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Combinatorial Chemistry & High Throughput Screening

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ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

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Research Article

Neoadjuvant Endocrine Therapy: A Potential Way to Make Cold Hormone Receptor-Rich Breast Cancer Hot

Author(s): Yinan Wu, Xiaonan Gong, Kaiyue Wang, Chengcheng Yu, Jili Qiu, Suzhan Zhang*, Yue Hu* and Kaimin Hu*

Volume 26, Issue 5, 2023

Published on: 04 August, 2022

Page: [1030 - 1041] Pages: 12

DOI: 10.2174/1386207325666220617145448

Price: $65

Abstract

Background: Turning the “cold” tumor immune microenvironment into “hot” is a critical issue in cancer treatment today. Hormone receptor-rich breast cancer (HR+ BC) was previously considered immunologically quiescent.

Objective: This study aims to explore the immunomodulatory effects of endocrine therapy on HR+ BCs.

Methods: The infiltrations and alterations of the tumor immune microenvironment in HR+ BCs before, after 10-14 days, and after three months of neoadjuvant endocrine therapy were computationally analyzed according to MCP-counter, CIBERSORT, xCell algorithms, and gene-set enrichment analysis (GSEA). The primary microarray data were obtained from three HR+ BC gene expression datasets (GSE20181, GSE55374, and GSE59515). Single-sample GSEA of hallmark and immune response gene sets was performed to evaluate the correlation between suspected treatment response and activated immune pathways in tumors.

Results: Both immune and stromal cells were specifically recruited into the HR+ BCs who responded to the neoadjuvant endocrine therapy by letrozole. Besides the enhanced infiltrations of immunosurveillance-related cells such as CD8+ T cells, dendritic cells, and the activation of immune response-related signals, the immunosuppressive M2-like macrophages, as well as the expression of immune checkpoint genes like PDCD1, SIRPA, and some HLA genes, were also stimulated in responders. We identified four pretreatment indicators (the intrinsic luminal subtype, the estrogen response early/late pathway, and the epithelial-mesenchymal transition pathway) as potential predictors of both clinical response and the activation of the tumor immune microenvironment post letrozole.

Conclusion: Neoadjuvant endocrine therapy showed a promising way to convert the immunologically “cold” HR+ BCs into “hot” tumors. This study provides new insights into the application of immunotherapy for HR+ BCs, especially those who respond to endocrine therapy.

Keywords: HR+ BCs, immune infiltrating, endocrine therapy, predictive marker, immunotherapy, EMT.

