The Tumor Microenvironment Affects Circulating Tumor Cells Metastasis and the Efficacy of Immune Checkpoint Blockade in Non-small Cell Lung Cancer

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Abstract

Lung cancer is one of the most lethal malignancies, with non-small cell lung cancer (NSCLC) being the most common histologic subtype. Metastasis leads to poor prognosis for patients with cancer. Tumor cells leave the tumor lesions, invade the surrounding stroma, and enter the bloodstream as circulating tumor cells (CTCs). The development of CTCs is the beginning of metastasis. The internal environment in which tumor cells grow and survive is called the tumor microenvironment (TME). It includes tumor cells, fibroblasts, immune cells, and the extracellular matrix. The TME is complex and dynamic. Moreover, the TME plays an important role in tumor development and metastasis and significantly impacts therapeutic outcomes. Immune checkpoint blockade (ICB) aims to inhibit the interaction of ligands with their corresponding receptors. ICB has the function of restoring the anti-tumor effect of immune cells. This review examines how TME interacts with CTCs, allowing CTCs to evade immunity and facilitating CTC metastasis. TME not only affects the progression of tumor metastasis but also interacts with tumor cells, which may affect the efficacy of immunotherapy.

Graphical Abstract

[1]
Kocarnik, J.M.; Compton, K. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: A systematic analysis for the global burden of disease study 2019. JAMA Oncol., 2022, 8(3), 420-444.
[http://dx.doi.org/10.1001/jamaoncol.2021.6987] [PMID: 34967848]
[2]
Majem, B.; Nadal, E.; Muñoz-Pinedo, C. Exploiting metabolic vulnerabilities of Non small cell lung carcinoma. Semin. Cell Dev. Biol., 2020, 98, 54-62.
[http://dx.doi.org/10.1016/j.semcdb.2019.06.004] [PMID: 31238096]
[3]
Imyanitov, E.N.; Iyevleva, A.G.; Levchenko, E.V. Molecular testing and targeted therapy for non-small cell lung cancer: Current status and perspectives. Crit. Rev. Oncol. Hematol., 2021, 157, 103194.
[http://dx.doi.org/10.1016/j.critrevonc.2020.103194] [PMID: 33316418]
[4]
Mamdouhi, T.; Twomey, J.D.; McSweeney, K.M.; Zhang, B. Fugitives on the run: Circulating tumor cells (CTCs) in metastatic diseases. Cancer Metastasis Rev., 2019, 38(1-2), 297-305.
[http://dx.doi.org/10.1007/s10555-019-09795-4] [PMID: 31053984]
[5]
Hurtado, P.; Martínez-Pena, I.; Piñeiro, R. Dangerous liaisons: Circulating tumor cells (CTCs) and cancer-associated fibroblasts (CAFs). Cancers, 2020, 12(10), 2861.
[http://dx.doi.org/10.3390/cancers12102861] [PMID: 33027902]
[6]
Binnewies, M.; Roberts, E.W.; Kersten, K.; Chan, V.; Fearon, D.F.; Merad, M.; Coussens, L.M.; Gabrilovich, D.I.; Ostrand-Rosenberg, S.; Hedrick, C.C.; Vonderheide, R.H.; Pittet, M.J.; Jain, R.K.; Zou, W.; Howcroft, T.K.; Woodhouse, E.C.; Weinberg, R.A.; Krummel, M.F. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med., 2018, 24(5), 541-550.
[http://dx.doi.org/10.1038/s41591-018-0014-x] [PMID: 29686425]
[7]
Liu, Y.; Zhang, Y.; Ding, Y. Platelet-mediated tumor metastasis mechanism and the role of cell adhesion molecules. Crit. Rev. Oncol. Hematol., 2021, 167, 103502.
[http://dx.doi.org/10.1016/j.critrevonc.2021.103502]
[8]
Klemm, F.; Joyce, J.A. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol., 2015, 25(4), 198-213.
[http://dx.doi.org/10.1016/j.tcb.2014.11.006] [PMID: 25540894]
[9]
Tang, T.; Huang, X.; Zhang, G.; Hong, Z.; Bai, X.; Liang, T. Advantages of targeting the tumor immune microenvironment over blocking immune checkpoint in cancer immunotherapy. Signal Transduct. Target. Ther., 2021, 6(1), 72.
[http://dx.doi.org/10.1038/s41392-020-00449-4] [PMID: 33608497]
[10]
Kumagai, S.; Togashi, Y.; Kamada, T.; Sugiyama, E.; Nishinakamura, H.; Takeuchi, Y.; Vitaly, K.; Itahashi, K.; Maeda, Y.; Matsui, S.; Shibahara, T.; Yamashita, Y.; Irie, T.; Tsuge, A.; Fukuoka, S.; Kawazoe, A.; Udagawa, H.; Kirita, K.; Aokage, K.; Ishii, G.; Kuwata, T.; Nakama, K.; Kawazu, M.; Ueno, T.; Yamazaki, N.; Goto, K.; Tsuboi, M.; Mano, H.; Doi, T.; Shitara, K.; Nishikawa, H. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies. Nat. Immunol., 2020, 21(11), 1346-1358.
