Review
. 2016 Oct; 4:59.
doi: 10.1186/s40425-016-0165-6.

Clinical significance of tumor-infiltrating lymphocytes in breast cancer

Sasha E Stanton 1 Mary L Disis 1 
Affiliations
  • PMID: 27777769
  •     53 References
  •     121 citations

Abstract

Tumor infiltrating lymphocytes (TIL) play an essential role in mediating response to chemotherapy and improving clinical outcomes in all subtypes of breast cancer. Triple negative breast cancers (TN) are most likely to have tumors with >50 % lymphocytic infiltrate, termed lymphocyte predominant breast cancer, and derive the greatest survival benefit from each 10 % increase in TIL. The majority of HER2+ breast cancers have similar level of immune infiltrate as TN breast cancer yet the presence of TILs has not shown the same survival benefit. For HER2+ breast cancers, type 1 T-cells, either increased TBET+ tumor infiltration or increased type 1 HER2-specific CD4+ T-cells in the peripheral blood, are associated with better outcomes. Hormone receptor positive HER2 negative tumors tend to have the least immune infiltrate yet are the only breast cancer subtype to show worse prognosis with increased FOXP3 regulatory T-cell infiltrate. Notably, all breast cancer subtypes have tumors with low, intermediate, or high TIL infiltrate. Tumors with high TILs may also have increased PD-L1 expression which might be the reason that TN breast cancer seems to demonstrate the most robust clinical response to immune checkpoint inhibitor therapy but further investigation is needed. Tumors with intermediate or low levels of pre-treatment immune infiltrate, on the other hand, may benefit from an intervention that may increase TIL, particularly type 1 T-cells. Examples of these interventions include specific types of cytotoxic chemotherapy, radiation, or vaccine therapy. Therefore, the systematic evaluation of TIL and specific populations of TIL may be able to both guide prognosis and the appropriate sequencing of therapies in breast cancer.

Keywords: Breast cancer; CD8 T-cell; FOXP3; Tumor infiltrating lymphocytes.

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Haoyu Ren, Daixing Hu, Yu Mao, Xinliang Su.
Med Sci Monit, 2020 Apr 07; 26. PMID: 32251269    Free PMC article.
The resveratrol analogue, HS‑1793, enhances the effects of radiation therapy through the induction of anti‑tumor immunity in mammary tumor growth.
Joong Sun Kim, Soo Kyung Jeong, +4 authors, Min Ho Jeong.
Int J Oncol, 2020 Apr 03; 56(6). PMID: 32236622    Free PMC article.
MiR-18a and miR-18b are expressed in the stroma of oestrogen receptor alpha negative breast cancers.
Nina Gran Egeland, Kristin Jonsdottir, +7 authors, Emiel A M Janssen.
BMC Cancer, 2020 May 07; 20(1). PMID: 32370743    Free PMC article.
Correlations between tumor-infiltrating and circulating lymphocyte subpopulations in advanced renal cancer patients treated with nivolumab.
Melissa Bersanelli, Letizia Gnetti, +12 authors, Sebastiano Buti.
Acta Biomed, 2020 Jan 08; 90(4). PMID: 31910171    Free PMC article.
γδ T cells are the predominant T cell type in opossum mammaries during lactation.
Bethaney D Fehrenkamp, Robert D Miller.
Dev Comp Immunol, 2019 Feb 16; 95. PMID: 30768943    Free PMC article.
Prognostic and Clinicopathological Correlations of Cell Cycle Marker Expressions before and after the Primary Systemic Therapy of Breast Cancer.
Tímea Tőkés, Anna-Mária Tőkés, +6 authors, Magdolna Dank.
Pathol Oncol Res, 2019 Aug 26; 26(3). PMID: 31446607    Free PMC article.
The Effects of Obesity on Anti-Cancer Immunity and Cancer Immunotherapy.
Matthew J Woodall, Silke Neumann, +2 authors, Sarah L Young.
Cancers (Basel), 2020 May 20; 12(5). PMID: 32422865    Free PMC article.
Review.
Modeling of the immune response in the pathogenesis of solid tumors and its prognostic significance.
