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Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Research Article

Concomitant Expression of CD39, CD69, and CD103 Identifies Antitumor CD8+ T Cells in Breast Cancer Implications for Adoptive Cell Therapy

Author(s): Grace Ivonne Gattas Lama*, Gregory Noél, Francisco Carlos López Márquez, Faviel Francisco González Galarza, Adria Imelda Prieto Hinojosa, Lydia Enith Nava Rivera, Karen Willard-Gallo and Jesús Rafael Arguëllo Astorga*

Volume 25, Issue 13, 2024

Published on: 16 October, 2023

Page: [1747 - 1757] Pages: 11

DOI: 10.2174/1389201025666230901094219

Price: $65

Abstract

Background: In cancer, an effective immune response involves the action of several different cell types, among which CD8 T cells play a major role as they can specifically recognize and kill cancer cells via the release of cytotoxic molecules and cytokines, being of major importance for adoptive cell transfer (ACT) of ex vivo expanded tumor-infiltrating lymphocytes (TILs). The inflammation resulting from the tumor growth attracts both activated and bystander T cells. For an effective antitumor response, the T cell must express a specific group of chemokine receptors and integrins which include CD103, CD39, CD69, and CD25. These markers had already been analyzed in various cancers, not including breast cancer and their subsequent subtypes, until now. To analyze, the key receptors on ex vivo expanded tumor-infiltrating lymphocytes in luminal A and luminal B breast cancer (BC) subtypes.

Materials and Methods: We were successful in expanding TILs ex vivo using a standard TIL culture condition from a cohort study of 15 primary luminal A and luminal B breast cancer patients. Furthermore, we examined the expression of CD103, CD39, CD69, and CD25 biomarkers after the expansion by flow cytometry.

Results: We found that the information about the percentage of TILs obtainable after the ex vivo expansion is not associated to nor it is dependent on the heterogeneity of the TIL population before the expansion and does not differ by the molecular subtype (p>0.05). We also found that there is a major population of memory-resident antitumor CD8+CD103+CD39+ and CD8+CD103+ CD69+ TILs present in the stroma after the expansion when compared to CD4 immunosubtypes (p<0.0001). Only the CD8+CD103+CD39+ subpopulation was related to BC subtype (0.0009).

Conclusion: Evidence from our study suggests that CD8 TILs present in the stroma of luminal A and luminal B breast cancer patients can be quantified and phenotyped by flow cytometry and be further expanded ex vivo. The immuno-phenotyping of these markers may be targeted to improve the success of immunotherapeutic approaches, such as adoptive cellular therapy (ACT) in patients with BC.