[http://dx.doi.org/10.1038/s41590-020-0769-3] [PMID: 32868929]
[11]
Gu, X.; Huang, X.; Zhang, X.; Wang, C. Development and validation of a dna methylation-related classifier of circulating tumour cells to predict prognosis and to provide a therapeutic strategy in lung adenocarcinoma. Int. J. Biol. Sci., 2022, 18(13), 4984-5000.
[http://dx.doi.org/10.7150/ijbs.75284] [PMID: 35982906]
[12]
Pansy, K.; Uhl, B.; Krstic, J.; Szmyra, M.; Fechter, K.; Santiso, A.; Thüminger, L.; Greinix, H.; Kargl, J.; Prochazka, K.; Feichtinger, J.; Deutsch, A.J.A. Immune regulatory processes of the tumor microenvironment under malignant conditions. Int. J. Mol. Sci., 2021, 22(24), 13311.
[http://dx.doi.org/10.3390/ijms222413311] [PMID: 34948104]
[13]
Li, L.; Yu, R.; Cai, T. Effects of immune cells and cytokines on inflammation and immunosuppression in the tumor microenvironment. Int. Immunopharmacol., 2020, 88, 106939.
[http://dx.doi.org/10.1016/j.intimp.2020.106939]
[14]
Altorki, N.K.; Markowitz, G.J.; Gao, D.; Port, J.L.; Saxena, A.; Stiles, B.; McGraw, T.; Mittal, V. The lung microenvironment: An important regulator of tumour growth and metastasis. Nat. Rev. Cancer, 2019, 19(1), 9-31.
[http://dx.doi.org/10.1038/s41568-018-0081-9] [PMID: 30532012]
[15]
Paijens, S.T.; Vledder, A.; de Bruyn, M.; Nijman, H.W. Tumor-infiltrating lymphocytes in the immunotherapy era. Cell. Mol. Immunol., 2021, 18(4), 842-859.
[http://dx.doi.org/10.1038/s41423-020-00565-9] [PMID: 33139907]
[16]
Fu, T.; Dai, L.J.; Wu, S.Y.; Xiao, Y.; Ma, D.; Jiang, Y.Z.; Shao, Z.M. Spatial architecture of the immune microenvironment orchestrates tumor immunity and therapeutic response. J. Hematol. Oncol., 2021, 14(1), 98.
[http://dx.doi.org/10.1186/s13045-021-01103-4] [PMID: 34172088]
[17]
Giese, M.A.; Hind, L.E.; Huttenlocher, A. Neutrophil plasticity in the tumor microenvironment. Blood, 2019, 133(20), 2159-2167.
[http://dx.doi.org/10.1182/blood-2018-11-844548] [PMID: 30898857]
[18]
Roma-Rodrigues, C.; Mendes, R.; Baptista, P.; Fernandes, A. Targeting tumor microenvironment for cancer therapy. Int. J. Mol. Sci., 2019, 20(4), 840.
[http://dx.doi.org/10.3390/ijms20040840] [PMID: 30781344]
[19]
Li, Z.; Deng, J.; Sun, J. Hyperthermia targeting the tumor microenvironment facilitates immune checkpoint inhibitors. Front. Immunol., 2020, 11, 595207.
[http://dx.doi.org/10.3389/fimmu.2020.595207]
[20]
Sasidharan Nair, V.; Elkord, E. Immune checkpoint inhibitors in cancer therapy: a focus on T-regulatory cells. Immunol. Cell Biol., 2018, 96(1), 21-33.
[http://dx.doi.org/10.1111/imcb.1003] [PMID: 29359507]
[21]
Wu, T.; Dai, Y. Tumor microenvironment and therapeutic response. Cancer Lett., 2017, 387, 61-68.
[http://dx.doi.org/10.1016/j.canlet.2016.01.043]
[22]
Najafi, M.; Goradel, N.H.; Farhood, B.; Salehi, E.; Solhjoo, S.; Toolee, H.; Kharazinejad, E.; Mortezaee, K. Tumor microenvironment: Interactions and therapy. J. Cell. Physiol., 2019, 234(5), 5700-5721.
[http://dx.doi.org/10.1002/jcp.27425] [PMID: 30378106]
[23]
Buoncervello, M.; Gabriele, L.; Toschi, E. The janus face of tumor microenvironment targeted by immunotherapy. Int. J. Mol. Sci., 2019, 20(17), 4320.
[http://dx.doi.org/10.3390/ijms20174320] [PMID: 31484464]
[24]
Kai, F.; Drain, A.P.; Weaver, V.M. The extracellular matrix modulates the metastatic journey. Dev. Cell, 2019, 49(3), 332-346.
[http://dx.doi.org/10.1016/j.devcel.2019.03.026] [PMID: 31063753]
[25]
Girigoswami, K.; Saini, D.; Girigoswami, A. Extracellular matrix remodeling and development of cancer. Stem Cell Rev. Rep., 2021, 17(3), 739-747.
[http://dx.doi.org/10.1007/s12015-020-10070-1] [PMID: 33128168]
[26]
Niland, S.; Riscanevo, A.X.; Eble, J.A. Matrix metalloproteinases shape the tumor microenvironment in cancer progression. Int. J. Mol. Sci., 2021, 23(1), 146.