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[1]
Galon, J.; Bruni, D. Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat. Rev. Drug Discov., 2019, 18(3), 197-218.
[http://dx.doi.org/10.1038/s41573-018-0007-y] [PMID: 30610226]
[2]
Adams, S.; Gatti-Mays, M.E.; Kalinsky, K.; Korde, L.A.; Sharon, E.; Amiri-Kordestani, L.; Bear, H.; McArthur, H.L.; Frank, E.; Perlmutter, J.; Page, D.B.; Vincent, B.; Hayes, J.F.; Gulley, J.L.; Litton, J.K.; Hortobagyi, G.N.; Chia, S.; Krop, I.; White, J.; Sparano, J.; Disis, M.L.; Mittendorf, E.A. Current landscape of immunotherapy in breast cancer: A review. JAMA Oncol., 2019, 5(8), 1205-1214.
[http://dx.doi.org/10.1001/jamaoncol.2018.7147] [PMID: 30973611]
[3]
Dirix, L.Y.; Takacs, I.; Jerusalem, G.; Nikolinakos, P.; Arkenau, H.T.; Forero-Torres, A.; Boccia, R.; Lippman, M.E.; Somer, R.; Smakal, M.; Emens, L.A.; Hrinczenko, B.; Edenfield, W.; Gurtler, J.; von Heydebreck, A.; Grote, H.J.; Chin, K.; Hamilton, E.P. Avelumab, an anti-PD-L1 antibody, in patients with locally advanced or metastatic breast cancer: A phase 1b JAVELIN solid tumor study. Breast Cancer Res. Treat., 2018, 167(3), 671-686.
[http://dx.doi.org/10.1007/s10549-017-4537-5] [PMID: 29063313]
[4]
Rugo, H.S.; Delord, J.P.; Im, S.A.; Ott, P.A.; Piha-Paul, S.A.; Bedard, P.L.; Sachdev, J.; Le Tourneau, C.; van Brummelen, E.M.J.; Varga, A.; Salgado, R.; Loi, S.; Saraf, S.; Pietrangelo, D.; Karantza, V.; Tan, A.R. Safety and antitumor activity of pembrolizumab in patients with estrogen receptor-positive/human epidermal growth factor receptor 2-negative advanced breast cancer. Clin. Cancer Res., 2018, 24(12), 2804-2811.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-3452] [PMID: 29559561]
[5]
DeSantis, C.E.; Ma, J.; Gaudet, M.M.; Newman, L.A.; Miller, K.D.; Goding Sauer, A.; Jemal, A.; Siegel, R.L. Breast cancer statistics, 2019. CA Cancer J. Clin., 2019, 69(6), 438-451.
[http://dx.doi.org/10.3322/caac.21583] [PMID: 31577379]
[6]
Waks, A.G.; Stover, D.G.; Guerriero, J.L.; Dillon, D.; Barry, W.T.; Gjini, E.; Hartl, C.; Lo, W.; Savoie, J.; Brock, J.; Wesolowski, R.; Li, Z.; Damicis, A.; Philips, A.V.; Wu, Y.; Yang, F.; Sullivan, A.; Danaher, P.; Brauer, H.A.; Osmani, W.; Lipschitz, M.; Hoadley, K.A.; Goldberg, M.; Perou, C.M.; Rodig, S.; Winer, E.P.; Krop, I.E.; Mittendorf, E.A.; Tolaney, S.M. The immune microenvironment in hormone receptor-positive breast cancer before and after preoperative chemotherapy. Clin. Cancer Res., 2019, 25(15), 4644-4655.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0173] [PMID: 31061067]
[7]
Nanda, R.; Liu, M.C.; Yau, C.; Shatsky, R.; Pusztai, L.; Wallace, A.; Chien, A.J.; Forero-Torres, A.; Ellis, E.; Han, H.; Clark, A.; Albain, K.; Boughey, J.C.; Jaskowiak, N.T.; Elias, A.; Isaacs, C.; Kemmer, K.; Helsten, T.; Majure, M.; Stringer-Reasor, E.; Parker, C.; Lee, M.C.; Haddad, T.; Cohen, R.N.; Asare, S.; Wilson, A.; Hirst, G.L.; Singhrao, R.; Steeg, K.; Asare, A.; Matthews, J.B.; Berry, S.; Sanil, A.; Schwab, R.; Symmans, W.F.; van ’t Veer, L.; Yee, D.; DeMichele, A.; Hylton, N.M.; Melisko, M.; Perlmutter, J.; Rugo, H.S.; Berry, D.A.; Esserman, L.J. Effect of pembrolizumab plus neoadjuvant chemotherapy on pathologic complete response in women with early-stage breast cancer: An analysis of the ongoing phase 2 adaptively randomized I-SPY2 trial. JAMA Oncol., 2020, 6(5), 676-684.
