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Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Review Article

Immunotherapy in Breast Cancer Patients: A Focus on the Use of the Currently Available Biomarkers in Oncology

Author(s): Carmen Criscitiello, Elena Guerini-Rocco, Giulia Viale, Caterina Fumagalli, Elham Sajjadi, Konstantinos Venetis, Roberto Piciotti, Marco Invernizzi, Umberto Malapelle and Nicola Fusco*

Volume 22, Issue 4, 2022

Published on: 13 August, 2021

Page: [787 - 800] Pages: 14

DOI: 10.2174/1871520621666210706144112

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Abstract

Immune Checkpoint Inhibitors (ICIs) have remarkably modified the way solid tumors are managed, including breast cancer. Unfortunately, only a relatively small number of breast cancer patients significantly respond to these treatments. To maximize the immunotherapy benefit in breast cancer, several efforts are currently being put forward for the identification of i) the best therapeutic strategy (i.e. ICI monotherapy or in association with chemotherapy, radiotherapy, or other drugs); ii) optimal timing for administration (e.g. early/advanced stage of disease; adjuvant/ neoadjuvant setting); iii) most effective and reliable predictive biomarkers of response (e.g. tumor-infiltrating lymphocytes, programmed death-ligand 1, microsatellite instability associated with mismatch repair deficiency, and tumor mutational burden). In this article, we review the impacts and gaps in the characterization of immune-related biomarkers raised by clinical and translational research studies with immunotherapy treatments. Particular emphasis has been put on the documented evidence of significant clinical benefits of ICI in different randomized clinical trials, along with preanalytical and analytical issues in predictive biomarkers pathological assessment.

Keywords: Breast cancer, biomarkers, immunotherapy, TILs, PD-L1, mismatch repair, microsatellite instability, tumor mutational burden.

Graphical Abstract
[1]
Ribas, A.; Wolchok, J.D. Cancer immunotherapy using checkpoint blockade. Science, 2018, 359(6382), 1350-1355.
[http://dx.doi.org/10.1126/science.aar4060]
[2]
Pusztai, L.; Karn, T.; Safonov, A.; Abu-Khalaf, M.M.; Bianchini, G. New strategies in breast cancer: immunotherapy. Clin. Cancer Res., 2016, 22(9), 2105-2110.
[3]
Criscitiello, C.; Curigliano, G. Immunotherapy of breast cancer. Prog. Tumor Res., 2015, 42, 30-43.
[http://dx.doi.org/10.1159/000437183]
[4]
Pagni, F.; Guerini-Rocco, E.; Schultheis, A.M.; Grazia, G.; Rijavec, E.; Ghidini, M.; Lopez, G.; Venetis, K.; Croci, G.A.; Malapelle, U.; Fusco, N. targeting immune-related biological processes in solid tumors: we do need biomarkers. Int. J. Mol. Sci., 2019, 20(21)E5452
[http://dx.doi.org/10.3390/ijms20215452]
[5]
Barroso-Sousa, R.; Tolaney, S.M. Clinical development of PD-1/PD-L1 inhibitors in breast cancer: still a long way to go. Curr. Treat. Options Oncol., 2020, 21(7), 59.
[http://dx.doi.org/10.1007/s11864-020-00756-6]
[6]
Venetis, K.; Invernizzi, M.; Sajjadi, E.; Curigliano, G.; Fusco, N. Cellular immunotherapy in breast cancer: the quest for consistent biomarkers. Cancer Treat. Rev., 2020, 90102089
[http://dx.doi.org/10.1016/j.ctrv.2020.102089]
[7]
Napolitano, M.; Schipilliti, F.M.; Trudu, L.; Bertolini, F. Immunotherapy in head and neck cancer: the great challenge of patient selection. Crit. Rev. Oncol. Hematol., 2019, 144102829
[http://dx.doi.org/10.1016/j.critrevonc.2019.102829]
[8]
Signorelli, D.; Giannatempo, P.; Grazia, G.; Aiello, M.M.; Bertolini, F.; Mirabile, A.; Buti, S.; Vasile, E.; Scotti, V.; Pisapia, P.; Cona, M.S.; Rolfo, C.; Malapelle, U. Patients selection for immunotherapy in solid tumors: overcome the naïve vision of a single biomarker. BioMed Res. Int., 2019, 20199056417
[http://dx.doi.org/10.1155/2019/9056417]
[9]
Lopez, G.; Noale, M.; Corti, C.; Gaudioso, G.; Sajjadi, E.; Venetis, K.; Gambini, D.; Runza, L.; Costanza, J.; Pesenti, C.; Grossi, F.; Maggi, S.; Ferrero, S.; Bosari, S.; Fusco, N. PTEN expression as a complementary biomarker for mismatch repair testing in breast cancer. Int. J. Mol. Sci., 2020, 21(4)E1461
[http://dx.doi.org/10.3390/ijms21041461]
[10]
Fusco, N.; Sajjadi, E.; Venetis, K.; Gaudioso, G.; Lopez, G.; Corti, C.; Rocco, E.G.; Criscitiello, C.; Malapelle, U.; Invernizzi, M. PTEN alterations and their role in cancer management: are we making headway on precision medicine? Genes (Basel), 2020, 11(7), 719.
[http://dx.doi.org/10.3390/genes11070719]
[11]
Malone, E.R.; Oliva, M.; Sabatini, P.J.B.; Stockley, T.L.; Siu, L.L. Molecular profiling for precision cancer therapies. Genome Med., 2020, 12(1), 8.
[http://dx.doi.org/10.1186/s13073-019-0703-1]
[12]
Peng, Z.; Su, P.; Yang, Y.; Yao, X.; Zhang, Y.; Jin, F.; Yang, B. Identification of CTLA-4 associated with tumor microenvironment and competing interactions in triple negative breast cancer by co-expression network analysis. J. Cancer, 2020, 11(21), 6365-6375.
[http://dx.doi.org/10.7150/jca.46301]
[13]
Navarrete-Bernal, M.G.C.; Cervantes-Badillo, M.G.; Martínez-Herrera, J.F.; Lara-Torres, C.O.; Gerson-Cwilich, R.; Zentella-Dehesa, A.; Ibarra-Sánchez, M.J.; Esparza-López, J.; Montesinos, J.J.; Cortés-Morales, V.A.; Osorio-Pérez, D.; Villegas-Osorno, D.A.; Reyes-Sánchez, E.; Salazar-Sojo, P.; Tallabs-Utrilla, L.F.; Romero-Córdoba, S.; Rocha-Zavaleta, L. Biological landscape of triple negative breast cancers expressing CTLA-4. Front. Oncol., 2020, 10, 1206-1206.
[http://dx.doi.org/10.3389/fonc.2020.01206]
[14]
Kassardjian, A.; Shintaku, P.I.; Moatamed, N.A. Expression of immune checkpoint regulators, Cytotoxic T Lymphocyte Antigen 4 (CTLA-4) and Programmed Death-Ligand 1 (PD-L1), in female breast carcinomas. PLoS One, 2018, 13(4)e0195958
[http://dx.doi.org/10.1371/journal.pone.0195958]
[15]
Larkin, J.; Chiarion-Sileni, V.; Gonzalez, R.; Grob, J.J.; Cowey, C.L.; Lao, C.D.; Schadendorf, D.; Dummer, R.; Smylie, M.; Rutkowski, P.; Ferrucci, P.F.; Hill, A.; Wagstaff, J.; Carlino, M.S.; Haanen, J.B.; Maio, M.; Marquez-Rodas, I.; McArthur, G.A.; Ascierto, P.A.; Long, G.V.; Callahan, M.K.; Postow, M.A.; Grossmann, K.; Sznol, M.; Dreno, B.; Bastholt, L.; Yang, A.; Rollin, L.M.; Horak, C.; Hodi, F.S.; Wolchok, J.D. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med., 2015, 373(1), 23-34.
[http://dx.doi.org/10.1056/NEJMoa1504030]
[16]
Santabarbara, G.; Maione, P.; Rossi, A.; Palazzolo, G.; Gridelli, C. Novel immunotherapy in the treatment of advanced non-small cell lung cancer. Expert Rev. Clin. Pharmacol., 2016, 9(12), 1571-1581.
[http://dx.doi.org/10.1080/17512433.2016.1236681]
[17]
Leal, H.S.H.M. Breast cancer immunotherapy: from biology to current clinical applications. Eur. Med. J., 2020, 5(2), 113-124.
[18]
Nanda, R.; Chow, L.Q.; 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]
[19]
Adams, S.; Schmid, P.; Rugo, H.S.; Winer, E.P.; Loirat, D.; Awada, A.; Cescon, D.W.; Iwata, H.; Campone, M.; Nanda, R.; Hui, R.; Curigliano, G.; Toppmeyer, D.; O’Shaughnessy, J.; Loi, S.; Paluch-Shimon, S.; Tan, A.R.; Card, D.; Zhao, J.; Karantza, V.; Cortes, J. Pembrolizumab monotherapy for previously treated metastatic triple-negative breast cancer: cohort A of the phase II KEYNOTE-086 study. Ann. Oncol., 2019, 30(3), 397-404.
[20]
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.; Rugo, H.S.; Tan, A.R.; Jia, L.; Ding, Y.; Karantza, V.; Schmid, P. Pembrolizumab monotherapy for previously untreated, PD-L1-positive, metastatic triple-negative breast cancer: cohort B of the phase II KEYNOTE-086 study. Ann. Oncol., 2019, 30(3), 405-411.