Łukasz Zadka, Damian J Grybowski, Piotr Dzięgiel.
Cell Oncol (Dordr), 2020 Jun 04; 43(4). PMID: 32488850    Free PMC article.
Review.
Blockade of PD-1, PD-L1, and TIM-3 Altered Distinct Immune- and Cancer-Related Signaling Pathways in the Transcriptome of Human Breast Cancer Explants.
Reem Saleh, Salman M Toor, +2 authors, Eyad Elkord.
Genes (Basel), 2020 Jul 04; 11(6). PMID: 32616706    Free PMC article.
Erythrocyte membrane fatty acids and breast cancer risk by tumor tissue expression of immuno-inflammatory markers and fatty acid synthase: a nested case-control study.
Emma E McGee, Claire H Kim, +10 authors, A Heather Eliassen.
Breast Cancer Res, 2020 Jul 24; 22(1). PMID: 32698885    Free PMC article.
Esophageal Microenvironment: From Precursor Microenvironment to Premetastatic Niche.
Peng Han, Peng Cao, +4 authors, Fan Li.
Cancer Manag Res, 2020 Aug 09; 12. PMID: 32765088    Free PMC article.
Review.
Computational Identification of Tumor Suppressor Genes Based on Gene Expression Profiles in Normal and Cancerous Gastrointestinal Tissues.
Qingrong Sun, Md Nazim Uddin, +2 authors, Maode Lai.
J Oncol, 2020 Aug 11; 2020. PMID: 32774369    Free PMC article.
Relaxin-expressing oncolytic adenovirus induces remodeling of physical and immunological aspects of cold tumor to potentiate PD-1 blockade.
Bo-Kyeong Jung, Hae Young Ko, +6 authors, Chae-Ok Yun.
J Immunother Cancer, 2020 Aug 06; 8(2). PMID: 32753544    Free PMC article.
A novel culture method that sustains ERα signaling in human breast cancer tissue microstructures.
Ana Luísa Cartaxo, Marta F Estrada, +9 authors, Catarina Brito.
J Exp Clin Cancer Res, 2020 Aug 19; 39(1). PMID: 32807212    Free PMC article.
Combination of PARP Inhibitor Olaparib, and PD-L1 Inhibitor Durvalumab, in Recurrent Ovarian Cancer: a Proof-of-Concept Phase II Study.
Erika J Lampert, Alexandra Zimmer, +15 authors, Jung-Min Lee.
Clin Cancer Res, 2020 May 14; 26(16). PMID: 32398324    Free PMC article.
HDAC6 Plays a Noncanonical Role in the Regulation of Antitumor Immune Responses, Dissemination, and Invasiveness of Breast Cancer.
Debarati Banik, Satish Noonepalle, +11 authors, Alejandro Villagra.
Cancer Res, 2020 Jul 02; 80(17). PMID: 32605998    Free PMC article.
Improved prognosis of low baseline neutrophil-to-lymphocyte ratio is significantly exclusive in breast cancer patients with high absolute counts of lymphocytes.
Yukie Fujimoto, Hiromi Ozawa, +4 authors, Yasuo Miyoshi.
Mol Clin Oncol, 2019 Jan 27; 10(2). PMID: 30680208    Free PMC article.
A novel combination of chemotherapy and immunotherapy controls tumor growth in mice with a human immune system.
Aude Burlion, Rodrigo N Ramos, +7 authors, Gilles Marodon.
Oncoimmunology, 2019 May 31; 8(7). PMID: 31143518    Free PMC article.
Correlate the TP53 Mutation and the HRAS Mutation with Immune Signatures in Head and Neck Squamous Cell Cancer.
Haoyu Lyu, Mengyuan Li, +2 authors, Xiaosheng Wang.
Comput Struct Biotechnol J, 2019 Aug 21; 17. PMID: 31428295    Free PMC article.
Identification of CTLA-4 associated with tumor microenvironment and competing interactions in triple negative breast cancer by co-expression network analysis.
Ziqi Peng, Peng Su, +4 authors, Bowen Yang.
J Cancer, 2020 Oct 10; 11(21). PMID: 33033520    Free PMC article.