[http://dx.doi.org/10.1001/jamaoncol.2019.6650] [PMID: 32053137]
[8]
Sella, T.; Weiss, A.; Mittendorf, E.A.; King, T.A.; Pilewskie, M.; Giuliano, A.E.; Metzger-Filho, O. Neoadjuvant endocrine therapy in clinical practice: A review. JAMA Oncol., 2021, 7(11), 1700-1708.
[http://dx.doi.org/10.1001/jamaoncol.2021.2132] [PMID: 34499101]
[9]
Martí, C.; Sánchez-Méndez, J.I. The present and future of neoadjuvant endocrine therapy for breast cancer treatment. Cancers (Basel), 2021, 13(11), 2538.
[http://dx.doi.org/10.3390/cancers13112538] [PMID: 34064183]
[10]
Polanczyk, M.J.; Hopke, C.; Vandenbark, A.A.; Offner, H. Estrogen-mediated immunomodulation involves reduced activation of effector T cells, potentiation of Treg cells, and enhanced expression of the PD-1 costimulatory pathway. J. Neurosci. Res., 2006, 84(2), 370-378.
[http://dx.doi.org/10.1002/jnr.20881] [PMID: 16676326]
[11]
Wang, J.; Zhang, Q.; Jin, S.; Feng, M.; Kang, X.; Zhao, S.; Liu, S.; Zhao, W. Immoderate inhibition of estrogen by anastrozole enhances the severity of experimental polyarthritis. Exp. Gerontol., 2009, 44(6-7), 398-405.
[http://dx.doi.org/10.1016/j.exger.2009.03.003] [PMID: 19298850]
[12]
Leek, J.T.; Johnson, W.E.; Parker, H.S.; Jaffe, A.E.; Storey, J.D. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics, 2012, 28(6), 882-883.
[http://dx.doi.org/10.1093/bioinformatics/bts034] [PMID: 22257669]
[13]
Becht, E.; Giraldo, N.A.; Lacroix, L.; Buttard, B.; Elarouci, N.; Petitprez, F.; Selves, J.; Laurent-Puig, P.; Sautès-Fridman, C.; Fridman, W.H.; de Reyniès, A. Estimating the population abundance of tissue-infiltrating immune and stromal cell populations using gene expression. Genome Biol., 2016, 17(1), 218.
[http://dx.doi.org/10.1186/s13059-016-1070-5] [PMID: 27765066]
[14]
Newman, A.M.; Liu, C.L.; Green, M.R.; Gentles, A.J.; Feng, W.; Xu, Y.; Hoang, C.D.; Diehn, M.; Alizadeh, A.A. Robust enumeration of cell subsets from tissue expression profiles. Nat. Methods, 2015, 12(5), 453-457.
[http://dx.doi.org/10.1038/nmeth.3337] [PMID: 25822800]
[15]
Aran, D.; Hu, Z.; Butte, A.J. xCell: Digitally portraying the tissue cellular heterogeneity landscape. Genome Biol., 2017, 18(1), 220.
[http://dx.doi.org/10.1186/s13059-017-1349-1] [PMID: 29141660]
[16]
Wu, Z.H.; Tang, Y.; Yu, H.; Li, H.D. The role of ferroptosis in breast cancer patients: A comprehensive analysis. Cell Death Discov., 2021, 7(1), 93.
[http://dx.doi.org/10.1038/s41420-021-00473-5] [PMID: 33947836]
[17]
Marin-Acevedo, J.A.; Kimbrough, E.O.; Lou, Y. Next generation of immune checkpoint inhibitors and beyond. J. Hematol. Oncol., 2021, 14(1), 45.
[http://dx.doi.org/10.1186/s13045-021-01056-8] [PMID: 33741032]
[18]
Sharma, P.; Siddiqui, B.A.; Anandhan, S.; Yadav, S.S.; Subudhi, S.K.; Gao, J.; Goswami, S.; Allison, J.P. The next decade of immune checkpoint therapy. Cancer Discov., 2021, 11(4), 838-857.
[http://dx.doi.org/10.1158/2159-8290.CD-20-1680] [PMID: 33811120]
[19]
Subramanian, A.; Tamayo, P.; Mootha, V.K.; Mukherjee, S.; Ebert, B.L.; Gillette, M.A.; Paulovich, A.; Pomeroy, S.L.; Golub, T.R.; Lander, E.S.; Mesirov, J.P. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA, 2005, 102(43), 15545-15550.
[http://dx.doi.org/10.1073/pnas.0506580102] [PMID: 16199517]
[20]