[http://dx.doi.org/10.1093/annonc/mdy518]
[21]
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: a Phase 1 study. JAMA Oncol., 2019, 5(1), 74-82.
[http://dx.doi.org/10.1001/jamaoncol.2018.4224]
[22]
Cyprian, F.S.; Akhtar, S.; Gatalica, Z.; Vranic, S. Targeted immunotherapy with a checkpoint inhibitor in combination with chemotherapy: a new clinical paradigm in the treatment of triple-negative breast cancer. Bosn. J. Basic Med. Sci., 2019, 19(3), 227-233.
[http://dx.doi.org/10.17305/bjbms.2019.4204]
[23]
Marra, A.; Trapani, D.; Viale, G.; Criscitiello, C.; Curigliano, G. Practical classification of triple-negative breast cancer: intratumoral heterogeneity, mechanisms of drug resistance, and novel therapies. NPJ Breast Cancer, 2020, 6, 54.
[http://dx.doi.org/10.1038/s41523-020-00197-2]
[24]
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]
[25]
Schmid, P.; Rugo, H.S.; Adams, S.; Schneeweiss, A.; Barrios, C.H.; Iwata, H.; Diéras, V.; Henschel, V.; Molinero, L.; Chui, S.Y.; Maiya, V.; Husain, A.; Winer, E.P.; Loi, S.; Emens, L.A. Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol., 2020, 21(1), 44-59.
[http://dx.doi.org/10.1016/S1470-2045(19)30689-8]
[26]
Dent, R.; Andre, F.; Goncalves, A.; Kummel, S.; Martin, M.; Schmid, P.; Schuetz, F.; Swain, S.M.; Easton, V.; Pollex, E.; Cortés, J. 2018.
[27]
Cortés, J.; André, F.; Gonçalves, A.; Kümmel, S.; Martín, M.; Schmid, P.; Schuetz, F.; Swain, S.M.; Easton, V.; Pollex, E.; Deurloo, R.; Dent, R. IMpassion132 Phase III trial: atezolizumab and chemotherapy in early relapsing metastatic triple-negative breast cancer. Future Oncol., 2019, 15(17), 1951-1961.
[http://dx.doi.org/10.2217/fon-2019-0059]
[28]
Cortes, J.; Cescon, D.W.; Rugo, H.S.; Nowecki, Z. Im, S.A.; Yusof, M.M.; Gallardo, C.; Lipatov, O.; Barrios, C.H.; Holgado, E.; Iwata, H.; Masuda, N.; Otero, M.T.; Gokmen, E.; Loi, S.; Guo, Z.; Zhao, J.; Aktan, G.; Karantza, V.; Schmid, P. 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), 1817-1828.
[http://dx.doi.org/10.1016/S0140-6736(20)32531-9]
[29]
Kulangara, K.; Zhang, N.; Corigliano, E.; Guerrero, L.; Waldroup, S.; Jaiswal, D.; Ms, M.J.; Shah, S.; Hanks, D.; Wang, J.; Lunceford, J.; Savage, M.J.; Juco, J.; Emancipator, K. Clinical utility of the combined positive score for programmed death ligand-1 expression and the approval of pembrolizumab for treatment of gastric cancer. Arch. Pathol. Lab. Med., 2019, 143(3), 330-337.
[http://dx.doi.org/10.5858/arpa.2018-0043-OA]
[30]
Ogiya, R.; Niikura, N.; Kumaki, N.; Bianchini, G.; Kitano, S.; Iwamoto, T.; Hayashi, N.; Yokoyama, K.; Oshitanai, R.; Terao, M.; Morioka, T.; Tsuda, B.; Okamura, T.; Saito, Y.; Suzuki, Y.; Tokuda, Y. Comparison of tumor-infiltrating lymphocytes between primary and metastatic tumors in breast cancer patients. Cancer Sci., 2016, 107(12), 1730-1735.
[http://dx.doi.org/10.1111/cas.13101]
[31]
Luen, S.J.; Salgado, R.; Fox, S.; Savas, P.; Eng-Wong, J.; Clark, E.; Kiermaier, A.; Swain, S.M.; Baselga, J.; Michiels, S.; Loi, S. Tumour-infiltrating lymphocytes in advanced HER2-positive breast cancer treated with pertuzumab or placebo in addition to trastuzumab and docetaxel: a retrospective analysis of the CLEOPATRA study. Lancet Oncol., 2017, 18(1), 52-62.
[http://dx.doi.org/10.1016/S1470-2045(16)30631-3]
[32]
Dieci, M.V.; Tsvetkova, V.; Orvieto, E.; Piacentini, F.; Ficarra, G.; Griguolo, G.; Miglietta, F.; Giarratano, T.; Omarini, C.; Bonaguro, S.; Cappellesso, R.; Aliberti, C.; Vernaci, G.; Giorgi, C.A.; Faggioni, G.; Tasca, G.; Conte, P.; Guarneri, V. Immune characterization of breast cancer metastases: prognostic implications. Breast Cancer Res., 2018, 20(1), 62.
[http://dx.doi.org/10.1186/s13058-018-1003-1]
[33]
Szekely, B.; Bossuyt, V.; Li, X.; Wali, V.B.; Patwardhan, G.A.; Frederick, C.; Silber, A.; Park, T.; Harigopal, M.; Pelekanou, V.; Zhang, M.; Yan, Q.; Rimm, D.L.; Bianchini, G.; Hatzis, C.; Pusztai, L. Immunological differences between primary and metastatic breast cancer. Ann. Oncol., 2018, 29(11), 2232-2239.
[34]
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]
[35]
Loibl, S.; Untch, M.; Burchardi, N.; Huober, J.; Sinn, B.V.; Blohmer, J.U.; Grischke, E.M.; Furlanetto, J.; Tesch, H.; Hanusch, C.; Engels, K.; Rezai, M.; Jackisch, C.; Schmitt, W.D.; von Minckwitz, G.; Thomalla, J.; Kümmel, S.; Rautenberg, B.; Fasching, P.A.; Weber, K.; Rhiem, K.; Denkert, C.; Schneeweiss, A. A randomised phase II study investigating durvalumab in addition to an anthracycline taxane-based neoadjuvant therapy in early triple-negative breast cancer: clinical results and biomarker analysis of GeparNuevo study. Ann. Oncol., 2019, 30(8), 1279-1288.
[http://dx.doi.org/10.1093/annonc/mdz158]
[36]
Gianni, L.; Huang, C-S.; Egle, D.; Bermejo, B.; Zamagni, C.; Thill, M.; Anton, A.; Zambelli, S.; Bianchini, G.; Russo, S.; Ciruelos, E.; Greil, R.; Semiglazov, V.; Colleoni, M.; Kelly, C.; Mariani, G.; Mastro, L.D.; Maffeis, I.; Valagussa, P.; Viale, G. Abstract GS3-04: Pathologic Complete Response (pCR) to neoadjuvant treatment with or without atezolizumab in triple negative, early high-risk and locally advanced breast cancer. NeoTRIPaPDL1 Michelangelo randomized study. Cancer Res., 2020, 80(4)(Suppl.), GS3-GS04.
[37]
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]
[38]
Rugo, H.S.; Delord, J.P. 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.
[39]
Tolaney, S.M.; Barroso-Sousa, R.; Keenan, T.; Trippa, L.; Hu, J.; Luis, I.M.V.D.; Wulf, G.M.; Spring, L.; Sinclair, N.F.; Andrews, C.; Pittenger, J.D.; Richardson, E.T.; Dillon, D.; Lin, N.U.; Overmoyer, B.; Partridge, A.H.; VanAllen, E.; Mittendorf, E.A.; Winer, E.P.; Krop, I.E. Randomized phase II study of Eribulin mesylate (E) with or without Pembrolizumab (P) for Hormone Receptor-positive (HR plus) Metastatic Breast Cancer (MBC). J. Clin. Oncol., 2019, 37(15), 1004.
[40]
Goel, S.; DeCristo, M.J.; Watt, A.C. BrinJones, H.; Sceneay, J.; Li, B.B.; Khan, N.; Ubellacker, J.M.; Xie, S.; Metzger-Filho, O.; Hoog, J.; Ellis, M.J.; Ma, C.X.; Ramm, S.; Krop, I.E.; Winer, E.P.; Roberts, T.M.; Kim, H.J.; McAllister, S.S.; Zhao, J.J. CDK4/6 inhibition triggers anti-tumour immunity. Nature, 2017, 548(7668), 471-475.
[http://dx.doi.org/10.1038/nature23465]
[41]
Rugo, H.S.; Kabos, P.; Beck, J.T.; Chisamore, M.J.; Hossain, A.; Chen, Y.; Tolaney, S.M. 2020.
[42]
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]
[43]
Emens, L.A.; Esteva, F.J.; Beresford, M.; Saura, C.; De Laurentiis, M.; Kim, S.B.; Im, S.A.; Wang, Y.; Salgado, R.; Mani, A.; Shah, J.; Lambertini, C.; Liu, H.; de Haas, S.L.; Patre, M.; Loi, S. Trastuzumab emtansine plus atezolizumab versus trastuzumab emtansine plus placebo in previously treated, HER2-positive advanced breast cancer (KATE2): a phase 2, multicentre, randomised, double-blind trial. Lancet Oncol., 2020, 21(10), 1283-1295.
[http://dx.doi.org/10.1016/S1470-2045(20)30465-4]
[44]
Bedard, P.L.; Hyman, D.M.; Davids, M.S.; Siu, L.L. Small molecules, big impact: 20 years of targeted therapy in oncology. Lancet, 2020, 395(10229), 1078-1088.