Prognostic Value of SLC4A4 and its Correlation with Immune Infiltration in Colon Adenocarcinoma.
Xiaoli Chen, Jianing Chen, Yan Feng, Wei Guan.
Med Sci Monit, 2020 Sep 20; 26. PMID: 32949121    Free PMC article.
Feasibility study on pre or postoperative accelerated radiotherapy (POP-ART) in breast cancer patients.
Hans Van Hulle, Vincent Vakaet, +11 authors, Liv Veldeman.
Pilot Feasibility Stud, 2020 Oct 17; 6. PMID: 33062295    Free PMC article.
The NAD-dependent deacetylase SIRT2 regulates T cell differentiation involved in tumor immune response.
Cui Jiang, Jingwei Liu, +13 authors, Liu Cao.
Int J Biol Sci, 2020 Oct 17; 16(15). PMID: 33061819    Free PMC article.
The Role of the Tumor Microenvironment in Developing Successful Therapeutic and Secondary Prophylactic Breast Cancer Vaccines.
Benjamin Gordon, Vijayakrishna K Gadi.
Vaccines (Basel), 2020 Sep 18; 8(3). PMID: 32937885    Free PMC article.
Review.
TILs Immunophenotype in Breast Cancer Predicts Local Failure and Overall Survival: Analysis in a Large Radiotherapy Trial with Long-Term Follow-Up.
Ewan Millar, Lois Browne, +8 authors, Peter H Graham.
Cancers (Basel), 2020 Aug 23; 12(9). PMID: 32825588    Free PMC article.
Ovarian Cancer Cells Promote Glycolysis Metabolism and TLR8-Mediated Metabolic Control of Human CD4+ T Cells.
Wenwen Shang, Rui Xu, +3 authors, Fang Wang.
Front Oncol, 2020 Oct 27; 10. PMID: 33102225    Free PMC article.
NLRP3 as Putative Marker of Ipilimumab-Induced Cardiotoxicity in the Presence of Hyperglycemia in Estrogen-Responsive and Triple-Negative Breast Cancer Cells.
Vincenzo Quagliariello, Michelino De Laurentiis, +8 authors, Nicola Maurea.
Int J Mol Sci, 2020 Oct 25; 21(20). PMID: 33096896    Free PMC article.
A Methylation-Based Reclassification of Bladder Cancer Based on Immune Cell Genes.
Qizhan Luo, Thomas-Alexander Vögeli.
Cancers (Basel), 2020 Oct 24; 12(10). PMID: 33092083    Free PMC article.
Differential kynurenine pathway metabolism in highly metastatic aggressive breast cancer subtypes: beyond IDO1-induced immunosuppression.
Benjamin Heng, Ayse A Bilgin, +8 authors, Gilles J Guillemin.
Breast Cancer Res, 2020 Oct 29; 22(1). PMID: 33109232    Free PMC article.
Abundance of Regulatory T Cell (Treg) as a Predictive Biomarker for Neoadjuvant Chemotherapy in Triple-Negative Breast Cancer.
Masanori Oshi, Mariko Asaoka, +7 authors, Kazuaki Takabe.
Cancers (Basel), 2020 Oct 23; 12(10). PMID: 33086518    Free PMC article.
A comparison of complete pathologic response rates following neoadjuvant chemotherapy among South African breast cancer patients with and without concurrent HIV infection.
Sarah Nietz, Daniel S O'Neil, +13 authors, Herbert Cubasch.
Breast Cancer Res Treat, 2020 Sep 03; 184(3). PMID: 32875480    Free PMC article.
Expression of Monocarboxylate Transporter 1 in Immunosuppressive Macrophages Is Associated With the Poor Prognosis in Breast Cancer.
Bei Li, Qian Yang, +4 authors, Shengrong Sun.
Front Oncol, 2020 Nov 13; 10. PMID: 33178603    Free PMC article.
The Tumor Microenvironment of Primitive and Metastatic Breast Cancer: Implications for Novel Therapeutic Strategies.
Giovanni Zarrilli, Gianluca Businello, +8 authors, Matteo Fassan.