Ritchie, M.E.; Phipson, B.; Wu, D.; Hu, Y.; Law, C.W.; Shi, W.; Smyth, G.K. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 2015, 43(7), e47.
[http://dx.doi.org/10.1093/nar/gkv007] [PMID: 25605792]
[21]
Parker, J.S.; Mullins, M.; Cheang, M.C.; Leung, S.; Voduc, D.; Vickery, T.; Davies, S.; Fauron, C.; He, X.; Hu, Z.; Quackenbush, J.F.; Stijleman, I.J.; Palazzo, J.; Marron, J.S.; Nobel, A.B.; Mardis, E.; Nielsen, T.O.; Ellis, M.J.; Perou, C.M.; Bernard, P.S. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol., 2009, 27(8), 1160-1167.
[http://dx.doi.org/10.1200/JCO.2008.18.1370] [PMID: 19204204]
[22]
Yamazaki, T.; Buqué, A.; Ames, T.D.; Galluzzi, L. PT-112 induces immunogenic cell death and synergizes with immune checkpoint blockers in mouse tumor models. OncoImmunology, 2020, 9(1), 1721810.
[http://dx.doi.org/10.1080/2162402X.2020.1721810] [PMID: 32117585]
[23]
Pfirschke, C.; Engblom, C.; Rickelt, S.; Cortez-Retamozo, V.; Garris, C.; Pucci, F.; Yamazaki, T.; Poirier-Colame, V.; Newton, A.; Redouane, Y.; Lin, Y.J.; Wojtkiewicz, G.; Iwamoto, Y.; Mino-Kenudson, M.; Huynh, T.G.; Hynes, R.O.; Freeman, G.J.; Kroemer, G.; Zitvogel, L.; Weissleder, R.; Pittet, M.J. Immunogenic chemotherapy sensitizes tumors to checkpoint blockade therapy. Immunity, 2016, 44(2), 343-354.
[http://dx.doi.org/10.1016/j.immuni.2015.11.024] [PMID: 26872698]
[24]
Generali, D.; Bates, G.; Berruti, A.; Brizzi, M.P.; Campo, L.; Bonardi, S.; Bersiga, A.; Allevi, G.; Milani, M.; Aguggini, S.; Dogliotti, L.; Banham, A.H.; Harris, A.L.; Bottini, A.; Fox, S.B. Immunomodulation of FOXP3+ regulatory T cells by the aromatase inhibitor letrozole in breast cancer patients. Clin. Cancer Res., 2009, 15(3), 1046-1051.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1507] [PMID: 19188178]
[25]
Chan, M.S.; Wang, L.; Felizola, S.J.; Ueno, T.; Toi, M.; Loo, W.; Chow, L.W.; Suzuki, T.; Sasano, H. Changes of tumor infiltrating lymphocyte subtypes before and after neoadjuvant endocrine therapy in estrogen receptor-positive breast cancer patients--an immunohistochemical study of Cd8+ and Foxp3+ using double immunostaining with correlation to the pathobiological response of the patients. Int. J. Biol. Markers, 2012, 27(4), e295-e304.
[http://dx.doi.org/10.5301/JBM.2012.10439] [PMID: 23280127]
[26]
Mello-Grand, M.; Singh, V.; Ghimenti, C.; Scatolini, M.; Regolo, L.; Grosso, E.; Zambelli, A.; Da Prada, G.A.; Villani, L.; Fregoni, V.; Baiardi, P.; Marsoni, S.; Miller, W.R.; Costa, A.; Chiorino, G. Gene expression profiling and prediction of response to hormonal neoadjuvant treatment with anastrozole in surgically resectable breast cancer. Breast Cancer Res. Treat., 2010, 121(2), 399-411.
[http://dx.doi.org/10.1007/s10549-010-0887-y] [PMID: 20428938]
[27]
Wajant, H.; Pfizenmaier, K.; Scheurich, P. Tumor necrosis factor signaling. Cell Death Differ., 2003, 10(1), 45-65.
[http://dx.doi.org/10.1038/sj.cdd.4401189] [PMID: 12655295]
[28]
Walport, M.J. Complement. First of two parts. N. Engl. J. Med., 2001, 344(14), 1058-1066.
[http://dx.doi.org/10.1056/NEJM200104053441406] [PMID: 11287977]
[29]
Boehm, U.; Klamp, T.; Groot, M.; Howard, J.C. Cellular responses to interferon-gamma. Annu. Rev. Immunol., 1997, 15(1), 749-795.
[http://dx.doi.org/10.1146/annurev.immunol.15.1.749] [PMID: 9143706]
[30]