[http://dx.doi.org/10.1016/S0140-6736(20)30164-1]
[45]
Guo, L.; Wei, R.; Lin, Y.; Kwok, H.F. Clinical and recent patents applications of PD-1/PD-L1 targeting immunotherapy in cancer treatment-current progress, strategy, and future perspective. Front. Immunol., 2020, 11, 1508.
[http://dx.doi.org/10.3389/fimmu.2020.01508]
[46]
Shaabani, S.; Huizinga, H.P.S.; Butera, R.; Kouchi, A.; Guzik, K.; Magiera-Mularz, K.; Holak, T.A.; Dömling, A. A patent review on PD-1/PD-L1 antagonists: small molecules, peptides, and macrocycles (2015-2018). Expert Opin. Ther. Pat., 2018, 28(9), 665-678.
[http://dx.doi.org/10.1080/13543776.2018.1512706]
[47]
Guzik, K.; Tomala, M.; Muszak, D.; Konieczny, M.; Hec, A.; Błaszkiewicz, U.; Pustuła, M.; Butera, R.; Dömling, A.; Holak, T.A. Development of the inhibitors that target the PD-1/PD-L1 interaction-A brief look at progress on small molecules, peptides and macrocycles. Molecules, 2019, 24(11)E2071
[http://dx.doi.org/10.3390/molecules24112071]
[48]
Smith, W.M.; Purvis, I.J.; Bomstad, C.N.; Labak, C.M.; Velpula, K.K.; Tsung, A.J.; Regan, J.N.; Venkataraman, S.; Vibhakar, R.; Asuthkar, S. Therapeutic targeting of immune checkpoints with small molecule inhibitors. Am. J. Transl. Res., 2019, 11(2), 529-541.
[49]
Skalniak, L.; Zak, K.M.; Guzik, K.; Magiera, K.; Musielak, B.; Pachota, M.; Szelazek, B.; Kocik, J.; Grudnik, P.; Tomala, M.; Krzanik, S.; Pyrc, K.; Dömling, A.; Dubin, G.; Holak, T.A. Small-molecule inhibitors of PD-1/PD-L1 immune checkpoint alleviate the PD-L1-induced exhaustion of T-cells. Oncotarget, 2017, 8(42), 72167-72181.
[http://dx.doi.org/10.18632/oncotarget.20050]
[50]
Ganesan, A.; Ahmed, M.; Okoye, I.; Arutyunova, E.; Babu, D.; Turnbull, W.L.; Kundu, J.K.; Shields, J.; Agopsowicz, K.C.; Xu, L.; Tabana, Y.; Srivastava, N.; Zhang, G.; Moon, T.C.; Belovodskiy, A.; Hena, M.; Kandadai, A.S.; Hosseini, S.N.; Hitt, M.; Walker, J.; Smylie, M.; West, F.G.; Siraki, A.G.; Lemieux, M.J.; Elahi, S.; Nieman, J.A.; Tyrrell, D.L.; Houghton, M.; Barakat, K. Comprehensive in vitro characterization of PD-L1 small molecule inhibitors. Sci. Rep., 2019, 9(1), 12392.
[http://dx.doi.org/10.1038/s41598-019-48826-6]
[51]
Konieczny, M.; Musielak, B.; Kocik, J.; Skalniak, L.; Sala, D.; Czub, M.; Magiera-Mularz, K.; Rodriguez, I.; Myrcha, M.; Stec, M.; Siedlar, M.; Holak, T.A.; Plewka, J. Di-bromo-based small-molecule inhibitors of the PD-1/PD-L1 immune checkpoint. J. Med. Chem., 2020, 63(19), 11271-11285.
[http://dx.doi.org/10.1021/acs.jmedchem.0c01260]
[52]
Li, K.; Tian, H. Development of small-molecule immune checkpoint inhibitors of PD-1/PD-L1 as a new therapeutic strategy for tumour immunotherapy. J. Drug Target., 2019, 27(3), 244-256.
[http://dx.doi.org/10.1080/1061186X.2018.1440400]
[53]
Musielak, B.; Kocik, J.; Skalniak, L.; Magiera-Mularz, K.; Sala, D.; Czub, M.; Stec, M.; Siedlar, M.; Holak, T.A.; Plewka, J. CA-170 - A potent small-molecule PD-L1 inhibitor or not? Molecules, 2019, 24(15)E2804
[http://dx.doi.org/10.3390/molecules24152804]
[54]
Tomioka, N.; Azuma, M.; Ikarashi, M.; Yamamoto, M.; Sato, M.; Watanabe, K.I.; Yamashiro, K.; Takahashi, M. The therapeutic candidate for immune checkpoint inhibitors elucidated by the status of Tumor-Infiltrating Lymphocytes (TILs) and Programmed Death Ligand 1 (PD-L1) expression in Triple Negative Breast Cancer (TNBC). Breast Cancer, 2018, 25(1), 34-42.
[http://dx.doi.org/10.1007/s12282-017-0781-0]
[55]
Mills, A.M.; Dill, E.A.; Moskaluk, C.A.; Dziegielewski, J.; Bullock, T.N.; Dillon, P.M. The relationship between mismatch repair deficiency and PD-L1 expression in breast carcinoma. Am. J. Surg. Pathol., 2018, 42(2), 183-191.
[http://dx.doi.org/10.1097/PAS.0000000000000949]
[56]
Curigliano, G.; Burstein, H.J.; Winer, E.P.; Gnant, M.; Dubsky, P.; Loibl, S.; Colleoni, M.; Regan, M.M.; Piccart-Gebhart, M.; Senn, H.J.; Thürlimann, B.; André, F.; Baselga, J.; Bergh, J.; Bonnefoi, H.; Brucker, S.Y.; Cardoso, F.; Carey, L.; Ciruelos, E.; Cuzick, J.; Denkert, C.; Di Leo, A.; Ejlertsen, B.; Francis, P.; Galimberti, V.; Garber, J.; Gulluoglu, B.; Goodwin, P.; Harbeck, N.; Hayes, D.F.; Huang, C.S.; Huober, J.; Hussein, K.; Jassem, J.; Jiang, Z.; Karlsson, P.; Morrow, M.; Orecchia, R.; Osborne, K.C.; Pagani, O.; Partridge, A.H.; Pritchard, K.; Ro, J.; Rutgers, E.J.T.; Sedlmayer, F.; Semiglazov, V.; Shao, Z.; Smith, I.; Toi, M.; Tutt, A.; Viale, G.; Watanabe, T.; Whelan, T.J.; Xu, B. De-escalating and escalating treatments for early-stage breast cancer: the St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann. Oncol., 2017, 28(8), 1700-1712.
[http://dx.doi.org/10.1093/annonc/mdx308]
[57]
Reis-Filho, J.S.; Tutt, A.N. Triple negative tumours: a critical review. Histopathology, 2008, 52(1), 108-118.
[http://dx.doi.org/10.1111/j.1365-2559.2007.02889.x]
[58]
Mao, Y.; Qu, Q.; Chen, X.; Huang, O.; Wu, J.; Shen, K. The prognostic value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. PLoS One, 2016, 11(4)e0152500
[http://dx.doi.org/10.1371/journal.pone.0152500]
[59]
Rooney, M.S.; Shukla, S.A.; Wu, C.J.; Getz, G.; Hacohen, N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell, 2015, 160(1-2), 48-61.
[http://dx.doi.org/10.1016/j.cell.2014.12.033]
[60]
Zitvogel, L.; Apetoh, L.; Ghiringhelli, F.; Kroemer, G. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol., 2008, 8(1), 59-73.
[http://dx.doi.org/10.1038/nri2216]
[61]
Wang, Y.; Waters, J.; Leung, M.L.; Unruh, A.; Roh, W.; Shi, X.; Chen, K.; Scheet, P.; Vattathil, S.; Liang, H.; Multani, A.; Zhang, H.; Zhao, R.; Michor, F.; Meric-Bernstam, F.; Navin, N.E. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature, 2014, 512(7513), 155-160.
[http://dx.doi.org/10.1038/nature13600]
[62]
Fusco, N.; Vaira, V.; Righi, I.; Sajjadi, E.; Venetis, K.; Lopez, G.; Cattaneo, M.; Castellani, M.; Rosso, L.; Nosotti, M.; Clerici, M.; Ferrero, S. Characterization of the immune microenvironment in malignant pleural mesothelioma reveals prognostic subgroups of patients. Lung Cancer, 2020, 150, 53-61.
[http://dx.doi.org/10.1016/j.lungcan.2020.09.026]
[63]
Denkert, C.; Loibl, S.; Noske, A.; Roller, M.; Müller, B.M.; Komor, M.; Budczies, J.; Darb-Esfahani, S.; Kronenwett, R.; Hanusch, C.; von Törne, C.; Weichert, W.; Engels, K.; Solbach, C.; Schrader, I.; Dietel, M.; von Minckwitz, G. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J. Clin. Oncol., 2010, 28(1), 105-113.