[http://dx.doi.org/10.3390/ijms23010146] [PMID: 35008569]
[27]
Najafi, M.; Farhood, B.; Mortezaee, K. Extracellular matrix (ECM) stiffness and degradation as cancer drivers. J. Cell. Biochem., 2019, 120(3), 2782-2790.
[28]
Khalaf, K.; Hana, D.; Chou, J.T.T.; Singh, C.; Mackiewicz, A.; Kaczmarek, M. Aspects of the tumor microenvironment involved in immune resistance and drug resistance. Front. Immunol., 2021, 12, 656364.
[http://dx.doi.org/10.3389/fimmu.2021.656364] [PMID: 34122412]
[29]
Hinshaw, D.C.; Shevde, L.A. The tumor microenvironment innately modulates cancer progression. Cancer Res., 2019, 79(18), 4557-4566.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-3962] [PMID: 31350295]
[30]
Micalizzi, D.S.; Maheswaran, S.; Haber, D.A. A conduit to metastasis: Circulating tumor cell biology. Genes Dev., 2017, 31(18), 1827-1840.
[http://dx.doi.org/10.1101/gad.305805.117] [PMID: 29051388]
[31]
Aceto, N.; Bardia, A.; Miyamoto, D.T.; Donaldson, M.C.; Wittner, B.S.; Spencer, J.A.; Yu, M.; Pely, A.; Engstrom, A.; Zhu, H.; Brannigan, B.W.; Kapur, R.; Stott, S.L.; Shioda, T.; Ramaswamy, S.; Ting, D.T.; Lin, C.P.; Toner, M.; Haber, D.A.; Maheswaran, S. Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis. Cell, 2014, 158(5), 1110-1122.
[http://dx.doi.org/10.1016/j.cell.2014.07.013] [PMID: 25171411]
[32]
Herath, S.; Razavi Bazaz, S.; Monkman, J.; Ebrahimi Warkiani, M.; Richard, D.; O’Byrne, K.; Kulasinghe, A. Circulating tumor cell clusters: Insights into tumour dissemination and metastasis. Expert Rev. Mol. Diagn., 2020, 20(11), 1139-1147.
[http://dx.doi.org/10.1080/14737159.2020.1846523] [PMID: 33140979]
[33]
Castro-Giner, F.; Aceto, N. Tracking cancer progression: From circulating tumor cells to metastasis. Genome Med., 2020, 12(1), 31.
[http://dx.doi.org/10.1186/s13073-020-00728-3] [PMID: 32192534]
[34]
Labelle, M.; Hynes, R.O. The initial hours of metastasis: The importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov., 2012, 2(12), 1091-1099.
[http://dx.doi.org/10.1158/2159-8290.CD-12-0329] [PMID: 23166151]
[35]
Badia-Ramentol, J.; Linares, J.; Gómez-Llonin, A.; Calon, A. Minimal residual disease, metastasis and immunity. Biomolecules, 2021, 11(2), 130.
[http://dx.doi.org/10.3390/biom11020130] [PMID: 33498251]
[36]
Ward, M.P.E.; Kane, E. L.; A Norris, L.; Mohamed, B.M.; Kelly, T.; Bates, M.; Clarke, A.; Brady, N.; Martin, C.M.; Brooks, R.D.; Brooks, D.A.; Selemidis, S.; Hanniffy, S.; Dixon, E.P.; A O’Toole, S.; J O’Leary, J. Platelets, immune cells and the coagulation cascade; friend or foe of the circulating tumour cell? Mol. Cancer, 2021, 20(1), 59.
[http://dx.doi.org/10.1186/s12943-021-01347-1] [PMID: 33789677]
[37]
Garrido-Navas, C.; de Miguel-Perez, D.; Exposito-Hernandez, J.; Bayarri, C.; Amezcua, V.; Ortigosa, A.; Valdivia, J.; Guerrero, R.; Garcia Puche, J.L.; Lorente, J.A.; Serrano, M.J. Cooperative and escaping mechanisms between circulating tumor cells and blood constituents. Cells, 2019, 8(11), 1382.
[http://dx.doi.org/10.3390/cells8111382] [PMID: 31684193]
[38]
Zhong, X.; Zhang, H.; Zhu, Y.; Liang, Y.; Yuan, Z.; Li, J.; Li, J.; Li, X.; Jia, Y.; He, T.; Zhu, J.; Sun, Y.; Jiang, W.; Zhang, H.; Wang, C.; Ke, Z. Circulating tumor cells in cancer patients: developments and clinical applications for immunotherapy. Mol. Cancer, 2020, 19(1), 15.
[http://dx.doi.org/10.1186/s12943-020-1141-9] [PMID: 31980023]
[39]
Lucotti, S.; Muschel, R.J. Platelets and metastasis: New implications of an old interplay. Front. Oncol., 2020, 10, 1350.
[http://dx.doi.org/10.3389/fonc.2020.01350] [PMID: 33042789]
[40]
Lou, X.L.; Sun, J.; Gong, S.Q.; Yu, X.F.; Gong, R.; Deng, H. Interaction between circulating cancer cells and platelets: Clinical implication. Chin. J. Cancer Res., 2015, 27(5), 450-460.