Denkert, C.; von Minckwitz, G.; Darb-Esfahani, S.; Lederer, B.; Heppner, B.I.; Weber, K.E.; Budczies, J.; Huober, J.; Klauschen, F.; Furlanetto, J.; Schmitt, W.D.; Blohmer, J.U.; Karn, T.; Pfitzner, B.M.; Kümmel, S.; Engels, K.; Schneeweiss, A.; Hartmann, A.; Noske, A.; Fasching, P.A.; Jackisch, C.; van Mackelenbergh, M.; Sinn, P.; Schem, C.; Hanusch, C.; Untch, M.; Loibl, S. 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.
[http://dx.doi.org/10.1016/S1470-2045(17)30904-X] [PMID: 29233559]
[31]
Schmid, P.; Adams, S.; Rugo, H.S.; Schneeweiss, A.; Barrios, C.H.; Iwata, H.; Diéras, V.; Hegg, R. Im, S.A.; Shaw Wright, G.; Henschel, V.; Molinero, L.; Chui, S.Y.; Funke, R.; Husain, A.; Winer, E.P.; Loi, S.; Emens, L.A. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N. Engl. J. Med., 2018, 379(22), 2108-2121.
[http://dx.doi.org/10.1056/NEJMoa1809615] [PMID: 30345906]
[32]
Mittendorf, E.A.; Zhang, H.; Barrios, C.H.; Saji, S.; Jung, K.H.; Hegg, R.; Koehler, A.; Sohn, J.; Iwata, H.; Telli, M.L.; Ferrario, C.; Punie, K.; Penault-Llorca, F.; Patel, S.; Duc, A.N.; Liste-Hermoso, M.; Maiya, V.; Molinero, L.; Chui, S.Y.; Harbeck, N. Neoadjuvant atezolizumab in combination with sequential nab-paclitaxel and anthracycline-based chemotherapy versus placebo and chemotherapy in patients with early-stage triple-negative breast cancer (IMpassion031): A randomised, double-blind, phase 3 trial. Lancet, 2020, 396(10257), 1090-1100.
[http://dx.doi.org/10.1016/S0140-6736(20)31953-X] [PMID: 32966830]
[33]
Schmid, P.; Cortes, J.; Pusztai, L.; McArthur, H.; Kümmel, S.; Bergh, J.; Denkert, C.; Park, Y.H.; Hui, R.; Harbeck, N.; Takahashi, M.; Foukakis, T.; Fasching, P.A.; Cardoso, F.; Untch, M.; Jia, L.; Karantza, V.; Zhao, J.; Aktan, G.; Dent, R.; O’Shaughnessy, J. Pembrolizumab for early triple-negative breast cancer. N. Engl. J. Med., 2020, 382(9), 810-821.
[http://dx.doi.org/10.1056/NEJMoa1910549] [PMID: 32101663]
[34]
Dieci, M.V.; Griguolo, G.; Miglietta, F.; Guarneri, V. The immune system and hormone-receptor positive breast cancer: Is it really a dead end? Cancer Treat. Rev., 2016, 46, 9-19.
[http://dx.doi.org/10.1016/j.ctrv.2016.03.011] [PMID: 27055087]
[35]
Muenst, S.; Schaerli, A.R.; Gao, F.; Däster, S.; Trella, E.; Droeser, R.A.; Muraro, M.G.; Zajac, P.; Zanetti, R.; Gillanders, W.E.; Weber, W.P.; Soysal, S.D. Expression of programmed death ligand 1 (PD-L1) is associated with poor prognosis in human breast cancer. Breast Cancer Res. Treat., 2014, 146(1), 15-24.
[http://dx.doi.org/10.1007/s10549-014-2988-5] [PMID: 24842267]
[36]
Ghebeh, H.; Mohammed, S.; Al-Omair, A.; Qattan, A.; Lehe, C.; Al-Qudaihi, G.; Elkum, N.; Alshabanah, M.; Bin Amer, S.; Tulbah, A.; Ajarim, D.; Al-Tweigeri, T.; Dermime, S. The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: Correlation with important high-risk prognostic factors. Neoplasia, 2006, 8(3), 190-198.
[http://dx.doi.org/10.1593/neo.05733] [PMID: 16611412]
[37]
Park, S.J.; Ye, W.; Xiao, R.; Silvin, C.; Padget, M.; Hodge, J.W.; Van Waes, C.; Schmitt, N.C. Cisplatin and oxaliplatin induce similar immunogenic changes in preclinical models of head and neck cancer. Oral Oncol., 2019, 95, 127-135.
[http://dx.doi.org/10.1016/j.oraloncology.2019.06.016] [PMID: 31345380]
[38]
Wu, Y.; Deng, Z.; Wang, H.; Ma, W.; Zhou, C.; Zhang, S. Repeated cycles of 5-fluorouracil chemotherapy impaired anti-tumor functions of cytotoxic T cells in a CT26 tumor-bearing mouse model. BMC Immunol., 2016, 17(1), 29.