Int J Mol Sci, 2020 Nov 05; 21(21). PMID: 33143050    Free PMC article.
Review.
Type I interferon/IRF7 axis instigates chemotherapy-induced immunological dormancy in breast cancer.
Qiang Lan, Sanam Peyvandi, +9 authors, Curzio Rüegg.
Oncogene, 2018 Dec 14; 38(15). PMID: 30546090    Free PMC article.
Correlation between apparent diffusion coefficient of magnetic resonance imaging and tumor-infiltrating lymphocytes in breast cancer.
Marco Fogante, Corrado Tagliati, +3 authors, Andrea Giovagnoni.
Radiol Med, 2019 Feb 27; 124(7). PMID: 30806920
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.
Anna Glajcar, Joanna Szpor, +2 authors, Krzysztof Okoń.
Virchows Arch, 2019 Apr 25; 475(1). PMID: 31016433    Free PMC article.
TAAR1 levels and sub-cellular distribution are cell line but not breast cancer subtype specific.
Mallory S Pitts, Josh N McShane, +2 authors, Mark D Berry.
Histochem Cell Biol, 2019 May 22; 152(2). PMID: 31111198
Novel miRNA Targets and Therapies in the Triple-Negative Breast Cancer Microenvironment: An Emerging Hope for a Challenging Disease.
Amal Qattan.
Int J Mol Sci, 2020 Dec 02; 21(23). PMID: 33255471    Free PMC article.
Review.
The molecular landscape of Asian breast cancers reveals clinically relevant population-specific differences.
Jia-Wern Pan, Muhammad Mamduh Ahmad Zabidi, +10 authors, Soo-Hwang Teo.
Nat Commun, 2020 Dec 24; 11(1). PMID: 33353943    Free PMC article.
Prognostic Role of Immune Markers in Triple Negative Breast Carcinoma.
Hulya Sahin Ozkan, Mustafa Umit Ugurlu, Perran Fulden Yumuk, Handan Kaya.
Pathol Oncol Res, 2020 Jul 19; 26(4). PMID: 32681436
Multiplex immunofluorescence to measure dynamic changes in tumor-infiltrating lymphocytes and PD-L1 in early-stage breast cancer.
Katherine Sanchez, Isaac Kim, +11 authors, David B Page.
Breast Cancer Res, 2021 Jan 09; 23(1). PMID: 33413574    Free PMC article.
Addition of carboplatin-gemcitabine as second-line neoadjuvant chemotherapy in non-responsive locally advanced breast cancer patients to standard neoadjuvant chemotherapy and evaluation of factors affecting response: a randomized controlled trial.
Dena Firouzabadi, Amirreza Dehghanian, +2 authors, Abdolrasoul Talei.
BMC Cancer, 2021 Jan 13; 21(1). PMID: 33430808    Free PMC article.
Prognostic and predictive parameters in breast pathology: a pathologist's primer.
Kimberly H Allison.
Mod Pathol, 2020 Nov 07; 34(Suppl 1). PMID: 33154551
Comprehensive analysis of glutathione peroxidase-1 (GPX1) expression and prognostic value in three different types of renal cell carcinoma.
Shaohua Chen, Xiaotao Su, +4 authors, Siqin Zhang.
Transl Androl Urol, 2021 Jan 19; 9(6). PMID: 33457246    Free PMC article.
Identification of Prognostic Biomarkers and Molecular Targets Among JAK Family in Breast Cancer.
Fangteng Liu, Hengyu Wu.
J Inflamm Res, 2021 Jan 21; 14. PMID: 33469338    Free PMC article.
COL1A1 Is a Potential Prognostic Biomarker and Correlated with Immune Infiltration in Mesothelioma.
Cangang Zhang, Shanshan Liu, +3 authors, Haibo Liu.
Biomed Res Int, 2021 Jan 26; 2021. PMID: 33490271    Free PMC article.
Immune microenvironment in different molecular subtypes of ductal breast carcinoma.
Mona Sadeghalvad, Hamid-Reza Mohammadi-Motlagh, Nima Rezaei.
Breast Cancer Res Treat, 2020 Oct 05; 185(2). PMID: 33011829
Review.