[http://dx.doi.org/10.1200/JCO.2009.23.7370]
[64]
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]
[65]
Denkert, C.; Wienert, S.; Poterie, A.; Loibl, S.; Budczies, J.; Badve, S.; Bago-Horvath, Z.; Bane, A.; Bedri, S.; Brock, J.; Chmielik, E.; Christgen, M.; Colpaert, C.; Demaria, S.; Van den Eynden, G.; Floris, G.; Fox, S.B.; Gao, D.; Ingold Heppner, B.; Kim, S.R.; Kos, Z.; Kreipe, H.H.; Lakhani, S.R.; Penault-Llorca, F.; Pruneri, G.; Radosevic-Robin, N.; Rimm, D.L.; Schnitt, S.J.; Sinn, B.V.; Sinn, P.; Sirtaine, N.; O’Toole, S.A.; Viale, G.; Van de Vijver, K.; de Wind, R.; von Minckwitz, G.; Klauschen, F.; Untch, M.; Fasching, P.A.; Reimer, T.; Willard-Gallo, K.; Michiels, S.; Loi, S.; Salgado, R. Standardized evaluation of tumor-infiltrating lymphocytes in breast cancer: results of the ring studies of the international immuno-oncology biomarker working group. Mod. Pathol., 2016, 29(10), 1155-1164.
[http://dx.doi.org/10.1038/modpathol.2016.109]
[66]
Loi, S.; Michiels, S.; Salgado, R.; Sirtaine, N.; Jose, V.; Fumagalli, D.; Kellokumpu-Lehtinen, P.L.; Bono, P.; Kataja, V.; Desmedt, C.; Piccart, M.J.; Loibl, S.; Denkert, C.; Smyth, M.J.; Joensuu, H.; Sotiriou, 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), 1544-1550.
[http://dx.doi.org/10.1093/annonc/mdu112]
[67]
Ali, H.R.; Provenzano, E.; Dawson, S.J.; Blows, F.M.; Liu, B.; Shah, M.; Earl, H.M.; Poole, C.J.; Hiller, L.; Dunn, J.A.; Bowden, S.J.; Twelves, C.; Bartlett, J.M.; Mahmoud, S.M.; Rakha, E.; Ellis, I.O.; Liu, S.; Gao, D.; Nielsen, T.O.; Pharoah, P.D.; Caldas, C. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann. Oncol., 2014, 25(8), 1536-1543.
[http://dx.doi.org/10.1093/annonc/mdu191]
[68]
Salgado, R.; Denkert, C.; Campbell, C.; Savas, P.; Nuciforo, P.; Aura, C.; de Azambuja, E.; Eidtmann, H.; Ellis, C.E.; Baselga, J.; Piccart-Gebhart, M.J.; Michiels, S.; Bradbury, I.; Sotiriou, C.; Loi, S. Tumor-infiltrating lymphocytes and associations with pathological complete response and event-free survival in HER2-positive early-stage breast cancer treated with lapatinib and trastuzumab: a secondary analysis of the NeoALTTO trial. JAMA Oncol., 2015, 1(4), 448-454.
[http://dx.doi.org/10.1001/jamaoncol.2015.0830]
[69]
Adams, S.; Gray, R.J.; Demaria, S.; Goldstein, L.; Perez, E.A.; Shulman, L.N.; Martino, S.; Wang, M.; Jones, V.E.; Saphner, T.J.; Wolff, A.C.; Wood, W.C.; Davidson, N.E.; Sledge, G.W.; Sparano, J.A.; Badve, S.S. 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), 2959-2966.
[http://dx.doi.org/10.1200/JCO.2013.55.0491]
[70]
Park, J.H.; Jonas, S.F.; Bataillon, G.; Criscitiello, C.; Salgado, R.; Loi, S.; Viale, G.; Lee, H.J.; Dieci, M.V.; Kim, S.B.; Vincent-Salomon, A.; Curigliano, G.; André, F.; Michiels, S. Prognostic value of tumor-infiltrating lymphocytes in patients with early-stage Triple-Negative Breast Cancers (TNBC) who did not receive adjuvant chemotherapy. Ann. Oncol., 2019, 30(12), 1941-1949.
[http://dx.doi.org/10.1093/annonc/mdz395]
[71]
Dieci, M.V.; Criscitiello, C.; Goubar, A.; Viale, G.; Conte, P.; Guarneri, V.; Ficarra, G.; Mathieu, M.C.; Delaloge, S.; Curigliano, G.; Andre, F. Prognostic value of tumor-infiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: a retrospective multicenter study. Ann. Oncol., 2014, 25(3), 611-618.
[http://dx.doi.org/10.1093/annonc/mdt556]
[72]
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.; Wang, 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 (mTNBC): results from KEYNOTE-086. Ann. Oncol., 2017, 28, v608.
[http://dx.doi.org/10.1093/annonc/mdx440.005]
[73]
Adams, S.; Schmid, P.; Rugo, H.S.; Winer, E.P.; Loirat, D.; Awada, A.; Cescon, D.W.; Iwata, H.; Campone, M.; Nanda, R.; Hui, R.; Curigliano, G.; Toppmeyer, D.; O’Shaughnessy, J.; Loi, S.; Paluch-Shimon, S.; Tan, A.R.; Card, D.; Zhao, J.; Karantza, V.; Cortés, J. Pembrolizumab monotherapy for previously treated metastatic triple-negative breast cancer: cohort A of the phase II KEYNOTE-086 study. Ann. Oncol., 2019, 30(3), 397-404.
[http://dx.doi.org/10.1093/annonc/mdy517]
[74]
Zou, Y.; Zou, X.; Zheng, S.; Tang, H.; Zhang, L.; Liu, P.; Xie, X. Efficacy and predictive factors of immune checkpoint inhibitors in metastatic breast cancer: a systematic review and meta-analysis. Ther. Adv. Med. Oncol., 2020, 121758835920940928
[http://dx.doi.org/10.1177/1758835920940928]
[75]
Pusztai, L.; Hofstatter, E.W.; Chung, G.G.; Horowitz, N.R.; Lannin, D.R.; Killelea, B.K.; Chagpar, A.B.; DiGiovanna, M.; Frederick, C.; Burello, T.; Harigopal, M. Durvalumab (MEDI4736) concurrent with nab-paclitaxel and dose dense doxorubicin cyclophosphamide (ddAC) as neoadjuvant therapy for Triple Negative Breast Cancer (TNBC). J. Clin. Oncol., 2018, 36(15), 586.
[http://dx.doi.org/10.1200/JCO.2018.36.15_suppl.586]
[76]
Schnell, A.; Bod, L.; Madi, A.; Kuchroo, V.K. The yin and yang of co-inhibitory receptors: toward anti-tumor immunity without autoimmunity. Cell Res., 2020, 30(4), 285-299.
[http://dx.doi.org/10.1038/s41422-020-0277-x]
[77]
Dermani, F.K.; Samadi, P.; Rahmani, G.; Kohlan, A.K.; Najafi, R. PD-1/PD-L1 immune checkpoint: potential target for cancer therapy. J. Cell. Physiol., 2019, 234(2), 1313-1325.
[http://dx.doi.org/10.1002/jcp.27172]
[78]
Cha, J.H.; Chan, L.C.; Li, C.W.; Hsu, J.L.; Hung, M.C. Mechanisms controlling PD-L1 expression in cancer. Mol. Cell, 2019, 76(3), 359-370.
[http://dx.doi.org/10.1016/j.molcel.2019.09.030]
[79]
Bastaki, S.; Irandoust, M.; Ahmadi, A.; Hojjat-Farsangi, M.; Ambrose, P.; Hallaj, S.; Edalati, M.; Ghalamfarsa, G.; Azizi, G.; Yousefi, M.; Chalajour, H.; Jadidi-Niaragh, F. PD-L1/PD-1 axis as a potent therapeutic target in breast cancer. Life Sci., 2020, 247117437
[http://dx.doi.org/10.1016/j.lfs.2020.117437]
[80]
Baptista, M.Z.; Sarian, L.O.; Derchain, S.F.; Pinto, G.A.; Vassallo, J. Prognostic significance of PD-L1 and PD-L2 in breast cancer. Hum. Pathol., 2016, 47(1), 78-84.
[http://dx.doi.org/10.1016/j.humpath.2015.09.006]
[81]
Han, Y.; Liu, D.; Li, L. PD-1/PD-L1 pathway: current researches in cancer. Am. J. Cancer Res., 2020, 10(3), 727-742.
[82]
Zhang, J.Y.; Yan, Y.Y.; Li, J.J.; Adhikari, R.; Fu, L.W. PD-1/PD-L1 based combinational cancer therapy: icing on the cake. Front. Pharmacol., 2020, 11, 722.
[http://dx.doi.org/10.3389/fphar.2020.00722]
[83]
Seliger, B. Basis of PD1/PD-L1 therapies. J. Clin. Med., 2019, 8(12)E2168
[http://dx.doi.org/10.3390/jcm8122168]
[84]
Tokumaru, Y.; Joyce, D.; Takabe, K. Current status and limitations of immunotherapy for breast cancer. Surgery, 2020, 167(3), 628-630.
[http://dx.doi.org/10.1016/j.surg.2019.09.018]
[85]
de Melo Gagliato, D.; Buzaid, A.C.; Perez-Garcia, J.; Cortes, J. Immunotherapy in breast cancer: current practice and clinical challenges. BioDrugs, 2020, 34(5), 611-623.
[http://dx.doi.org/10.1007/s40259-020-00436-9]
[86]
Rugo, H.S.; Loi, S.; Adams, S.; Schmid, P.; Schneeweiss, A.; Barrios, C.H.; Iwata, H.; Dieras, V.C.; Winer, E.P.; Kockx, M.; Peeters, D.; Chui, S.Y.; Lin, J.C.; Nguyen Duc, A.; Viale, G.; Molinero, L.; Emens, L.A. LBA20 - Performance of PD-L1 Immunohistochemistry (IHC) assays in unresectable locally advanced or metastatic Triple-Negative Breast Cancer (mTNBC): post-hoc analysis of IMpassion130. Ann. Oncol., 2019, 30, v858-v859.