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[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Schumacher, T.N.; Schreiber, R.D. Neoantigens in cancer immunotherapy. Sci., 2015, 348(6230), 69-74.
[http://dx.doi.org/10.1126/science.aaa4971] [PMID: 25838375]
[3]
Savas, P.; Salgado, R.; Denkert, C.; Sotiriou, C.; Darcy, P.K.; Smyth, M.J.; Loi, S. Clinical relevance of host immunity in breast cancer: From TILs to the clinic. Nat. Rev. Clin. Oncol., 2016, 13(4), 228-241.
[http://dx.doi.org/10.1038/nrclinonc.2015.215] [PMID: 26667975]
[4]
Loi, S.; Adams, S.; Schmid, P.; Cortés, J.; Cescon, D.W.; Winer, E.P.; Toppmeyer, D.L.; Rugo, H.S.; De Laurentiis, M.; Nanda, R.; Iwata, H.; Awada, A.; Tan, A.; Aktan, G.; Karantza, V.; Salgado, R. Relationship between tumor infiltrating lymphocyte (TIL) levels and response to pembrolizumab (pembro) in metastatic triple- negative breast cancer: Results from KEYNOTE-086. Ann. Oncol., 2017, 28(S5), 608.
[http://dx.doi.org/10.1093/annonc/mdx440.005]
[5]
Loi, S.; Drubay, D.; Adams, S.; Pruneri, G.; Francis, P.A.; Lacroix-Triki, M.; Joensuu, H.; Dieci, M.V.; Badve, S.; Demaria, S.; Gray, R.; Munzone, E.; Lemonnier, J.; Sotiriou, C.; Piccart, M.J.; Kellokumpu-Lehtinen, P.L.; Vingiani, A.; Gray, K.; Andre, F.; Denkert, C.; Salgado, R.; Michiels, S. Tumor-infiltrating lymphocytes and Prognosis: A pooled individual patient analysis of early-stage triple-negative breast cancers. J. Clin. Oncol., 2019, 37(7), 559-569.
[http://dx.doi.org/10.1200/JCO.18.01010] [PMID: 30650045]
[6]
Nanda, R.; Chow, L.Q.M.; Dees, E.C.; Berger, R.; Gupta, S.; Geva, R.; Pusztai, L.; Pathiraja, K.; Aktan, G.; Cheng, J.D.; Karantza, V.; Buisseret, L. Pembrolizumab in patients with advanced triple-negative breast cancer: Phase Ib KEYNOTE-012 study. J. Clin. Oncol., 2016, 34(21), 2460-2467.
[http://dx.doi.org/10.1200/JCO.2015.64.8931] [PMID: 27138582]
[7]
Emens, L.A.; Cruz, C.; Eder, J.P.; Braiteh, F.; Chung, C.; Tolaney, S.M.; Kuter, I.; Nanda, R.; Cassier, P.A.; Delord, J.P.; Gordon, M.S.; ElGabry, E.; Chang, C.W.; Sarkar, I.; Grossman, W.; O’Hear, C.; Fassò, M.; Molinero, L.; Schmid, P. Long-term clinical outcomes and biomarker analyses of atezolizumab therapy for patients with metastatic triple-negative breast cancer. JAMA Oncol., 2019, 5(1), 74-82.
[http://dx.doi.org/10.1001/jamaoncol.2018.4224] [PMID: 30242306]
[8]
Adams, S.; Loi, S.; Toppmeyer, D.; Cescon, D.W.; De Laurentiis, M.; Nanda, R.; Winer, E.P.; Mukai, H.; Tamura, K.; Armstrong, A.; Liu, M.C.; Iwata, H.; Ryvo, L.; Wimberger, P.; Card, D.; Ding, Y.; Karantza, V.; Schmid, P. Phase 2 study of pembrolizumab as first-line therapy for PD-L1–positive metastatic triple-negative breast cancer (mTNBC): Preliminary data from KEYNOTE-086 cohort B. J. Clin. Oncol., 2017, 35(S15), 1088.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.1088]
[9]
Schmid, P.; Park, Y.H.; Muñoz-Couselo, E.; Kim, S.B.; Sohn, J. Im, S-A.; Holgado, E.; Wang, Y.; Dang, T.; Aktan, G.; Cortés, J. Pembrolizumab (pembro) + chemotherapy (chemo) as neoadjuvant treatment for triple negative breast cancer (TNBC): Preliminary results from KEYNOTE-173. J. Clin. Oncol., 2017, 35(S15), 556.
[http://dx.doi.org/10.1200/JCO.2017.35.15_suppl.556]
[10]