[PMID: 26543331]
[41]
Gkountela, S.; Castro-Giner, F.; Szczerba, B.M.; Vetter, M.; Landin, J.; Scherrer, R.; Krol, I.; Scheidmann, M.C.; Beisel, C.; Stirnimann, C.U.; Kurzeder, C.; Heinzelmann-Schwarz, V.; Rochlitz, C.; Weber, W.P.; Aceto, N. Circulating tumor cell clustering shapes DNA methylation to enable metastasis seeding. Cell, 2019, 176(1-2), 98-112.e14.
[http://dx.doi.org/10.1016/j.cell.2018.11.046] [PMID: 30633912]
[42]
Yu, M. Metastasis stemming from circulating tumor cell clusters. Trends Cell Biol., 2019, 29(4), 275-276.
[http://dx.doi.org/10.1016/j.tcb.2019.02.001] [PMID: 30799250]
[43]
Nengroo, M.A.; Verma, A.; Datta, D. Cytokine chemokine network in tumor microenvironment: Impact on CSC properties and therapeutic applications. Cytokine, 2022, 156, 155916.
[http://dx.doi.org/10.1016/j.cyto.2022.155916] [PMID: 35644058]
[44]
Chou, M.Y.; Yang, M.H. Interplay of immunometabolism and epithelial-mesenchymal transition in the tumor microenvironment. Int. J. Mol. Sci., 2021, 22(18), 9878.
[http://dx.doi.org/10.3390/ijms22189878] [PMID: 34576042]
[45]
Pantazaka, E.; Vardas, V.; Roumeliotou, A.; Kakavogiannis, S.; Kallergi, G. Clinical relevance of mesenchymal- and stem-associated phenotypes in circulating tumor cells isolated from lung cancer patients. Cancers, 2021, 13(9), 2158.
[http://dx.doi.org/10.3390/cancers13092158] [PMID: 33947159]
[46]
Liu, T.; Xu, H.; Huang, M.; Ma, W.; Saxena, D.; Lustig, R.A.; Alonso-Basanta, M.; Zhang, Z.; O’Rourke, D.M.; Zhang, L.; Gong, Y.; Kao, G.D.; Dorsey, J.F.; Fan, Y. Circulating glioma cells exhibit stem cell-like properties. Cancer Res., 2018, 78(23), 6632-6642.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-0650] [PMID: 30322863]
[47]
Alamgeer, M.; Ganju, V.; Szczepny, A.; Russell, P.A.; Prodanovic, Z.; Kumar, B.; Wainer, Z.; Brown, T.; Schneider-Kolsky, M.; Conron, M.; Wright, G.; Watkins, D.N. The prognostic significance of aldehyde dehydrogenase 1A1 (ALDH1A1) and CD133 expression in early stage non-small cell lung cancer. Thorax, 2013, 68(12), 1095-1104.
[http://dx.doi.org/10.1136/thoraxjnl-2012-203021] [PMID: 23878161]
[48]
Werner, S.; Stenzl, A.; Pantel, K. Expression of Epithelial Mesenchymal Transition and Cancer Stem Cell Markers in Circulating Tumor Cells. In: Isolation and Molecular Characterization of Circulating Tumor Cells; Springer: Cham, 2017; pp. 205-228.
[http://dx.doi.org/10.1007/978-3-319-55947-6_11]
[49]
Takemoto, A.; Okitaka, M.; Takagi, S. A critical role of platelet TGF-beta release in podoplanin-mediated tumour invasion and metastasis. Sci. Rep., 2017, 7, 42186.
[http://dx.doi.org/10.1038/srep42186] [PMID: 28176852]
[50]
Murlidhar, V.; Reddy, R.M.; Fouladdel, S.; Zhao, L.; Ishikawa, M.K.; Grabauskiene, S.; Zhang, Z.; Lin, J.; Chang, A.C.; Carrott, P.; Lynch, W.R.; Orringer, M.B.; Kumar-Sinha, C.; Palanisamy, N.; Beer, D.G.; Wicha, M.S.; Ramnath, N.; Azizi, E.; Nagrath, S. Poor prognosis indicated by venous circulating tumor cell clusters in early-stage lung cancers. Cancer Res., 2017, 77(18), 5194-5206.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2072] [PMID: 28716896]
[51]
Li, Z.; Fan, L.; Wu, Y.; Niu, Y.; Zhang, X.; Wang, B.; Yao, Y.; Chen, C.; Qi, N.; Wang, D.D.; Lin, P.P.; Tang, D.; Gao, W. Analysis of the prognostic role and biological characteristics of circulating tumor cell-associated white blood cell clusters in non-small cell lung cancer. J. Thorac. Dis., 2022, 14(5), 1544-1555.
[http://dx.doi.org/10.21037/jtd-22-423] [PMID: 35693614]
[52]
Maurer, S.; Kropp, K.N.; Klein, G.; Steinle, A.; Haen, S.P.; Walz, J.S.; Hinterleitner, C.; Märklin, M.; Kopp, H.G.; Salih, H.R. Platelet-mediated shedding of NKG2D ligands impairs NK cell immune-surveillance of tumor cells. OncoImmunology, 2018, 7(2), e1364827.