[http://dx.doi.org/10.1093/annonc/mdz394.009]
[87]
Corti, C.; Sajjadi, E.; Fusco, N. Determination of mismatch repair status in human cancer and its clinical significance: does one size fit all? Adv. Anat. Pathol., 2019, 26(4), 270-279.
[http://dx.doi.org/10.1097/PAP.0000000000000234]
[88]
Gupta, D.; Heinen, C.D. The mismatch repair-dependent DNA damage response: mechanisms and implications. DNA Repair (Amst.), 2019, 78, 60-69.
[http://dx.doi.org/10.1016/j.dnarep.2019.03.009]
[89]
Bradford, K.C.; Wilkins, H.; Hao, P.; Li, Z.M.; Wang, B.; Burke, D.; Wu, D.; Smith, A.E.; Spaller, L.; Du, C.; Gauer, J.W.; Chan, E.; Hsieh, P.; Weninger, K.R.; Erie, D.A. Dynamic human MutSα-MutLα complexes compact mismatched DNA. Proc. Natl. Acad. Sci. USA, 2020, 117(28), 16302-16312.
[http://dx.doi.org/10.1073/pnas.1918519117]
[90]
Li, K.; Luo, H.; Huang, L.; Luo, H.; Zhu, X. Microsatellite instability: A review of what the oncologist should know. Cancer Cell Int., 2020, 20, 16.
[http://dx.doi.org/10.1186/s12935-019-1091-8]
[91]
Zhang, J.; Shih, D.J.H.; Lin, S-Y. Role of DNA repair defects in predicting immunotherapy response. Biomark. Res., 2020, 8(1), 23.
[http://dx.doi.org/10.1186/s40364-020-00202-7]
[92]
Venetis, K.; Sajjadi, E.; Haricharan, S.; Fusco, N. Mismatch repair testing in breast cancer: the path to tumor-specific immuno-oncology biomarkers. Transl. Cancer Res., 2020, 9(7), 4060-4064.
[http://dx.doi.org/10.21037/tcr-20-1852]
[93]
Boyiadzis, M.M.; Kirkwood, J.M.; Marshall, J.L.; Pritchard, C.C.; Azad, N.S.; Gulley, J.L. Significance and implications of FDA approval of pembrolizumab for biomarker-defined disease. J. Immunother. Cancer, 2018, 6(1), 35.
[http://dx.doi.org/10.1186/s40425-018-0342-x]
[94]
Musacchio, L.; Boccia, S.M.; Caruso, G.; Santangelo, G.; Fischetti, M.; Tomao, F.; Perniola, G.; Palaia, I.; Muzii, L.; Pignata, S.; Benedetti Panici, P.; Di Donato, V. Immune checkpoint inhibitors: A promising choice for endometrial cancer patients? J. Clin. Med., 2020, 9(6)E1721
[http://dx.doi.org/10.3390/jcm9061721]
[96]
Sajjadi, E.; Venetis, K.; Piciotti, R.; Invernizzi, M.; Guerini-Rocco, E.; Haricharan, S.; Fusco, N. Mismatch repair-deficient hormone receptor-positive breast cancers: biology and pathological characterization. Cancer Cell Int., 2021, 21(1), 266.
[http://dx.doi.org/10.1186/s12935-021-01976-y]
[97]
Cheng, A.S.; Leung, S.C.Y.; Gao, D.; Burugu, S.; Anurag, M.; Ellis, M.J.; Nielsen, T.O. Mismatch repair protein loss in breast cancer: clinicopathological associations in a large British Columbia cohort. Breast Cancer Res. Treat., 2020, 179(1), 3-10.
[http://dx.doi.org/10.1007/s10549-019-05438-y]
[98]
Fusco, N.; Lopez, G.; Corti, C.; Pesenti, C.; Colapietro, P.; Ercoli, G.; Gaudioso, G.; Faversani, A.; Gambini, D.; Michelotti, A.; Despini, L.; Blundo, C.; Vaira, V.; Miozzo, M.; Ferrero, S.; Bosari, S. 2018.
[99]
Lee, S.E.; Lee, H.S.; Kim, K.Y.; Park, J.H.; Roh, H.; Park, H.Y.; Kim, W.S. High prevalence of the MLH1 V384D germline mutation in patients with HER2-positive luminal B breast cancer. Sci. Rep., 2019, 9(1), 10966.
[http://dx.doi.org/10.1038/s41598-019-47439-3]
[100]
Le, D.T.; Durham, J.N.; Smith, K.N.; Wang, H.; Bartlett, B.R.; Aulakh, L.K.; Lu, S.; Kemberling, H.; Wilt, C.; Luber, B.S.; Wong, F.; Azad, N.S.; Rucki, A.A.; Laheru, D.; Donehower, R.; Zaheer, A.; Fisher, G.A.; Crocenzi, T.S.; Lee, J.J.; Greten, T.F.; Duffy, A.G.; Ciombor, K.K.; Eyring, A.D.; Lam, B.H.; Joe, A.; Kang, S.P.; Holdhoff, M.; Danilova, L.; Cope, L.; Meyer, C.; Zhou, S.; Goldberg, R.M.; Armstrong, D.K.; Bever, K.M.; Fader, A.N.; Taube, J.; Housseau, F.; Spetzler, D.; Xiao, N.; Pardoll, D.M.; Papadopoulos, N.; Kinzler, K.W.; Eshleman, J.R.; Vogelstein, B.; Anders, R.A.; Diaz, L.A., Jr Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science, 2017, 357(6349), 409-413.
[http://dx.doi.org/10.1126/science.aan6733]
[101]
Davies, H.; Morganella, S.; Purdie, C.A.; Jang, S.J.; Borgen, E.; Russnes, H.; Glodzik, D.; Zou, X.; Viari, A.; Richardson, A.L.; Børresen-Dale, A.L.; Thompson, A.; Eyfjord, J.E.; Kong, G.; Stratton, M.R.; Nik-Zainal, S. Whole-genome sequencing reveals breast cancers with mismatch repair deficiency. Cancer Res., 2017, 77(18), 4755-4762.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-1083]
[102]
Fremd, C.; Hlevnjak, M.; Zapatka, M.; Zoernig, I.; Halama, N.; Fejzibegovic, N.; Thewes, V.; Lichter, P.; Schirmacher, P.; Kloor, M.; Marmé, F.; Schütz, F.; Kosaloglu, Z.; Sinn, H.P.; Jäger, D.; Schneeweiss, A. mismatch repair deficiency drives durable complete remission by targeting programmed death receptor 1 in a metastatic luminal breast cancer patient. Breast Care (Basel), 2019, 14(1), 53-59.
[http://dx.doi.org/10.1159/000492580]
[103]
Zehir, A.; Benayed, R.; Shah, R.H.; Syed, A.; Middha, S.; Kim, H.R.; Srinivasan, P.; Gao, J.; Chakravarty, D.; Devlin, S.M.; Hellmann, M.D.; Barron, D.A.; Schram, A.M.; Hameed, M.; Dogan, S.; Ross, D.S.; Hechtman, J.F.; DeLair, D.F.; Yao, J.; Mandelker, D.L.; Cheng, D.T.; Chandramohan, R.; Mohanty, A.S.; Ptashkin, R.N.; Jayakumaran, G.; Prasad, M.; Syed, M.H.; Rema, A.B.; Liu, Z.Y.; Nafa, K.; Borsu, L.; Sadowska, J.; Casanova, J.; Bacares, R.; Kiecka, I.J.; Razumova, A.; Son, J.B.; Stewart, L.; Baldi, T.; Mullaney, K.A.; Al-Ahmadie, H.; Vakiani, E.; Abeshouse, A.A.; Penson, A.V.; Jonsson, P.; Camacho, N.; Chang, M.T.; Won, H.H.; Gross, B.E.; Kundra, R.; Heins, Z.J.; Chen, H.W.; Phillips, S.; Zhang, H.; Wang, J.; Ochoa, A.; Wills, J.; Eubank, M.; Thomas, S.B.; Gardos, S.M.; Reales, D.N.; Galle, J.; Durany, R.; Cambria, R.; Abida, W.; Cercek, A.; Feldman, D.R.; Gounder, M.M.; Hakimi, A.A.; Harding, J.J.; Iyer, G.; Janjigian, Y.Y.; Jordan, E.J.; Kelly, C.M.; Lowery, M.A.; Morris, L.G.T.; Omuro, A.M.; Raj, N.; Razavi, P.; Shoushtari, A.N.; Shukla, N.; Soumerai, T.E.; Varghese, A.M.; Yaeger, R.; Coleman, J.; Bochner, B.; Riely, G.J.; Saltz, L.B.; Scher, H.I.; Sabbatini, P.J.; Robson, M.E.; Klimstra, D.S.; Taylor, B.S.; Baselga, J.; Schultz, N.; Hyman, D.M.; Arcila, M.E.; Solit, D.B.; Ladanyi, M.; Berger, M.F. Mutational landscape of metastatic cancer revealed from prospective clinical sequencing of 10,000 patients. Nat. Med., 2017, 23(6), 703-713.
[http://dx.doi.org/10.1038/nm.4333]
[104]
Angerilli, V.; Galuppini, F.; Pagni, F.; Fusco, N.; Malapelle, U.; Fassan, M. The role of the pathologist in the next-generation era of tumor molecular characterization. Diagnostics (Basel), 2021, 11(2), 339.