RNA m6A Methylation Regulators Subclassify Luminal Subtype in Breast Cancer.
Lin Yang, Shuangling Wu, +4 authors, Wei-Min Tong.
Front Oncol, 2021 Feb 16; 10. PMID: 33585234    Free PMC article.
Overexpression of LncRNA BM466146 Predicts Better Prognosis of Breast Cancer.
Yunxiang Zhang, Xiaotong Dong, +9 authors, Peng Gao.
Front Oncol, 2021 Feb 16; 10. PMID: 33585256    Free PMC article.
AURKA and FAM83A are prognostic biomarkers and correlated with Tumor-infiltrating Lymphocytes in smoking related Lung Adenocarcinoma.
Mengyu Zhang, Chen Huo, +4 authors, Yiqing Qu.
J Cancer, 2021 Feb 23; 12(6). PMID: 33613763    Free PMC article.
TIGIT promotes CD8+T cells exhaustion and predicts poor prognosis of colorectal cancer.
Rongpu Liang, Xudong Zhu, +9 authors, Bo Wei.
Cancer Immunol Immunother, 2021 Feb 27;. PMID: 33634371
Inflammation markers on benign breast biopsy are associated with risk of invasive breast cancer in African American women.
Asra N Shaik, Katrin Kiavash, +7 authors, Michele L Cote.
Breast Cancer Res Treat, 2020 Oct 29; 185(3). PMID: 33113091
Back to simplicity: a four-marker blood cell score to quantify prognostically relevant myeloid cells in melanoma patients.
Veronica Huber, Lorenza Di Guardo, +18 authors, Licia Rivoltini.
J Immunother Cancer, 2021 Feb 17; 9(2). PMID: 33589521    Free PMC article.
Pre-treatment neutrophil-lymphocyte and platelet-lymphocyte ratios as additional markers for breast cancer progression: A retrospective cohort study.
Sumadi Lukman Anwar, Roby Cahyono, +3 authors, Teguh Aryandono.
Ann Med Surg (Lond), 2021 Mar 05; 63. PMID: 33659054    Free PMC article.
Reclassification of Kidney Clear Cell Carcinoma Based on Immune Cell Gene-Related DNA CpG Pairs.
Qizhan Luo, Thomas-Alexander Vögeli.
Biomedicines, 2021 Mar 07; 9(2). PMID: 33672457    Free PMC article.
Association between the preoperative neutrophil-to-lymphocyte ratio and tertiary lymphoid structures surrounding tumor in gastric cancer.
Yoshihito Yamakoshi, Hiroaki Tanaka, +9 authors, Masaichi Ohira.
Mol Clin Oncol, 2021 Mar 09; 14(4). PMID: 33680464    Free PMC article.
Enhanced humoral immunity in breast cancer patients with high serum concentration of anti-HER2 autoantibody.
Yasufumi Sato, Masafumi Shimoda, +7 authors, Kenzo Shimazu.
Cancer Med, 2021 Jan 29; 10(4). PMID: 33506656    Free PMC article.
Hyperglycemia and Chemoresistance in Breast Cancer: From Cellular Mechanisms to Treatment Response.
Jie Qiu, Qinghui Zheng, Xuli Meng.
Front Oncol, 2021 Mar 16; 11. PMID: 33718202    Free PMC article.
Review.
Tumor cell intrinsic RON signaling suppresses innate immune responses in breast cancer through inhibition of IRAK4 signaling.
Jennifer R Bourn, Sasha J Ruiz-Torres, +2 authors, Susan E Waltz.
Cancer Lett, 2021 Jan 29; 503. PMID: 33508385    Free PMC article.
High IRF8 expression correlates with CD8 T cell infiltration and is a predictive biomarker of therapy response in ER-negative breast cancer.
Gerardo Gatti, Courtney Betts, +11 authors, Mariana Maccioni.
Breast Cancer Res, 2021 Mar 27; 23(1). PMID: 33766090    Free PMC article.
A combination of PD‑1/PD‑L1 inhibitors: The prospect of overcoming the weakness of tumor immunotherapy (Review).