[http://dx.doi.org/10.1080/2162402X.2017.1364827] [PMID: 29308299]
[53]
Dianat-Moghadam, H.; Mahari, A.; Heidarifard, M.; Parnianfard, N.; Pourmousavi-Kh, L.; Rahbarghazi, R.; Amoozgar, Z. NK cells-directed therapies target circulating tumor cells and metastasis. Cancer Lett., 2021, 497, 41-53.
[http://dx.doi.org/10.1016/j.canlet.2020.09.021]
[54]
Manjunath, Y.; Upparahalli, S.V.; Avella, D.M.; Deroche, C.B.; Kimchi, E.T.; Staveley-O’Carroll, K.F.; Smith, C.J.; Li, G.; Kaifi, J.T. PD-L1 expression with epithelial mesenchymal transition of circulating tumor cells is associated with poor survival in curatively resected non-small cell lung cancer. Cancers, 2019, 11(6), 806.
[http://dx.doi.org/10.3390/cancers11060806] [PMID: 31212653]
[55]
Dianat-Moghadam, H.; Azizi, M.; Eslami-S, Z.; Cortés-Hernández, L.E.; Heidarifard, M.; Nouri, M.; Alix-Panabières, C. The role of circulating tumor cells in the metastatic cascade: Biology, technical challenges, and clinical relevance. Cancers, 2020, 12(4), 867.
[http://dx.doi.org/10.3390/cancers12040867] [PMID: 32260071]
[56]
Guo, B.; Oliver, T.G. Partners in crime: Neutrophil-CTC collusion in metastasis. Trends Immunol., 2019, 40(7), 556-559.
[http://dx.doi.org/10.1016/j.it.2019.04.009] [PMID: 31101536]
[57]
Yu, M.; Iriondo, O. Neutrophils help circulating tumor cells metastasize. Cancer Discov., 2019, 9(4), 458-459.
[http://dx.doi.org/10.1158/2159-8290.CD-NB2019-025] [PMID: 30803949]
[58]
Szczerba, B.M.; Castro-Giner, F.; Vetter, M.; Krol, I.; Gkountela, S.; Landin, J.; Scheidmann, M.C.; Donato, C.; Scherrer, R.; Singer, J.; Beisel, C.; Kurzeder, C.; Heinzelmann-Schwarz, V.; Rochlitz, C.; Weber, W.P.; Beerenwinkel, N.; Aceto, N. Neutrophils escort circulating tumour cells to enable cell cycle progression. Nature, 2019, 566(7745), 553-557.
[http://dx.doi.org/10.1038/s41586-019-0915-y] [PMID: 30728496]
[59]
Cools-Lartigue, J.; Spicer, J.; McDonald, B.; Gowing, S.; Chow, S.; Giannias, B.; Bourdeau, F.; Kubes, P.; Ferri, L. Neutrophil extracellular traps sequester circulating tumor cells and promote metastasis. J. Clin. Invest., 2013, 123(8), 3446-3458.
[http://dx.doi.org/10.1172/JCI67484] [PMID: 23863628]
[60]
Saini, M.; Szczerba, B.M.; Aceto, N. Circulating tumor cell-neutrophil tango along the metastatic process. Cancer Res., 2019, 79(24), 6067-6073.
[http://dx.doi.org/10.1158/0008-5472.CAN-19-1972] [PMID: 31527091]
[61]
El-Kenawi, A.; Hänggi, K.; Ruffell, B. The immune microenvironment and cancer metastasis. Cold Spring Harb. Perspect. Med., 2020, 10(4), a037424.
[http://dx.doi.org/10.1101/cshperspect.a037424] [PMID: 31501262]
[62]
Heeke, S.; Mograbi, B.; Alix-Panabières, C.; Hofman, P. Never travel alone: The crosstalk of circulating tumor cells and the blood microenvironment. Cells, 2019, 8(7), 714.
[http://dx.doi.org/10.3390/cells8070714] [PMID: 31337010]
[63]
Crosbie, P.A.J.; Shah, R.; Summers, Y.; Dive, C.; Blackhall, F. Prognostic and predictive biomarkers in early stage NSCLC: CTCs and serum/plasma markers. Transl. Lung Cancer Res., 2013, 2(5), 382-397.
[PMID: 25806257]
[64]
Deng, Z.; Wu, S.; Wang, Y.; Shi, D. Circulating tumor cell isolation for cancer diagnosis and prognosis. EBioMedicine, 2022, 83, 104237.
[http://dx.doi.org/10.1016/j.ebiom.2022.104237] [PMID: 36041264]
[65]
Fina, E.; Federico, D.; Novellis, P.; Dieci, E.; Monterisi, S.; Cioffi, F.; Mangiameli, G.; Finocchiaro, G.; Alloisio, M.; Veronesi, G. Subpopulations of circulating cells with morphological features of malignancy are preoperatively detected and have differential prognostic significance in non-small cell lung cancer. Cancers, 2021, 13(17), 4488.
