. Cancers. 2021;13(19):4895.
https://doi.org/10.3390/cancers13194895 DOI: https://doi.org/10.3390/cancers13194895
Debien V, De Caluwé A, Wang X, et al. Immunotherapy in breast cancer: an overview of current strategies and perspectives. npj Breast Cancer. 2023;9(1):1–10.
https://doi.org/10.1038/s41523-023-00508-3 DOI: https://doi.org/10.1038/s41523-023-00508-3
Gaynor N, Crown J, Collins DM. Immune checkpoint inhibitors: key trials and an emerging role in breast cancer. Semin Cancer Biol [Internet]. 2020 [cited 24-11-2021]. Available from: https://www.sciencedirect.com/science/article/pii/S1044579X20301528
Cortes J, Cescon DW, Rugo HS, et al. Pembrolizumab plus chemotherapy versus placebo plus chemotherapy for previously untreated locally recurrent inoperable or metastatic triple-negative breast cancer (KEYNOTE-355): a randomised, placebo-controlled, double-blind, phase 3 clinical trial. Lancet. 2020;396(10265):1817–28. DOI: https://doi.org/10.1016/S0140-6736(20)32531-9
Schmid P, Cortes J, Pusztai L, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020;382(9):810–21.
https://doi.org/10.1056/NEJMoa1910549 DOI: https://doi.org/10.1056/NEJMoa1910549
Schmid P, Adams S, Rugo HS, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379(22):2108–21.
https://doi.org/10.1056/NEJMoa1809615 DOI: https://doi.org/10.1056/NEJMoa1809615
Røssevold AH, Andresen NK, Bjerre CA, et al. Atezolizumab plus anthracycline-based chemotherapy in metastatic triple-negative breast cancer: the randomized, double-blind phase 2b ALICE trial. Nat Med. 2022;28(12):2573–83.
https://doi.org/10.1038/s41591-022-02126-1 DOI: https://doi.org/10.1038/s41591-022-02126-1
Merck.com [Internet]. European Commission Approves KEYTRUDA® (pembrolizumab) Plus Chemotherapy as Neoadjuvant Treatment, Then Continued as Adjuvant Monotherapy After Surgery for Locally Advanced or Early-Stage Triple-Negative Breast Cancer at High Risk of Recurrence. [cited 28-11-2023]. Available from: https://www.merck.com/news/european-commission-approves-keytruda-pembrolizumab-plus-chemotherapy-as-neoadjuvant-treatment-then-continued-as-adjuvant-monotherapy-after-surgery-for-locally-advanced-or-early-stage-triple/
Merck.com [Internet]. Merck’s KEYTRUDA® (pembrolizumab) Receives Four New Approvals in Japan, Including in High-Risk Early-Stage Triple-Negative Breast Cancer (TNBC). [cited 28-11-2023]. Available from: https://www.merck.com/news/mercks-keytruda-pembrolizumab-receives-four-new-approvals-in-japan-including-in-high-risk-early-stage-triple-negative-breast-cancer-tnbc/
Merck.com [Internet]. FDA approves KEYTRUDA® (pembrolizumab) for treatment of patients with high-risk early-stage triple-negative breast cancer in combination with chemotherapy as neoadjuvant treatment, then continued as single agent as adjuvant treatment after surgery. [cited 28-11-2023]. Available from: https://www.merck.com/news/fda-approves-keytruda-pembrolizumab-for-treatment-of-patients-with-high-risk-early-stage-triple-negative-breast-cancer-in-combination-with-chemotherapy-as-neoadjuvant-treatment-then-continued/
Blomberg OS, Kos K, Spagnuolo L, et al. Neoadjuvant immune checkpoint blockade triggers persistent and systemic Treg activation which blunts therapeutic efficacy against metastatic spread of breast tumors. Oncoimmunology. 2023;12(1):2201147.
https://doi.org/10.1080/2162402X.2023.2201147 DOI: https://doi.org/10.1080/2162402X.2023.2201147
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