[http://dx.doi.org/10.3390/diagnostics11020339]
[105]
Rizvi, N.A.; Hellmann, M.D.; Snyder, A.; Kvistborg, P.; Makarov, V.; Havel, J.J.; Lee, W.; Yuan, J.; Wong, P.; Ho, T.S.; Miller, M.L.; Rekhtman, N.; Moreira, A.L.; Ibrahim, F.; Bruggeman, C.; Gasmi, B.; Zappasodi, R.; Maeda, Y.; Sander, C.; Garon, E.B.; Merghoub, T.; Wolchok, J.D.; Schumacher, T.N.; Chan, T.A. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science, 2015, 348(6230), 124-128.
[http://dx.doi.org/10.1126/science.aaa1348]
[106]
Van Allen, E.M.; Miao, D.; Schilling, B.; Shukla, S.A.; Blank, C.; Zimmer, L.; Sucker, A.; Hillen, U.; Foppen, M.H.G.; Goldinger, S.M.; Utikal, J.; Hassel, J.C.; Weide, B.; Kaehler, K.C.; Loquai, C.; Mohr, P.; Gutzmer, R.; Dummer, R.; Gabriel, S.; Wu, C.J.; Schadendorf, D.; Garraway, L.A. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science, 2015, 350(6257), 207-211.
[http://dx.doi.org/10.1126/science.aad0095]
[107]
Chan, T.A.; Yarchoan, M.; Jaffee, E.; Swanton, C.; Quezada, S.A.; Stenzinger, A.; Peters, S. Development of tumor mutation burden as an immunotherapy biomarker: utility for the oncology clinic. Ann. Oncol., 2019, 30(1), 44-56.
[http://dx.doi.org/10.1093/annonc/mdy495]
[108]
Lawrence, M.S.; Stojanov, P.; Polak, P.; Kryukov, G.V.; Cibulskis, K.; Sivachenko, A.; Carter, S.L.; Stewart, C.; Mermel, C.H.; Roberts, S.A.; Kiezun, A.; Hammerman, P.S.; McKenna, A.; Drier, Y.; Zou, L.; Ramos, A.H.; Pugh, T.J.; Stransky, N.; Helman, E.; Kim, J.; Sougnez, C.; Ambrogio, L.; Nickerson, E.; Shefler, E.; Cortés, M.L.; Auclair, D.; Saksena, G.; Voet, D.; Noble, M.; DiCara, D.; Lin, P.; Lichtenstein, L.; Heiman, D.I.; Fennell, T.; Imielinski, M.; Hernandez, B.; Hodis, E.; Baca, S.; Dulak, A.M.; Lohr, J.; Landau, D.A.; Wu, C.J.; Melendez-Zajgla, J.; Hidalgo-Miranda, A.; Koren, A.; McCarroll, S.A.; Mora, J.; Crompton, B.; Onofrio, R.; Parkin, M.; Winckler, W.; Ardlie, K.; Gabriel, S.B.; Roberts, C.W.M.; Biegel, J.A.; Stegmaier, K.; Bass, A.J.; Garraway, L.A.; Meyerson, M.; Golub, T.R.; Gordenin, D.A.; Sunyaev, S.; Lander, E.S.; Getz, G. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature, 2013, 499(7457), 214-218.
[http://dx.doi.org/10.1038/nature12213]
[109]
Barroso-Sousa, R.; Jain, E.; Cohen, O.; Kim, D.; Buendia-Buendia, J.; Winer, E.; Lin, N.; Tolaney, S.M.; Wagle, N. Prevalence and mutational determinants of high tumor mutation burden in breast cancer. Ann. Oncol., 2020, 31(3), 387-394.
[http://dx.doi.org/10.1016/j.annonc.2019.11.010]
[110]
Mei, P.; Freitag, C.E.; Wei, L.; Zhang, Y.; Parwani, A.V.; Li, Z. High tumor mutation burden is associated with DNA damage repair gene mutation in breast carcinomas. Diagn. Pathol., 2020, 15(1), 50.
[http://dx.doi.org/10.1186/s13000-020-00971-7]
[111]
Karn, T.; Denkert, C.; Weber, K.E.; Holtrich, U.; Hanusch, C.; Sinn, B.V.; Higgs, B.W.; Jank, P.; Sinn, H.P.; Huober, J.; Becker, C.; Blohmer, J.U.; Marmé, F.; Schmitt, W.D.; Wu, S.; van Mackelenbergh, M.; Müller, V.; Schem, C.; Stickeler, E.; Fasching, P.A.; Jackisch, C.; Untch, M.; Schneeweiss, A.; Loibl, S. Tumor mutational burden and immune infiltration as independent predictors of response to neoadjuvant immune checkpoint inhibition in early TNBC in GeparNuevo. Ann. Oncol., 2020, 31(9), 1216-1222.
[http://dx.doi.org/10.1016/j.annonc.2020.05.015]
[112]
Karn, T.; Jiang, T.; Hatzis, C.; Sänger, N.; El-Balat, A.; Rody, A.; Holtrich, U.; Becker, S.; Bianchini, G.; Pusztai, L. Association between genomic metrics and immune infiltration in triple-negative breast cancer. JAMA Oncol., 2017, 3(12), 1707-1711.
[http://dx.doi.org/10.1001/jamaoncol.2017.2140]
[113]
Huang, R.S.P.; Haberberger, J.; Severson, E.; Duncan, D.L.; Hemmerich, A.; Edgerly, C.; Ferguson, N.L.; Williams, E.; Elvin, J.; Vergilio, J.A.; Killian, J.K.; Lin, D.I.; Tse, J.; Hiemenz, M.; Owens, C.; Danziger, N.; Hegde, P.S.; Venstrom, J.; Alexander, B.; Ross, J.S.; Ramkissoon, S.H. A pan-cancer analysis of PD-L1 immunohistochemistry and gene amplification, tumor mutation burden and microsatellite instability in 48,782 cases. Mod. Pathol., 2021, 34(2), 252-263.
[114]
Barrett, M.T.; Lenkiewicz, E.; Malasi, S.; Basu, A.; Yearley, J.H.; Annamalai, L.; McCullough, A.E.; Kosiorek, H.E.; Narang, P.; Wilson Sayres, M.A.; Chen, M.; Anderson, K.S.; Pockaj, B.A. The association of genomic lesions and PD-1/PD-L1 expression in resected triple-negative breast cancers. Breast Cancer Res., 2018, 20(1), 71.
[http://dx.doi.org/10.1186/s13058-018-1004-0]
[115]
Chumsri, S.; Sokol, E.S.; Soyano-Muller, A.E.; Parrondo, R.D.; Reynolds, G.A.; Nassar, A.; Thompson, E.A. Durable complete response with immune checkpoint inhibitor in breast cancer with high tumor mutational burden and APOBEC signature. J. Natl. Compr. Canc. Netw., 2020, 18(5), 517-521.
[http://dx.doi.org/10.6004/jnccn.2020.7543]
[116]
Voutsadakis, I.A. High tumor mutation burden and other immunotherapy response predictors in breast cancers: associations and therapeutic opportunities. Target. Oncol., 2020, 15(1), 127-138.
[http://dx.doi.org/10.1007/s11523-019-00689-7]
[117]
Lan, H.; Bu, Q.; Zhuang, L.; Ren, S.; Yan, X.; Li, Y.; Yu, Q.; Shi, X.; Zhao, J.; Guo, H.; Zhao, L. Frequency of homologous recombination-related gene mutations in breast cancer and their correlation with tumor mutation burden., 2020.
[118]
Angus, L.; Smid, M.; Wilting, S.M.; van Riet, J.; Van Hoeck, A.; Nguyen, L.; Nik-Zainal, S.; Steenbruggen, T.G.; Tjan-Heijnen, V.C.G.; Labots, M.; van Riel, J.M.G.H.; Bloemendal, H.J.; Steeghs, N.; Lolkema, M.P.; Voest, E.E.; van de Werken, H.J.G.; Jager, A.; Cuppen, E.; Sleijfer, S.; Martens, J.W.M. The genomic landscape of metastatic breast cancer highlights changes in mutation and signature frequencies. Nat. Genet., 2019, 51(10), 1450-1458.
[http://dx.doi.org/10.1038/s41588-019-0507-7]
[119]
Barroso-Sousa, R.; Keenan, T.E.; Pernas, S.; Exman, P.; Jain, E.; Garrido-Castro, A.C.; Hughes, M.; Bychkovsky, B.; Umeton, R.; Files, J.L.; Lindeman, N.I.; MacConaill, L.E.; Hodi, F.S.; Krop, I.E.; Dillon, D.; Winer, E.P.; Wagle, N.; Lin, N.U.; Mittendorf, E.A.; Van Allen, E.M.; Tolaney, S.M. Tumor mutational burden and PTEN alterations as molecular correlates of response to PD-1/L1 blockade in metastatic triple-negative breast cancer. Clin. Cancer Res., 2020, 26(11), 2565-2572.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-3507]
[120]
Zhang, X.; Zhao, W.; Wei, W.; You, Z.; Ou, X.; Sun, M.; Yin, Y.; Tang, X.; Zhao, Z.; Hu, C.; Liu, F.; Deng, J.; Mao, L.; Zhou, D.; Ren, Y.; Li, X.; Zhang, S.; Liu, C.; Geng, J.; Yao, G.; Song, B.; Liu, Y.; Li, D.; Jiang, Y.; Chen, Y.; Zhao, Y.; Yu, S.; Pang, D. Parallel analyses of somatic mutations in plasma circulating tumor DNA (ctDNA) and matched tumor tissues in early-stage breast cancer. Clin. Cancer Res., 2019, 25(21), 6546-6553.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-4055]
[121]
Campesato, L.F.; Barroso-Sousa, R.; Jimenez, L.; Correa, B.R.; Sabbaga, J.; Hoff, P.M.; Reis, L.F.; Galante, P.A.; Camargo, A.A. Comprehensive cancer-gene panels can be used to estimate mutational load and predict clinical benefit to PD-1 blockade in clinical practice. Oncotarget, 2015, 6(33), 34221-34227.