[http://dx.doi.org/10.3390/cancers13174488] [PMID: 34503298]
[66]
Gallo, M.; De Luca, A.; Maiello, M.R.; D’Alessio, A.; Esposito, C.; Chicchinelli, N.; Forgione, L.; Piccirillo, M.C.; Rocco, G.; Morabito, A.; Botti, G.; Normanno, N. Clinical utility of circulating tumor cells in patients with non-small-cell lung cancer. Transl. Lung Cancer Res., 2017, 6(4), 486-498.
[http://dx.doi.org/10.21037/tlcr.2017.05.07] [PMID: 28904891]
[67]
Zhang, Y.; Men, Y.; Wang, J.; Xing, P.; Zhao, J.; Li, J.; Xu, D.; Hui, Z.; Cui, W. Epithelial circulating tumor cells with a heterogeneous phenotype are associated with metastasis in NSCLC. J. Cancer Res. Clin. Oncol., 2022, 148(5), 1137-1146.
[http://dx.doi.org/10.1007/s00432-021-03681-9] [PMID: 34255149]
[68]
Li, Z.; Xu, K.; Tartarone, A.; Santarpia, M.; Zhu, Y.; Jiang, G. Circulating tumor cells can predict the prognosis of patients with non-small cell lung cancer after resection: A retrospective study. Transl. Lung Cancer Res., 2021, 10(2), 995-1006.
[http://dx.doi.org/10.21037/tlcr-21-149] [PMID: 33718038]
[69]
Liu, J.; Liu, Y.; Gu, C. Longitudinal Change of Circulating Tumor Cells During Chemoradiation and Its Correlation with Prognosis in Advanced Nonsmall-Cell Lung Cancer Patients In: In: Cancer Biotherapy and Radiopharmaceuticals Mary. Ann Liebert, Inc., publishers,; , 2021.
[http://dx.doi.org/10.1089/cbr.2020.4096]
[70]
Papadaki, M.A.; Messaritakis, I.; Fiste, O.; Souglakos, J.; Politaki, E.; Kotsakis, A.; Georgoulias, V.; Mavroudis, D.; Agelaki, S. Assessment of the efficacy and clinical utility of different circulating tumor cell (CTC) detection assays in patients with chemotherapy-naïve advanced or metastatic non-small cell lung cancer (NSCLC). Int. J. Mol. Sci., 2021, 22(2), 925.
[http://dx.doi.org/10.3390/ijms22020925] [PMID: 33477700]
[71]
Massa, C.; Seliger, B. The tumor microenvironment: Thousand obstacles for effector T cells. Cell. Immunol., 2019, 343, 103730.
[http://dx.doi.org/10.1016/j.cellimm.2017.12.004] [PMID: 29249298]
[72]
Sznol, M.; Melero, I. Revisiting anti-CTLA-4 antibodies in combination with PD-1 blockade for cancer immunotherapy. Ann. Oncol., 2021, 32(3), 295-297.
[http://dx.doi.org/10.1016/j.annonc.2020.11.018] [PMID: 33307201]
[73]
Li, Y.; Liu, J.; Gao, L. Targeting the tumor microenvironment to overcome immune checkpoint blockade therapy resistance. Immunol. Lett., 2020, 220, 88-96.
[http://dx.doi.org/10.1016/j.imlet.2019.03.006]
[74]
Paulsen, E.E.; Kilvaer, T.K.; Rakaee, M.; Richardsen, E.; Hald, S.M.; Andersen, S.; Busund, L.T.; Bremnes, R.M.; Donnem, T. CTLA-4 expression in the non-small cell lung cancer patient tumor microenvironment: diverging prognostic impact in primary tumors and lymph node metastases. Cancer Immunol. Immunother., 2017, 66(11), 1449-1461.
[http://dx.doi.org/10.1007/s00262-017-2039-2] [PMID: 28707078]
[75]
Bagchi, S.; Yuan, R.; Engleman, E.G. Immune checkpoint inhibitors for the treatment of cancer: Clinical impact and mechanisms of response and resistance. Annu. Rev. Pathol., 2021, 16(1), 223-249.
[http://dx.doi.org/10.1146/annurev-pathol-042020-042741] [PMID: 33197221]
[76]
Wang, Q.; Xie, B.; Liu, S.; Shi, Y.; Tao, Y.; Xiao, D.; Wang, W. What happens to the immune microenvironment after PD-1 inhibitor therapy? Front. Immunol., 2021, 12, 773168.
[http://dx.doi.org/10.3389/fimmu.2021.773168] [PMID: 35003090]
[77]
Aguilar, E.J.; Ricciuti, B.; Gainor, J.F.; Kehl, K.L.; Kravets, S.; Dahlberg, S.; Nishino, M.; Sholl, L.M.; Adeni, A.; Subegdjo, S.; Khosrowjerdi, S.; Peterson, R.M.; Digumarthy, S.; Liu, C.; Sauter, J.; Rizvi, H.; Arbour, K.C.; Carter, B.W.; Heymach, J.V.; Altan, M.; Hellmann, M.D.; Awad, M.M. Outcomes to first-line pembrolizumab in patients with non-small-cell lung cancer and very high PD-L1 expression. Ann. Oncol., 2019, 30(10), 1653-1659.