Xianbin Kong, Peng Lu, +8 authors, Jingyan Meng.
Mol Med Rep, 2021 Mar 25; 23(5). PMID: 33760188    Free PMC article.
Review.
Cryoablation and Immunotherapy for Breast Cancer: Overview and Rationale for Combined Therapy.
Helaina C Regen-Tuero, Robert C Ward, William M Sikov, Peter J Littrup.
Radiol Imaging Cancer, 2021 Apr 06; 3(2). PMID: 33817653    Free PMC article.
Review.
Construction of a risk map to understand the vulnerability of various types of cancer patients to COVID-19 infection.
Jian He, Xufang Yang, Hui Wang.
MedComm (Beijing), 2021 Apr 07; 2(1). PMID: 33821252    Free PMC article.
The Peripheral Immune Landscape of Breast Cancer: Clinical Findings and In Vitro Models for Biomarker Discovery.
Sofia Batalha, Sofia Ferreira, Catarina Brito.
Cancers (Basel), 2021 Apr 04; 13(6). PMID: 33804027    Free PMC article.
Review.
Identification of MEG8/miR-378d/SOBP axis as a novel regulatory network and associated with immune infiltrates in ovarian carcinoma by integrated bioinformatics analysis.
Jian Lei, Zhen-Yu He, +6 authors, Juan Zhou.
Cancer Med, 2021 Mar 21; 10(8). PMID: 33742531    Free PMC article.
TACC3 is a prognostic biomarker for kidney renal clear cell carcinoma and correlates with immune cell infiltration and T cell exhaustion.
Xiaoyan Fan, Boyi Liu, Zhiyu Wang, Dongwei He.
Aging (Albany NY), 2021 Mar 14; 13(6). PMID: 33714201    Free PMC article.
Prognostic role of proliferating CD8+ cytotoxic Tcells in human cancers.
Niclas C Blessin, Wenchao Li, +23 authors, Stefan Steurer.
Cell Oncol (Dordr), 2021 Apr 18;. PMID: 33864611
Algorithm-Based Meta-Analysis Reveals the Mechanistic Interaction of the Tumor Suppressor LIMD1 With Non-Small-Cell Lung Carcinoma.
Ling Wang, Ayrianna Sparks-Wallace, +2 authors, Shunbin Ning.
Front Oncol, 2021 Apr 20; 11. PMID: 33869018    Free PMC article.
Metabolism and immunity in breast cancer.
Deyu Zhang, Xiaojie Xu, Qinong Ye.
Front Med, 2020 Oct 20; 15(2). PMID: 33074528
Review.
LINC00460 Is a Dual Biomarker That Acts as a Predictor for Increased Prognosis in Basal-Like Breast Cancer and Potentially Regulates Immunogenic and Differentiation-Related Genes.
Mireya Cisneros-Villanueva, Lizbett Hidalgo-Pérez, +13 authors, Alfredo Hidalgo-Miranda.
Front Oncol, 2021 Apr 30; 11. PMID: 33912452    Free PMC article.
Inflammatory Markers in Cancer Immunotherapy.
Deepak Ravindranathan, Viraj A Master, Mehmet Asim Bilen.
Biology (Basel), 2021 May 01; 10(4). PMID: 33924623    Free PMC article.
Review.
VWCE as a potential biomarker associated with immune infiltrates in breast cancer.
Qin Huo, Zhenwei Li, +3 authors, Ni Xie.
Cancer Cell Int, 2021 May 23; 21(1). PMID: 34020650    Free PMC article.
The immune microenvironment and relation to outcome in patients with advanced breast cancer treated with docetaxel with or without gemcitabine.
Elisabeth S Stovgaard, Karama Asleh, +8 authors, Torsten O Nielsen.
Oncoimmunology, 2021 May 25; 10(1). PMID: 34026336    Free PMC article.
The Role of Inflammation in Breast and Prostate Cancer Metastasis to Bone.
Andy Göbel, Stefania Dell'Endice, +4 authors, Tilman D Rachner.
Int J Mol Sci, 2021 Jun 03; 22(10). PMID: 34064859    Free PMC article.
Review.