[http://dx.doi.org/10.18632/oncotarget.5950]
[122]
Hellmann, M.D.; Ciuleanu, T.E.; Pluzanski, A.; Lee, J.S.; Otterson, G.A.; Audigier-Valette, C.; Minenza, E.; Linardou, H.; Burgers, S.; Salman, P.; Borghaei, H.; Ramalingam, S.S.; Brahmer, J.; Reck, M.; O’Byrne, K.J.; Geese, W.J.; Green, G.; Chang, H.; Szustakowski, J.; Bhagavatheeswaran, P.; Healey, D.; Fu, Y.; Nathan, F.; Paz-Ares, L. Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden. N. Engl. J. Med., 2018, 378(22), 2093-2104.
[http://dx.doi.org/10.1056/NEJMoa1801946]
[123]
Goodman, A.M.; Kato, S.; Bazhenova, L.; Patel, S.P.; Frampton, G.M.; Miller, V.; Stephens, P.J.; Daniels, G.A.; Kurzrock, R. Tumor mutational burden as an independent predictor of response to immunotherapy in diverse cancers. Mol. Cancer Ther., 2017, 16(11), 2598-2608.
[http://dx.doi.org/10.1158/1535-7163.MCT-17-0386]
[124]
Legrand, F.A.; Gandara, D.R.; Mariathasan, S.; Powles, T.; He, X.; Zhang, W.; Jhunjhunwala, S.; Nickles, D.; Bourgon, R.; Schleifman, E.; Paul, S.M.; Kadel, E.E.; Kowanetz, M.; Cummings, C.; Li, Y.; Fabrizio, D.; Peters, E.; Hegde, P.S.; Amler, L.; Shames, D.S. Association of high tissue TMB and atezolizumab efficacy across multiple tumor types., 2018.
[126]
Samstein, R.M.; Lee, C.H.; Shoushtari, A.N.; Hellmann, M.D.; Shen, R.; Janjigian, Y.Y.; Barron, D.A.; Zehir, A.; Jordan, E.J.; Omuro, A.; Kaley, T.J.; Kendall, S.M.; Motzer, R.J.; Hakimi, A.A.; Voss, M.H.; Russo, P.; Rosenberg, J.; Iyer, G.; Bochner, B.H.; Bajorin, D.F.; Al-Ahmadie, H.A.; Chaft, J.E.; Rudin, C.M.; Riely, G.J.; Baxi, S.; Ho, A.L.; Wong, R.J.; Pfister, D.G.; Wolchok, J.D.; Barker, C.A.; Gutin, P.H.; Brennan, C.W.; Tabar, V.; Mellinghoff, I.K.; DeAngelis, L.M.; Ariyan, C.E.; Lee, N.; Tap, W.D.; Gounder, M.M.; D’Angelo, S.P.; Saltz, L.; Stadler, Z.K.; Scher, H.I.; Baselga, J.; Razavi, P.; Klebanoff, C.A.; Yaeger, R.; Segal, N.H.; Ku, G.Y.; DeMatteo, R.P.; Ladanyi, M.; Rizvi, N.A.; Berger, M.F.; Riaz, N.; Solit, D.B.; Chan, T.A.; Morris, L.G.T. Tumor mutational load predicts survival after immunotherapy across multiple cancer types. Nat. Genet., 2019, 51(2), 202-206.
[http://dx.doi.org/10.1038/s41588-018-0312-8]
[127]
Mosele, F.; Remon, J.; Mateo, J.; Westphalen, C.B.; Barlesi, F.; Lolkema, M.P.; Normanno, N.; Scarpa, A.; Robson, M.; Meric-Bernstam, F.; Wagle, N.; Stenzinger, A.; Bonastre, J.; Bayle, A.; Michiels, S.; Bièche, I.; Rouleau, E.; Jezdic, S.; Douillard, J.Y.; Reis-Filho, J.S.; Dienstmann, R.; André, F. Recommendations for the use of Next-Generation Sequencing (NGS) for patients with metastatic cancers: a report from the ESMO Precision Medicine Working Group. Ann. Oncol., 2020, 31(11), 1491-1505.
[http://dx.doi.org/10.1016/j.annonc.2020.07.014]
[128]
Vigliar, E.; Malapelle, U.; Bono, F.; Fusco, N.; Cortinovis, D.; Valtorta, E.; Spyridon, A.; Bimbatti, M.; Zocchi, M.; Piva, C.; Gaudioso, G.; Iaccarino, A.; Morbini, P.; Pagni, F. The reproducibility of the immunohistochemical PD-L1 testing in non-small-cell lung cancer: a multicentric Italian experience. BioMed Res. Int., 2019, 20196832909
[http://dx.doi.org/10.1155/2019/6832909]
[129]
Fumagalli, C.; Guerini-Rocco, E.; Vacirca, D.; Passaro, A.; Marinis, F.; Barberis, M. The immune profile of EGFR-mutated non-small-cell lung cancer at disease onset and progression after tyrosine kinase inhibitors therapy. Immunotherapy, 2018, 10(12), 1041-1045.
[http://dx.doi.org/10.2217/imt-2018-0027]
[130]
Hirsch, F.R.; McElhinny, A.; Stanforth, D.; Ranger-Moore, J.; Jansson, M.; Kulangara, K.; Richardson, W.; Towne, P.; Hanks, D.; Vennapusa, B.; Mistry, A.; Kalamegham, R.; Averbuch, S.; Novotny, J.; Rubin, E.; Emancipator, K.; McCaffery, I.; Williams, J.A.; Walker, J.; Longshore, J.; Tsao, M.S.; Kerr, K.M. PD-L1 immunohistochemistry assays for lung cancer: results from phase 1 of the blueprint PD-L1 IHC assay comparison project. J. Thorac. Oncol., 2017, 12(2), 208-222.
[http://dx.doi.org/10.1016/j.jtho.2016.11.2228]
[131]
Scott, M.; Scorer, P.; Barker, C.; Al-Masri, H. Comparison of patient populations identified by different PD-L1 assays in in Triple-Negative Breast Cancer (TNBC). Ann. Oncol., 2019, 30, iii4.
[http://dx.doi.org/10.1093/annonc/mdz095.009]
[133]
2020.
[134]
Cardoso, F.; Paluch-Shimon, S.; Senkus, E.; Curigliano, G.; Aapro, M.S.; André, F.; Barrios, C.H.; Bergh, J.; Bhattacharyya, G.S.; Biganzoli, L.; Boyle, F.; Cardoso, M.J.; Carey, L.A.; Cortés, J.; El Saghir, N.S.; Elzayat, M.; Eniu, A.; Fallowfield, L.; Francis, P.A.; Gelmon, K.; Gligorov, J.; Haidinger, R.; Harbeck, N.; Hu, X.; Kaufman, B.; Kaur, R.; Kiely, B.E.; Kim, S.B.; Lin, N.U.; Mertz, S.A.; Neciosup, S.; Offersen, B.V.; Ohno, S.; Pagani, O.; Prat, A.; Penault-Llorca, F.; Rugo, H.S.; Sledge, G.W.; Thomssen, C.; Vorobiof, D.A.; Wiseman, T.; Xu, B.; Norton, L.; Costa, A.; Winer, E.P. 5th ESO-ESMO international consensus guidelines for Advanced Breast Cancer (ABC 5). Ann. Oncol., 2020, 31(12), 1623-1649.
[http://dx.doi.org/10.1016/j.annonc.2020.09.010]
[136]
Marcus, L.; Lemery, S.J.; Keegan, P.; Pazdur, R. FDA approval summary: Pembrolizumab for the treatment of microsatellite instability-high solid tumors. Clin. Cancer Res., 2019, 25(13), 3753-3758.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-4070]
[137]
Loughrey, M.A-O.; McGrath, J.; Coleman, H.G.; Bankhead, P.A-O.; Maxwell, P.; McGready, C.; Bingham, V.; Humphries, M.A-O.; Craig, S.G.; McQuaid, S.; Salto-Tellez, M.; James, J.A-O. Identifying mismatch repair-deficient colon cancer: near-perfect concordance between immunohistochemistry and microsatellite instability testing in a large, population-based series. Histopathology, 2021, 78(3), 1365-2559.
[http://dx.doi.org/10.1111/his.14233]
[138]
Luchini, C.; Bibeau, F.; Ligtenberg, M.J.L.; Singh, N.; Nottegar, A.; Bosse, T.; Miller, R.; Riaz, N.; Douillard, J.Y.; Andre, F.; Scarpa, A. ESMO recommendations on microsatellite instability testing for immunotherapy in cancer, and its relationship with PD-1/PD-L1 expression and tumour mutational burden: a systematic review-based approach. Ann. Oncol., 2019, 30(8), 1232-1243.
[http://dx.doi.org/10.1093/annonc/mdz116]
[139]
Fumagalli, C.; Casadio, C.; Barberis, M.; Guarize, J.; Guerini-Rocco, E. Letter to the Editor. Clin. Lung Cancer, 2018, 19(4), e439-e440.
[http://dx.doi.org/10.1016/j.cllc.2018.03.001]
[140]
Agrawal, L.; Engel, K.B.; Greytak, S.R.; Moore, H.M. Understanding preanalytical variables and their effects on clinical biomarkers of oncology and immunotherapy. Semin. Cancer Biol., 2018, 52(Pt 2), 26-38.