[http://dx.doi.org/10.1093/annonc/mdz288] [PMID: 31435660]
[78]
De Marchi, P.; Leal, L.F.; Duval da Silva, V.; da Silva, E.C.A.; Cordeiro de Lima, V.C.; Reis, R.M. PD-L1 expression by Tumor Proportion Score (TPS) and Combined Positive Score (CPS) are similar in non-small cell lung cancer (NSCLC). J. Clin. Pathol., 2021, 74(11), 735-740.
[http://dx.doi.org/10.1136/jclinpath-2020-206832] [PMID: 33589532]
[79]
Brody, R.; Zhang, Y.; Ballas, M.; Siddiqui, M.K.; Gupta, P.; Barker, C.; Midha, A.; Walker, J. PD-L1 expression in advanced NSCLC: Insights into risk stratification and treatment selection from a systematic literature review. Lung Cancer, 2017, 112, 200-215.
[http://dx.doi.org/10.1016/j.lungcan.2017.08.005] [PMID: 29191596]
[80]
Pircher, A.; Heidegger, I.; Wolf, D. Atezolizumab for PD-L1-Selected Patients with NSCLC. N. Engl. J. Med., 2021, 384(6), 584.
[PMID: 33567201]
[81]
Peranzoni, E.; Lemoine, J.; Vimeux, L.; Feuillet, V.; Barrin, S.; Kantari-Mimoun, C.; Bercovici, N.; Guérin, M.; Biton, J.; Ouakrim, H.; Régnier, F.; Lupo, A.; Alifano, M.; Damotte, D.; Donnadieu, E. Macrophages impede CD8 T cells from reaching tumor cells and limit the efficacy of anti-PD-1 treatment. Proc. Natl. Acad. Sci. USA, 2018, 115(17), E4041-E4050.
[http://dx.doi.org/10.1073/pnas.1720948115] [PMID: 29632196]
[82]
Horton, B.L.; Morgan, D.M.; Momin, N.; Zagorulya, M.; Torres-Mejia, E.; Bhandarkar, V.; Wittrup, K.D.; Love, J.C.; Spranger, S. Lack of CD8 + T cell effector differentiation during priming mediates checkpoint blockade resistance in non-small cell lung cancer. Sci. Immunol., 2021, 6(64), eabi8800.
[http://dx.doi.org/10.1126/sciimmunol.abi8800] [PMID: 34714687]
[83]
Gomez-Roca, C.; Cassier, P.; Zamarin, D.; Machiels, J.P.; Luis Perez Gracia, J.; Stephen Hodi, F.; Taus, A.; Martinez Garcia, M.; Boni, V.; Eder, J.P.; Hafez, N.; Sullivan, R.; Mcdermott, D.; Champiat, S.; Aspeslagh, S.; Terret, C.; Jegg, A.M.; Jacob, W.; Cannarile, M.A.; Ries, C.; Korski, K.; Michielin, F.; Christen, R.; Babitzki, G.; Watson, C.; Meneses-Lorente, G.; Weisser, M.; Rüttinger, D.; Delord, J.P.; Marabelle, A. Anti-CSF-1R emactuzumab in combination with anti-PD-L1 atezolizumab in advanced solid tumor patients naïve or experienced for immune checkpoint blockade. J. Immunother. Cancer, 2022, 10(5), e004076.
[http://dx.doi.org/10.1136/jitc-2021-004076] [PMID: 35577503]
[84]
Bagley, S.J.; Kothari, S.; Aggarwal, C.; Bauml, J.M.; Alley, E.W.; Evans, T.L.; Kosteva, J.A.; Ciunci, C.A.; Gabriel, P.E.; Thompson, J.C.; Stonehouse-Lee, S.; Sherry, V.E.; Gilbert, E.; Eaby-Sandy, B.; Mutale, F.; DiLullo, G.; Cohen, R.B.; Vachani, A.; Langer, C.J. Pretreatment neutrophil-to-lymphocyte ratio as a marker of outcomes in nivolumab-treated patients with advanced non-small-cell lung cancer. Lung Cancer, 2017, 106, 1-7.
[http://dx.doi.org/10.1016/j.lungcan.2017.01.013] [PMID: 28285682]
[85]
Kim, K.H.; Kim, H.K.; Kim, H.D.; Kim, C.G.; Lee, H.; Han, J.W.; Choi, S.J.; Jeong, S.; Jeon, M.; Kim, H.; Koh, J.; Ku, B.M.; Park, S.H.; Ahn, M.J.; Shin, E.C. PD-1 blockade-unresponsive human tumor-infiltrating CD8+ T cells are marked by loss of CD28 expression and rescued by IL-15. Cell. Mol. Immunol., 2021, 18(2), 385-397.
[http://dx.doi.org/10.1038/s41423-020-0427-6] [PMID: 32332901]
[86]
Liu, Y.; Zugazagoitia, J.; Ahmed, F.S.; Henick, B.S.; Gettinger, S.N.; Herbst, R.S.; Schalper, K.A.; Rimm, D.L. Immune cell PD-L1 co-localizes with macrophages and is associated with outcome in PD-1 pathway blockade therapy. Clin. Cancer Res., 2020, 26(4), 970-977.