Buisseret, L.; Garaud, S.; de Wind, A.; Van den Eynden, G.; Boisson, A.; Solinas, C.; Gu-Trantien, C.; Naveaux, C.; Lodewyckx, J.N.; Duvillier, H.; Craciun, L.; Veys, I.; Larsimont, D.; Piccart-Gebhart, M.; Stagg, J.; Sotiriou, C.; Willard-Gallo, K. Tumor-infiltrating lymphocyte composition, organization and PD-1/PD-L1 expression are linked in breast cancer. OncoImmunology, 2017, 6(1), e1257452.
[http://dx.doi.org/10.1080/2162402X.2016.1257452] [PMID: 28197375]
[11]
Solinas, C.; Gombos, A.; Latifyan, S.; Piccart-Gebhart, M.; Kok, M.; Buisseret, L. Targeting immune checkpoints in breast cancer: An update of early results. ESMO Open, 2017, 2(5), e000255.
[http://dx.doi.org/10.1136/esmoopen-2017-000255] [PMID: 29177095]
[12]
Loi, S.; Giobbie-Hurder, A.; Gombos, A.; Bachelot, T.; Hui, R.; Curigliano, G.; Campone, M.; Biganzoli, L.; Bonnefoi, H.; Jerusalem, G.; Bartsch, R.; Rabaglio-Poretti, M.; Kammler, R.; Maibach, R.; Smyth, M.J.; Di Leo, A.; Colleoni, M.; Viale, G.; Regan, M.M.; André, F. Pembrolizumab plus trastuzumab in trastuzumab-resistant, advanced, HER2-positive breast cancer (PANACEA): A single-arm, multicentre, phase 1b–2 trial. Lancet Oncol., 2019, 20(3), 371-382.
[http://dx.doi.org/10.1016/S1470-2045(18)30812-X] [PMID: 30765258]
[13]
Dudley, M.E.; Wunderlich, J.R.; Shelton, T.E.; Even, J.; Rosenberg, S.A. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J. Immunother., 2003, 26(4), 332-342.
[http://dx.doi.org/10.1097/00002371-200307000-00005] [PMID: 12843795]
[14]
Rosenberg, S.A.; Dudley, M.E. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr. Opin. Immunol., 2009, 21(2), 233-240.
[http://dx.doi.org/10.1016/j.coi.2009.03.002] [PMID: 19304471]
[15]
Besser, M.J.; Shapira-Frommer, R.; Itzhaki, O.; Treves, A.J.; Zippel, D.B.; Levy, D.; Kubi, A.; Shoshani, N.; Zikich, D.; Ohayon, Y.; Ohayon, D.; Shalmon, B.; Markel, G.; Yerushalmi, R.; Apter, S.; Ben-Nun, A.; Ben-Ami, E.; Shimoni, A.; Nagler, A.; Schachter, J. Adoptive transfer of tumor-infiltrating lymphocytes in patients with metastatic melanoma: Intent-to-treat analysis and efficacy after failure to prior immunotherapies. Clin. Cancer Res., 2013, 19(17), 4792-4800.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-0380] [PMID: 23690483]
[16]
Cardoso, F.; Kyriakides, S.; Ohno, S.; Penault-Llorca, F.; Poortmans, P.; Rubio, I.T.; Zackrisson, S.; Senkus, E. Early breast cancer: ESMO Clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol., 2019, 30(8), 1194-1220.
[http://dx.doi.org/10.1093/annonc/mdz173] [PMID: 31161190]
[17]
Klebanoff, C.A.; Gattinoni, L.; Restifo, N.P. CD8 + T-cell memory in tumor immunology and immunotherapy. Immunol. Rev., 2006, 211(1), 214-224.
[http://dx.doi.org/10.1111/j.0105-2896.2006.00391.x] [PMID: 16824130]
[18]
Finn, O.J. Human tumor antigens yesterday, today, and tomorrow. Cancer Immunol. Res., 2017, 5(5), 347-354.
[http://dx.doi.org/10.1158/2326-6066.CIR-17-0112] [PMID: 28465452]
[19]
Gros, A.; Robbins, P.F.; Yao, X.; Li, Y.F.; Turcotte, S.; Tran, E.; Wunderlich, J.R.; Mixon, A.; Farid, S.; Dudley, M.E.; Hanada, K.; Almeida, J.R.; Darko, S.; Douek, D.C.; Yang, J.C.; Rosenberg, S.A. PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors. J. Clin. Invest., 2014, 124(5), 2246-2259.
[http://dx.doi.org/10.1172/JCI73639] [PMID: 24667641]
[20]
Inozume, T.; Hanada, K.; Wang, Q.J.; Ahmadzadeh, M.; Wunderlich, J.R.; Rosenberg, S.A.; Yang, J.C. Selection of CD8+PD-1+ lymphocytes in fresh human melanomas enriches for tumor-reactive T cells. J. Immunother., 2010, 33(9), 956-964.