[http://dx.doi.org/10.1016/j.semcancer.2017.12.008]
[141]
Rolfo, C.; Mack, P.C.; Scagliotti, G.V.; Baas, P.; Barlesi, F.; Bivona, T.G.; Herbst, R.S.; Mok, T.S.; Peled, N.; Pirker, R.; Raez, L.E.; Reck, M.; Riess, J.W.; Sequist, L.V.; Shepherd, F.A.; Sholl, L.M.; Tan, D.S.W.; Wakelee, H.A.; Wistuba, I.I.; Wynes, M.W.; Carbone, D.P.; Hirsch, F.R.; Gandara, D.R. Liquid biopsy for advanced Non-Small Cell Lung Cancer (NSCLC): a statement paper from the IASLC. J. Thorac. Oncol., 2018, 13(9), 1248-1268.
[http://dx.doi.org/10.1016/j.jtho.2018.05.030]
[142]
Gandara, D.R.; Paul, S.M.; Kowanetz, M.; Schleifman, E.; Zou, W.; Li, Y.; Rittmeyer, A.; Fehrenbacher, L.; Otto, G.; Malboeuf, C.; Lieber, D.S.; Lipson, D.; Silterra, J.; Amler, L.; Riehl, T.; Cummings, C.A.; Hegde, P.S.; Sandler, A.; Ballinger, M.; Fabrizio, D.; Mok, T.; Shames, D.S. Blood-based tumor mutational burden as a predictor of clinical benefit in non-small-cell lung cancer patients treated with atezolizumab. Nat. Med., 2018, 24(9), 1441-1448.
[http://dx.doi.org/10.1038/s41591-018-0134-3]
[143]
Georgiadis, A.; Durham, J.N.; Keefer, L.A.; Bartlett, B.R.; Zielonka, M.; Murphy, D.; White, J.R.; Lu, S.; Verner, E.L.; Ruan, F.; Riley, D.; Anders, R.A.; Gedvilaite, E.; Angiuoli, S.; Jones, S.; Velculescu, V.E.; Le, D.T.; Diaz, L.A., Jr; Sausen, M. Noninvasive detection of microsatellite instability and high tumor mutation burden in cancer patients treated with PD-1 blockade. Clin. Cancer Res., 2019, 25(23), 7024-7034.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-1372]
[144]
Hofman, P.; Heeke, S.; Alix-Panabières, C.; Pantel, K. Liquid biopsy in the era of immuno-oncology: is it ready for prime-time use for cancer patients? Ann. Oncol., 2019, 30(9), 1448-1459.
[http://dx.doi.org/10.1093/annonc/mdz196]
[145]
Bertucci, F.; Ng, C.K.Y.; Patsouris, A.; Droin, N.; Piscuoglio, S.; Carbuccia, N.; Soria, J.C.; Dien, A.T.; Adnani, Y.; Kamal, M.; Garnier, S.; Meurice, G.; Jimenez, M.; Dogan, S.; Verret, B.; Chaffanet, M.; Bachelot, T.; Campone, M.; Lefeuvre, C.; Bonnefoi, H.; Dalenc, F.; Jacquet, A.; De Filippo, M.R.; Babbar, N.; Birnbaum, D.; Filleron, T.; Le Tourneau, C.; André, F. Genomic characterization of metastatic breast cancers. Nature, 2019, 569(7757), 560-564.
[http://dx.doi.org/10.1038/s41586-019-1056-z]
[146]
Jiang, W.; Chan, C.K.; Weissman, I.L.; Kim, B.Y.S.; Hahn, S.M. Immune priming of the tumor microenvironment by radiation. Trends Cancer, 2016, 2(11), 638-645.
[http://dx.doi.org/10.1016/j.trecan.2016.09.007]
[147]
Golden, E.B.; Demaria, S.; Schiff, P.B.; Chachoua, A.; Formenti, S.C. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol. Res., 2013, 1(6), 365-372.
[http://dx.doi.org/10.1158/2326-6066.CIR-13-0115]
[148]
Solinas, C.; Marcoux, D.; Garaud, S.; Vitória, J.R.; Van den Eynden, G.; de Wind, A.; De Silva, P.; Boisson, A.; Craciun, L.; Larsimont, D.; Piccart-Gebhart, M.; Detours, V. t’Kint de Roodenbeke, D.; Willard-Gallo, K. BRCA gene mutations do not shape the extent and organization of tumor infiltrating lymphocytes in triple negative breast cancer. Cancer Lett., 2019, 450, 88-97.
[http://dx.doi.org/10.1016/j.canlet.2019.02.027]
[149]
Sønderstrup, I.M.H.; Jensen, M.B.; Ejlertsen, B.; Eriksen, J.O.; Gerdes, A.M.; Kruse, T.A.; Larsen, M.J.; Thomassen, M.; Laenkholm, A.V. Evaluation of tumor-infiltrating lymphocytes and association with prognosis in BRCA-mutated breast cancer. Acta Oncol., 2019, 58(3), 363-370.
[http://dx.doi.org/10.1080/0284186X.2018.1539239]
[150]
Criscitiello, C.; Curigliano, G. Tumour infiltrating lymphocytes and correlation with response to intensified platinum-based chemotherapy in BRCA-like tumours. Eur. J. Cancer, 2020, 127, 236-239.
[http://dx.doi.org/10.1016/j.ejca.2019.12.004]
[151]
Domchek, S.M.; Postel-Vinay, S.; Im, S.A.; Park, Y.H.; Delord, J.P.; Italiano, A.; Alexandre, J.; You, B.; Bastian, S.; Krebs, M.G.; Wang, D.; Waqar, S.N.; Lanasa, M.; Rhee, J.; Gao, H.; Rocher-Ros, V.; Jones, E.V.; Gulati, S.; Coenen-Stass, A.; Kozarewa, I.; Lai, Z.; Angell, H.K.; Opincar, L.; Herbolsheimer, P.; Kaufman, B. Olaparib and durvalumab in patients with germline BRCA-mutated metastatic breast cancer (MEDIOLA): an open-label, multicentre, phase 1/2, basket study. Lancet Oncol., 2020, 21(9), 1155-1164.
[http://dx.doi.org/10.1016/S1470-2045(20)30324-7]
[152]
Vinayak, S.; Tolaney, S.M.; Schwartzberg, L.; Mita, M.; McCann, G.; Tan, A.R.; Wahner-Hendrickson, A.E.; Forero, A.; Anders, C.; Wulf, G.M.; Dillon, P.; Lynce, F.; Zarwan, C.; Erban, J.K.; Zhou, Y.; Buerstatte, N.; Graham, J.R.; Arora, S.; Dezube, B.J.; Telli, M.L. Open-label clinical trial of niraparib combined with pembrolizumab for treatment of advanced or metastatic triple-negative breast cancer. JAMA Oncol., 2019, 5(8), 1132-1140.
[http://dx.doi.org/10.1001/jamaoncol.2019.1029]
[153]
Brignone, C.; Gutierrez, M.; Mefti, F.; Brain, E.; Jarcau, R.; Cvitkovic, F.; Bousetta, N.; Medioni, J.; Gligorov, J.; Grygar, C.; Marcu, M.; Triebel, F. First-line chemoimmunotherapy in metastatic breast carcinoma: combination of paclitaxel and IMP321 (LAG-3Ig) enhances immune responses and antitumor activity. J. Transl. Med., 2010, 8, 71.
[http://dx.doi.org/10.1186/1479-5876-8-71]
[154]
Hong, D.S.; Schoffski, P.; Calvo, A.; Sarantopoulos, J.; Ochoa De Olza, M.; Carvajal, R.D.; Prawira, A.; Kyi, C.; Esaki, T.; Akerley, W.L.; De Braud, F.G.; Hui, R.; Zhang, T.; Soo, R.A.; Maur, M.; Weickhardt, A.J.; Roy Chowdhury, N.; Sabatos-Peyton, C.; Kwak, E.L.; Tan, D.S.-W. 2018.
[155]
Tarantino, P.; Gandini, S.; Trapani, D.; Criscitiello, C.; Curigliano, G. Immunotherapy addition to neoadjuvant chemotherapy for early triple negative breast cancer: a systematic review and meta-analysis of randomized clinical trials. Crit. Rev. Oncol. Hematol., 2021, 159103223
[http://dx.doi.org/10.1016/j.critrevonc.2021.103223]
[156]
Vasen, H.F.; Blanco, I.; Aktan-Collan, K.; Gopie, J.P.; Alonso, A.; Aretz, S.; Bernstein, I.; Bertario, L.; Burn, J.; Capella, G.; Colas, C.; Engel, C.; Frayling, I.M.; Genuardi, M.; Heinimann, K.; Hes, F.J.; Hodgson, S.V.; Karagiannis, J.A.; Lalloo, F.; Lindblom, A.; Mecklin, J.P.; Møller, P.; Myrhoj, T.; Nagengast, F.M.; Parc, Y.; Ponz de Leon, M.; Renkonen-Sinisalo, L.; Sampson, J.R.; Stormorken, A.; Sijmons, R.H.; Tejpar, S.; Thomas, H.J.; Rahner, N.; Wijnen, J.T.; Järvinen, H.J.; Möslein, G. Revised guidelines for the clinical management of Lynch syndrome (HNPCC): recommendations by a group of European experts. Gut, 2013, 62(6), 812-823.
[http://dx.doi.org/10.1136/gutjnl-2012-304356]

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