[http://dx.doi.org/10.1186/s12865-016-0167-7] [PMID: 27645787]
[39]
Peng, J.; Hamanishi, J.; Matsumura, N.; Abiko, K.; Murat, K.; Baba, T.; Yamaguchi, K.; Horikawa, N.; Hosoe, Y.; Murphy, S.K.; Konishi, I.; Mandai, M. Chemotherapy induces programmed cell death-ligand 1 overexpression via the nuclear factor-κB to foster an immunosuppressive tumor microenvironment in ovarian cancer. Cancer Res., 2015, 75(23), 5034-5045.
[http://dx.doi.org/10.1158/0008-5472.CAN-14-3098] [PMID: 26573793]
[40]
Voorwerk, L.; Slagter, M.; Horlings, H.M.; Sikorska, K.; van de Vijver, K.K.; de Maaker, M.; Nederlof, I.; Kluin, R.J.C.; Warren, S.; Ong, S.; Wiersma, T.G.; Russell, N.S.; Lalezari, F.; Schouten, P.C.; Bakker, N.A.M.; Ketelaars, S.L.C.; Peters, D.; Lange, C.A.H.; van Werkhoven, E.; van Tinteren, H.; Mandjes, I.A.M.; Kemper, I.; Onderwater, S.; Chalabi, M.; Wilgenhof, S.; Haanen, J.B.A.G.; Salgado, R.; de Visser, K.E.; Sonke, G.S.; Wessels, L.F.A.; Linn, S.C.; Schumacher, T.N.; Blank, C.U.; Kok, M. Immune induction strategies in metastatic triple-negative breast cancer to enhance the sensitivity to PD-1 blockade: The TONIC trial. Nat. Med., 2019, 25(6), 920-928.
[http://dx.doi.org/10.1038/s41591-019-0432-4] [PMID: 31086347]
[41]
Otsubo, D.; Yamashita, K.; Fujita, M.; Nishi, M.; Kimura, Y.; Hasegawa, H.; Suzuki, S.; Kakeji, Y. Early-phase treatment by low-dose 5-fluorouracil or primary tumor resection inhibits MDSC-mediated lung metastasis formation. Anticancer Res., 2015, 35(8), 4425-4431.
[PMID: 26168482]
[42]
Dimeloe, S.; Frick, C.; Fischer, M.; Gubser, P.M.; Razik, L.; Bantug, G.R.; Ravon, M.; Langenkamp, A.; Hess, C. Human regulatory T cells lack the cyclophosphamide-extruding transporter ABCB1 and are more susceptible to cyclophosphamide-induced apoptosis. Eur. J. Immunol., 2014, 44(12), 3614-3620.
[http://dx.doi.org/10.1002/eji.201444879] [PMID: 25251877]
[43]
Ma, Y.; Mattarollo, S.R.; Adjemian, S.; Yang, H.; Aymeric, L.; Hannani, D.; Portela Catani, J.P.; Duret, H.; Teng, M.W.; Kepp, O.; Wang, Y.; Sistigu, A.; Schultze, J.L.; Stoll, G.; Galluzzi, L.; Zitvogel, L.; Smyth, M.J.; Kroemer, G. CCL2/CCR2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res., 2014, 74(2), 436-445.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-1265] [PMID: 24302580]
[44]
Wanderley, C.W.; Colón, D.F.; Luiz, J.P.M.; Oliveira, F.F.; Viacava, P.R.; Leite, C.A.; Pereira, J.A.; Silva, C.M.; Silva, C.R.; Silva, R.L.; Speck-Hernandez, C.A.; Mota, J.M.; Alves-Filho, J.C.; Lima-Junior, R.C.; Cunha, T.M.; Cunha, F.Q. Paclitaxel reduces tumor growth by reprogramming tumor-associated macrophages to an M1 profile in a TLR4-Dependent manner. Cancer Res., 2018, 78(20), 5891-5900.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-3480] [PMID: 30104241]
[45]
Schaer, D.A.; Geeganage, S.; Amaladas, N.; Lu, Z.H.; Rasmussen, E.R.; Sonyi, A.; Chin, D.; Capen, A.; Li, Y.; Meyer, C.M.; Jones, B.D.; Huang, X.; Luo, S.; Carpenito, C.; Roth, K.D.; Nikolayev, A.; Tan, B.; Brahmachary, M.; Chodavarapu, K.; Dorsey, F.C.; Manro, J.R.; Doman, T.N.; Donoho, G.P.; Surguladze, D.; Hall, G.E.; Kalos, M.; Novosiadly, R.D. The folate pathway inhibitor pemetrexed pleiotropically enhances effects of cancer immunotherapy. Clin. Cancer Res., 2019, 25(23), 7175-7188.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-0433] [PMID: 31409612]