[http://dx.doi.org/10.1097/CJI.0b013e3181fad2b0] [PMID: 20948441]
[21]
Wolfl, M.; Kuball, J.; Ho, W.Y.; Nguyen, H.; Manley, T.J.; Bleakley, M.; Greenberg, P.D. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood, 2007, 110(1), 201-210.
[http://dx.doi.org/10.1182/blood-2006-11-056168] [PMID: 17371945]
[22]
Ye, Q.; Song, D.G.; Poussin, M.; Yamamoto, T.; Best, A.; Li, C.; Coukos, G.; Powell, D.J., Jr CD137 accurately identifies and enriches for naturally occurring tumor-reactive T cells in tumor. Clin. Cancer Res., 2014, 20(1), 44-55.
[http://dx.doi.org/10.1158/1078-0432.CCR-13-0945] [PMID: 24045181]
[23]
Mueller, S.N.; Mackay, L.K. Tissue-resident memory T cells: Local specialists in immune defence. Nat. Rev. Immunol., 2016, 16(2), 79-89.
[http://dx.doi.org/10.1038/nri.2015.3] [PMID: 26688350]
[24]
Schenkel, J.M.; Fraser, K.A.; Beura, L.K.; Pauken, K.E.; Vezys, V.; Masopust, D. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Sci., 2014, 346(6205), 98-101.
[http://dx.doi.org/10.1126/science.1254536] [PMID: 25170049]
[25]
Schenkel, J.M.; Masopust, D. Tissue-resident memory T cells. Immunity, 2014, 41(6), 886-897.
[http://dx.doi.org/10.1016/j.immuni.2014.12.007] [PMID: 25526304]
[26]
El-Asady, R.; Yuan, R.; Liu, K.; Wang, D.; Gress, R.E.; Lucas, P.J.; Drachenberg, C.B.; Hadley, G.A. TGF-β–dependent CD103 expression by CD8+ T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease. J. Exp. Med., 2005, 201(10), 1647-1657.
[http://dx.doi.org/10.1084/jem.20041044] [PMID: 15897278]
[27]
Antonioli, L.; Pacher, P.; Vizi, E.S.; Haskó, G. CD39 and CD73 in immunity and inflammation. Trends Mol. Med., 2013, 19(6), 355-367.
[http://dx.doi.org/10.1016/j.molmed.2013.03.005] [PMID: 23601906]
[28]
Young, A.; Mittal, D.; Stagg, J.; Smyth, M.J. Targeting cancer-derived adenosine: New therapeutic approaches. Cancer Discov., 2014, 4(8), 879-888.
[http://dx.doi.org/10.1158/2159-8290.CD-14-0341] [PMID: 25035124]
[29]
Gupta, P.K.; Godec, J.; Wolski, D.; Adland, E.; Yates, K.; Pauken, K.E.; Cosgrove, C.; Ledderose, C.; Junger, W.G.; Robson, S.C.; Wherry, E.J.; Alter, G.; Goulder, P.J.R.; Klenerman, P.; Sharpe, A.H.; Lauer, G.M.; Haining, W.N. CD39 Expression identifies terminally exhausted CD8+ T cells. PLoS Pathog., 2015, 11(10), e1005177.
[http://dx.doi.org/10.1371/journal.ppat.1005177] [PMID: 26485519]
[30]
Masopust, D.; Soerens, A.G.; Tissue-Resident, T. Tissue-resident T cells and other resident leukocytes. Annu. Rev. Immunol., 2019, 37(1), 521-546.
[http://dx.doi.org/10.1146/annurev-immunol-042617-053214] [PMID: 30726153]
[31]
Gebhardt, T.; Wakim, L.M.; Eidsmo, L.; Reading, P.C.; Heath, W.R.; Carbone, F.R.; Memory, T. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol., 2009, 10(5), 524-530.
[http://dx.doi.org/10.1038/ni.1718] [PMID: 19305395]
[32]
Masopust, D.; Choo, D.; Vezys, V.; Wherry, E.J.; Duraiswamy, J.; Akondy, R.; Wang, J.; Casey, K.A.; Barber, D.L.; Kawamura, K.S.; Fraser, K.A.; Webby, R.J.; Brinkmann, V.; Butcher, E.C.; Newell, K.A.; Ahmed, R.; Dynamic, T. Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med., 2010, 207(3), 553-564.
[http://dx.doi.org/10.1084/jem.20090858] [PMID: 20156972]
[33]