[http://dx.doi.org/10.1158/1078-0432.CCR-19-1040] [PMID: 31615933]
[87]
Thommen, D.S.; Schreiner, J.; Müller, P.; Herzig, P.; Roller, A.; Belousov, A.; Umana, P.; Pisa, P.; Klein, C.; Bacac, M.; Fischer, O.S.; Moersig, W.; Savic Prince, S.; Levitsky, V.; Karanikas, V.; Lardinois, D.; Zippelius, A. Progression of lung cancer is associated with increased dysfunction of t cells defined by coexpression of multiple inhibitory receptors. Cancer Immunol. Res., 2015, 3(12), 1344-1355.
[http://dx.doi.org/10.1158/2326-6066.CIR-15-0097] [PMID: 26253731]
[88]
Koyama, S.; Akbay, E.A.; Li, Y.Y.; Herter-Sprie, G.S.; Buczkowski, K.A.; Richards, W.G.; Gandhi, L.; Redig, A.J.; Rodig, S.J.; Asahina, H.; Jones, R.E.; Kulkarni, M.M.; Kuraguchi, M.; Palakurthi, S.; Fecci, P.E.; Johnson, B.E.; Janne, P.A.; Engelman, J.A.; Gangadharan, S.P.; Costa, D.B.; Freeman, G.J.; Bueno, R.; Hodi, F.S.; Dranoff, G.; Wong, K.K.; Hammerman, P.S. Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat. Commun., 2016, 7(1), 10501.
[http://dx.doi.org/10.1038/ncomms10501] [PMID: 26883990]
[89]
Higgs, B.W.; Morehouse, C.A.; Streicher, K.; Brohawn, P.Z.; Pilataxi, F.; Gupta, A.; Ranade, K. Interferon gamma messenger RNA signature in tumor biopsies predicts outcomes in patients with non-small cell lung carcinoma or urothelial cancer treated with durvalumab. Clin. Cancer Res., 2018, 24(16), 3857-3866.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-3451] [PMID: 29716923]
[90]
Karachaliou, N.; Gonzalez-Cao, M.; Crespo, G.; Drozdowskyj, A.; Aldeguer, E.; Gimenez-Capitan, A.; Teixido, C.; Molina-Vila, M.A.; Viteri, S.; De Los Llanos Gil, M.; Algarra, S.M.; Perez-Ruiz, E.; Marquez-Rodas, I.; Rodriguez-Abreu, D.; Blanco, R.; Puertolas, T.; Royo, M.A.; Rosell, R. Interferon gamma, an important marker of response to immune checkpoint blockade in non-small cell lung cancer and melanoma patients. Ther. Adv. Med. Oncol., 2018, •••, 10.
[http://dx.doi.org/10.1177/1758834017749748] [PMID: 29383037]
[91]
Li, Q.; Ngo, P.T.; Egilmez, N.K. Anti-PD-1 antibody-mediated activation of type 17 T-cells undermines checkpoint blockade therapy. Cancer Immunol. Immunother., 2021, 70(6), 1789-1796.
[http://dx.doi.org/10.1007/s00262-020-02795-2] [PMID: 33245376]
[92]
Akbay, E.A.; Koyama, S.; Liu, Y.; Dries, R.; Bufe, L.E.; Silkes, M.; Alam, M.D.M.; Magee, D.M.; Jones, R.; Jinushi, M.; Kulkarni, M.; Carretero, J.; Wang, X.; Warner-Hatten, T.; Cavanaugh, J.D.; Osa, A.; Kumanogoh, A.; Freeman, G.J.; Awad, M.M.; Christiani, D.C.; Bueno, R.; Hammerman, P.S.; Dranoff, G.; Wong, K.K. Interleukin-17A promotes lung tumor progression through neutrophil attraction to tumor sites and mediating resistance to pd-1 blockade. J. Thorac. Oncol., 2017, 12(8), 1268-1279.
[http://dx.doi.org/10.1016/j.jtho.2017.04.017] [PMID: 28483607]
[93]
Chang, S.H. T helper 17 (Th17) cells and interleukin-17 (IL-17) in cancer. Arch. Pharm. Res., 2019, 42(7), 549-559.
[http://dx.doi.org/10.1007/s12272-019-01146-9] [PMID: 30941641]
[94]
Petitprez, F.; Meylan, M.; Reynies, A. de, The tumor microenvironment in the response to immune checkpoint blockade therapies. Front. Immunol., 2020, 11, 784.
[http://dx.doi.org/10.3389/fimmu.2020.00784]
[95]
Heinhuis, K.M.; Ros, W.; Kok, M.; Steeghs, N.; Beijnen, J.H.; Schellens, J.H.M. Enhancing antitumor response by combining immune checkpoint inhibitors with chemotherapy in solid tumors. Ann. Oncol., 2019, 30(2), 219-235.
[http://dx.doi.org/10.1093/annonc/mdy551] [PMID: 30608567]
[96]
Osipov, A.; Saung, M.T.; Zheng, L.; Murphy, A.G. Small molecule immunomodulation: the tumor microenvironment and overcoming immune escape. J. Immunother. Cancer, 2019, 7(1), 224.
[http://dx.doi.org/10.1186/s40425-019-0667-0] [PMID: 31439034]