[46]
Buhtoiarov, I.N.; Sondel, P.M.; Wigginton, J.M.; Buhtoiarova, T.N.; Yanke, E.M.; Mahvi, D.A.; Rakhmilevich, A.L. Anti-tumour synergy of cytotoxic chemotherapy and anti-CD40 plus CpG-ODN immunotherapy through repolarization of tumour-associated macrophages. Immunology, 2011, 132(2), 226-239.
[http://dx.doi.org/10.1111/j.1365-2567.2010.03357.x] [PMID: 21039467]
[47]
Xiao, Y.; Ma, D.; Zhao, S.; Suo, C.; Shi, J.; Xue, M.Z.; Ruan, M.; Wang, H.; Zhao, J.; Li, Q.; Wang, P.; Shi, L.; Yang, W.T.; Huang, W.; Hu, X.; Yu, K.D.; Huang, S.; Bertucci, F.; Jiang, Y.Z.; Shao, Z.M. Multi-Omics profiling reveals distinct microenvironment characterization and suggests immune escape mechanisms of triple-negative breast cancer. Clin. Cancer Res., 2019, 25(16), 5002-5014.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-3524] [PMID: 30837276]
[48]
Spranger, S. Mechanisms of tumor escape in the context of the T-cell-inflamed and the non-T-cell-inflamed tumor microenvironment. Int. Immunol., 2016, 28(8), 383-391.
[http://dx.doi.org/10.1093/intimm/dxw014] [PMID: 26989092]
[49]
Bi, M.; Zhang, Z.; Jiang, Y.Z.; Xue, P.; Wang, H.; Lai, Z.; Fu, X.; De Angelis, C.; Gong, Y.; Gao, Z.; Ruan, J.; Jin, V.X.; Marangoni, E.; Montaudon, E.; Glass, C.K.; Li, W.; Huang, T.H.; Shao, Z.M.; Schiff, R.; Chen, L.; Liu, Z. Enhancer reprogramming driven by high-order assemblies of transcription factors promotes phenotypic plasticity and breast cancer endocrine resistance. Nat. Cell Biol., 2020, 22(6), 701-715.
[http://dx.doi.org/10.1038/s41556-020-0514-z] [PMID: 32424275]
[50]
Vonderheide, R.H.; LoRusso, P.M.; Khalil, M.; Gartner, E.M.; Khaira, D.; Soulieres, D.; Dorazio, P.; Trosko, J.A.; Rüter, J.; Mariani, G.L.; Usari, T.; Domchek, S.M. 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), 3485-3494.
[http://dx.doi.org/10.1158/1078-0432.CCR-10-0505] [PMID: 20479064]
[51]
Whitworth, P.; Beitsch, P.; Mislowsky, A.; Pellicane, J.V.; Nash, C.; Murray, M.; Lee, L.A.; Dul, C.L.; Rotkis, M.; Baron, P.; Stork-Sloots, L.; de Snoo, F.A.; Beatty, J. Chemosensitivity and endocrine sensitivity in clinical luminal breast cancer patients in the prospective neoadjuvant breast registry symphony trial (NBRST) predicted by molecular subtyping. Ann. Surg. Oncol., 2017, 24(3), 669-675.
[http://dx.doi.org/10.1245/s10434-016-5600-x] [PMID: 27770345]
[52]
Iwata, H.; Masuda, N.; Yamamoto, Y.; Fujisawa, T.; Toyama, T.; Kashiwaba, M.; Ohtani, S.; Taira, N.; Sakai, T.; Hasegawa, Y.; Nakamura, R.; Akabane, H.; Shibahara, Y.; Sasano, H.; Yamaguchi, T.; Sakamaki, K.; Bailey, H.; Cherbavaz, D.B.; Jakubowski, D.M.; Sugiyama, N.; Chao, C.; Ohashi, Y. Validation of the 21-gene test as a predictor of clinical response to neoadjuvant hormonal therapy for ER+, HER2-negative breast cancer: The TransNEOS study. Breast Cancer Res. Treat., 2019, 173(1), 123-133.
[http://dx.doi.org/10.1007/s10549-018-4964-y] [PMID: 30242578]
[53]
Turnbull, A.K.; Arthur, L.M.; Renshaw, L.; Larionov, A.A.; Kay, C.; Dunbier, A.K.; Thomas, J.S.; Dowsett, M.; Sims, A.H.; Dixon, J.M. Accurate prediction and validation of response to endocrine therapy in breast cancer. J. Clin. Oncol., 2015, 33(20), 2270-2278.
[http://dx.doi.org/10.1200/JCO.2014.57.8963] [PMID: 26033813]

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