Duhen, T.; Duhen, R.; Montler, R.; Moses, J.; Moudgil, T.; de Miranda, N.F.; Goodall, C.P.; Blair, T.C.; Fox, B.A.; McDermott, J.E.; Chang, S.C.; Grunkemeier, G.; Leidner, R.; Bell, R.B.; Weinberg, A.D. Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors. Nat. Commun., 2018, 9(1), 2724.
[http://dx.doi.org/10.1038/s41467-018-05072-0] [PMID: 30006565]
[34]
Allakhverdi, Z.; Fitzpatrick, D.; Boisvert, A.; Baba, N.; Bouguermouh, S.; Sarfati, M.; Delespesse, G. Expression of CD103 identifies human regulatory T-cell subsets. J. Allergy Clin. Immunol., 2006, 118(6), 1342-1349.
[http://dx.doi.org/10.1016/j.jaci.2006.07.034] [PMID: 17137867]
[35]
Shiow, L.R.; Rosen, D.B.; Brdičková, N.; Xu, Y.; An, J.; Lanier, L.L.; Cyster, J.G.; Matloubian, M. CD69 acts downstream of interferon-α/β to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature, 2006, 440(7083), 540-544.
[http://dx.doi.org/10.1038/nature04606] [PMID: 16525420]
[36]
Byrne, A.; Savas, P.; Sant, S.; Li, R.; Virassamy, B.; Luen, S.J.; Beavis, P.A.; Mackay, L.K.; Neeson, P.J.; Loi, S. Tissue-resident memory T cells in breast cancer control and immunotherapy responses. Nat. Rev. Clin. Oncol., 2020, 17(6), 341-348.
[http://dx.doi.org/10.1038/s41571-020-0333-y] [PMID: 32112054]
[37]
Garaud, S.; Gu-Trantien, C.; Lodewyckx, J.N.; Boisson, A.; De Silva, P.; Buisseret, L.; Migliori, E.; Libin, M.; Naveaux, C.; Duvillier, H.; Willard-Gallo, K. A simple and rapid protocol to non-enzymatically dissociate fresh human tissues for the analysis of infiltrating lymphocytes. J. Vis. Exp., 2014, (94), 52392.
[http://dx.doi.org/10.3791/52392] [PMID: 25548995]
[38]
Buisseret, L.; Desmedt, C.; Garaud, S.; Fornili, M.; Wang, X.; Van den Eyden, G.; de Wind, A.; Duquenne, S.; Boisson, A.; Naveaux, C.; Rothé, F.; Rorive, S.; Decaestecker, C.; Larsimont, D.; Piccart-Gebhart, M.; Biganzoli, E.; Sotiriou, C.; Willard-Gallo, K. Reliability of tumor-infiltrating lymphocyte and tertiary lymphoid structure assessment in human breast cancer. Mod. Pathol., 2017, 30(9), 1204-1212.
[http://dx.doi.org/10.1038/modpathol.2017.43] [PMID: 28621322]
[39]
Lee, H.J.; Kim, Y.A.; Sim, C.K.; Heo, S.H.; Song, I.H.; Park, H.S.; Park, S.Y.; Bang, W.S.; Park, I.A.; Lee, M.; Lee, J.H.; Cho, Y.S.; Chang, S.; Jung, J.; Kim, J.; Lee, S.B.; Kim, S.Y.; Lee, M.S.; Gong, G. Expansion of tumor-infiltrating lymphocytes and their potential for application as adoptive cell transfer therapy in human breast cancer. Oncotarget, 2017, 8(69), 113345-113359.
[http://dx.doi.org/10.18632/oncotarget.23007] [PMID: 29371915]
[40]
Salgado, R.; Denkert, C.; Demaria, S.; Sirtaine, N.; Klauschen, F.; Pruneri, G.; Wienert, S.; Van den Eynden, G.; Baehner, F.L.; Penault-Llorca, F.; Perez, E.A.; Thompson, E.A.; Symmans, W.F.; Richardson, A.L.; Brock, J.; Criscitiello, C.; Bailey, H.; Ignatiadis, M.; Floris, G.; Sparano, J.; Kos, Z.; Nielsen, T.; Rimm, D.L.; Allison, K.H.; Reis-Filho, J.S.; Loibl, S.; Sotiriou, C.; Viale, G.; Badve, S.; Adams, S.; Willard-Gallo, K.; Loi, S. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: Recommendations by an international TILs working group 2014. Ann. Oncol., 2015, 26(2), 259-271.
[http://dx.doi.org/10.1093/annonc/mdu450] [PMID: 25214542]
[41]
Kverneland, A.H.; Chamberlain, C.A.; Borch, T.H.; Nielsen, M.; Mørk, S.K.; Kjeldsen, J.W.; Lorentzen, C.L.; Jørgensen, L.P.; Riis, L.B.; Yde, C.W.; Met, Ö.; Donia, M.; Marie Svane, I. Adoptive cell therapy with tumor-infiltrating lymphocytes supported by checkpoint inhibition across multiple solid cancer types. J. Immunother. Cancer, 2021, 9(10), e003499.
[http://dx.doi.org/10.1136/jitc-2021-003499] [PMID: 34607899]
[42]
Meng, S.; Li, L.; Zhou, M.; Jiang, W.; Niu, H.; Yang, K. Distribution and prognostic value of tumor infiltrating T cells in breast cancer. Mol. Med. Rep., 2018, 18(5), 4247-4258.
[http://dx.doi.org/10.3892/mmr.2018.9460] [PMID: 30221739]
[43]
Shi, F.; Chang, H.; Zhou, Q.; Zhao, Y.J.; Wu, G.J.; Song, Q.K. Distribution of CD4+ and CD8+ exhausted tumor-infiltrating lymphocytes in molecular subtypes of Chinese breast cancer patients. OncoTargets Ther., 2018, 11, 6139-6145.
[http://dx.doi.org/10.2147/OTT.S168057] [PMID: 30288049]
[44]
Zhang, S.; Liu, W.; Hu, B.; Wang, P.; Lv, X.; Chen, S.; Shao, Z. Prognostic significance of tumor-infiltrating natural killer cells in solid tumors: A systematic review and meta-analysis. Front. Immunol., 2020, 11, 1242.
[http://dx.doi.org/10.3389/fimmu.2020.01242] [PMID: 32714321]
[45]
Shenouda, M.M.; Gillgrass, A.; Nham, T.; Hogg, R.; Lee, A.J.; Chew, M.V.; Shafaei, M.; Aarts, C.; Lee, D.A.; Hassell, J.; Bane, A.; Dhesy-Thind, S.; Ashkar, A.A. Ex vivo expanded natural killer cells from breast cancer patients and healthy donors are highly cytotoxic against breast cancer cell lines and patient-derived tumours. Breast Cancer Res., 2017, 19(1), 76.
[http://dx.doi.org/10.1186/s13058-017-0867-9] [PMID: 28668076]
[46]
Fuentes-Antrás, J.; Guevara-Hoyer, K.; Baliu-Piqué, M.; García-Sáenz, J.Á.; Pérez-Segura, P. Pandiella, Atanasio; Ocaña, Alberto Adoptive cell therapy in breast cancer: A current perspective of next-generation medicine. Front. Oncol., 2020, 10, 605633.
[http://dx.doi.org/10.3389/fonc.2020.605633] [PMID: 33194771]
[47]
Huang, Y.; Ma, C.; Zhang, Q.; Ye, J.; Wang, F.; Zhang, Y.; Hunborg, P.; Varvares, M.A.; Hoft, D.F.; Hsueh, E.C.; Peng, G. CD4+ and CD8+ T cells have opposing roles in breast cancer progression and outcome. Oncotarget, 2015, 6(19), 17462-17478.
[http://dx.doi.org/10.18632/oncotarget.3958] [PMID: 25968569]
[48]
Mann, J.E.; Smith, J.D.; Birkeland, A.C.; Bellile, E.; Swiecicki, P.; Mierzwa, M.; Chinn, S.B.; Shuman, A.G.; Malloy, K.M.; Casper, K.A.; McLean, S.A.; Moyer, J.S.; Wolf, G.T.; Bradford, C.R.; Prince, M.E.; Carey, T.E.; McHugh, J.B.; Spector, M.E.; Brenner, J.C. Analysis of tumor-infiltrating CD103 resident memory T-cell content in recurrent laryngeal squamous cell carcinoma. Cancer Immunol. Immunother., 2019, 68(2), 213-220.
[http://dx.doi.org/10.1007/s00262-018-2256-3] [PMID: 30361882]
[49]
Djenidi, F.; Adam, J.; Goubar, A.; Durgeau, A.; Meurice, G.; de Montpréville, V.; Validire, P.; Besse, B.; Mami-Chouaib, F. CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients. J. Immunol., 2015, 194(7), 3475-3486.
[http://dx.doi.org/10.4049/jimmunol.1402711] [PMID: 25725111]
[50]
Vihervuori, H.; Autere, T.A.; Repo, H.; Kurki, S.; Kallio, L.; Lintunen, M.M.; Talvinen, K.; Kronqvist, P. Tumor-infiltrating lymphocytes and CD8+ T cells predict survival of triple-negative breast cancer. J. Cancer Res. Clin. Oncol., 2019, 145(12), 3105-3114.
[http://dx.doi.org/10.1007/s00432-019-03036-5] [PMID: 31562550]

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