Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response
Abstract
Simple Summary
Abstract
1. Introduction
2. Radiotherapy
3. Local Ablation Therapies
3.1. Radiofrequency Ablation
3.2. Microwave Ablation Therapy
3.3. High Intensity Focused Ultrasound Ablation
4. Checkpoint Inhibitors
4.1. PD-1-PD-L1 Axis
4.2. CTLA-4
4.3. TIM3
4.4. TIGIT-CD96
4.5. LAG3
5. Chemotherapy
5.1. Alkylating and Alkylating-Like Agents
5.2. Microtubule Targeting Agents
5.3. Antimetabolites
5.4. Anthracyclines
5.5. Other Anti-Cancer Agents
5.6. Combination Therapies
6. Protein Kinase Inhibitors
6.1. Src-Kinase Inhibitors
6.2. BRAF Inhibitors
6.3. GSK-3β Inhibitors
6.4. Other Protein Kinase Inhibitors
7. Oncolytic Viruses
8. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Campbell, K.S.; Hasegawa, J. Natural killer cell biology: An update and future directions. J. Allergy Clin. Immunol. 2013, 132, 536–544. [Google Scholar] [CrossRef]
- Vivier, E.; Tomasello, E.; Baratin, M.; Walzer, T.; Ugolini, S. Functions of natural killer cells. Nat. Immunol. 2008, 9, 503–510. [Google Scholar] [CrossRef]
- Cooper, M.A.; Fehniger, T.A.; Caligiuri, M.A. The biology of human natural killer-cell subsets. Trends Immunol. 2001, 22, 633–640. [Google Scholar] [CrossRef]
- Zamai, L.; Ahmad, M.; Bennett, I.M.; Azzoni, L.; Alnemri, E.S.; Perussia, B. Natural killer (NK) cell-mediated cytotoxicity: Differential use of TRAIL and Fas ligand by immature and mature primary human NK cells. J. Exp. Med. 1998, 188, 2375–2380. [Google Scholar] [CrossRef] [PubMed]
- Lanier, L.L. Up on the tightrope: Natural killer cell activation and inhibition. Nat. Immunol. 2008, 9, 495–502. [Google Scholar] [CrossRef]
- Veluchamy, J.P.; Kok, N.; van der Vliet, H.J.; Verheul, H.M.W.; de Gruijl, T.D.; Spanholtz, J. The rise of allogeneic Natural killer cells as a platform for cancer immunotherapy: Recent innovations and future developments. Front. Immunol. 2017, 8. [Google Scholar] [CrossRef] [PubMed]
- WHO Key Statistics. Available online: https://www.who.int/cancer/resources/keyfacts/en/ (accessed on 30 October 2020).
- WHO Europe Cancer. Available online: https://www.euro.who.int/en/health-topics/noncommunicable-diseases/cancer/cancer (accessed on 30 October 2020).
- Takeuchi, H.; Maehara, Y.; Tokunaga, E.; Koga, T.; Kakeji, Y.; Sugimachi, K. Prognostic significance of natural killer cell activity in patients with gastric carcinoma: A multivariate analysis. Am. J. Gastroenterol. 2001, 96, 574–578. [Google Scholar] [CrossRef] [PubMed]
- Tartter, P.I.; Steinberg, B.; Barron, D.M.; Martinelli, G. The Prognostic Significance of Natural Killer Cytotoxicity in Patients with Colorectal Cancer. Arch. Surg. 1987, 122, 1264–1268. [Google Scholar] [CrossRef]
- Luna, J.I.; Grossenbacher, S.K.; Murphy, W.J.; Canter, R.J. Natural Killer Cell Immunotherapy Targeting Cancer Stem Cells. Expert Opin. Biol. Ther. 2018, 17, 313–324. [Google Scholar] [CrossRef]
- Battella, S.; Cox, M.C.; Santoni, A.; Palmieri, G. Natural killer (NK) cells and anti-tumor therapeutic mAb: Unexplored interactions. J. Leukoc. Biol. 2016, 99, 87–96. [Google Scholar] [CrossRef]
- Baskar, R.; Lee, K.A.; Yeo, R.; Yeoh, K.W. Cancer and radiation therapy: Current advances and future directions. Int. J. Med. Sci. 2012, 9, 193–199. [Google Scholar] [CrossRef] [PubMed]
- Delaney, G.; Jacob, S.; Featherstone, C.; Barton, M. The role of Radiother in cancer treatment: Estimating optimal utilization from a review of evidence-based clinical guidelines. Cancer 2005, 104, 1129–1137. [Google Scholar] [CrossRef]
- Hietanen, T.; Pitkänen, M.; Kapanen, M.; Kellokumpu-Lehtinen, P.L. Post-irradiation viability and cytotoxicity of natural killer cells isolated from human peripheral blood using different methods. Int. J. Radiat. Biol. 2016, 92, 71–79. [Google Scholar] [CrossRef] [PubMed]
- Falcke, S.E.; Rühle, P.F.; Deloch, L.; Fietkau, R.; Frey, B.; Gaipl, U.S. Clinically relevant radiation exposure differentially impacts forms of cell death in human cells of the innate and adaptive immune system. Int. J. Mol. Sci. 2018, 19, 3574. [Google Scholar] [CrossRef]
- Hietanen, T.; Pitkänen, M.; Kapanen, M.; Kellokumpu-Lehtinen, P.L. Effects of single and fractionated irradiation on natural killer cell populations: Radiobiological characteristics of viability and cytotoxicity in vitro. Anticancer Res. 2015, 35, 5193–5200. [Google Scholar]
- Yang, G.; Kong, Q.; Wang, G.; Jin, H.; Zhou, L.; Yu, D.; Niu, C.; Han, W.; Li, W.; Cui, J. Low-dose ionizing radiation induces direct activation of natural killer cells and provides a novel approach for adoptive cellular immunotherapy. Cancer Biother. Radiopharm. 2014, 29. [Google Scholar] [CrossRef] [PubMed]
- Eric, A.; Juranic, Z.; Tisma, N.; Plesinac, V.; Borojevic, N.; Jovanovic, D.; Milovanovic, Z.; Gavrilovic, D.; Ilic, B. Radiotherapy-induced changes of peripheral blood lymphocyte subpopulations in cervical cancer patients: Relationship to clinical response. J. BUON 2009, 14, 79–83. [Google Scholar] [PubMed]
- Clave, E.; Socié, G.; Cosset, J.M.; Chaillet, M.P.; Tartour, E.; Girinsky, T.; Carosella, E.; Fridman, H.; Gluckman, E.; Mathiot, C. Multicolor flow cytometry analysis of blood cell subsets in patients given total body irradiation before bone marrow transplantation. Int. J. Radiat. Oncol. Biol. Phys. 1995. [Google Scholar] [CrossRef]
- Louagie, H.; van Eijkeren, M.; Philippe, J.; Thierens, H.; de Ridder, L. Changes in peripheral blood lymphocyte subsets in patients undergoing radiotherapy. Int. J. Radiat. Biol. 1999, 75, 767–771. [Google Scholar] [CrossRef]
- Mozaffari, F.; Lindemalm, C.; Choudhury, A.; Granstam-Björneklett, H.; Helander, I.; Lekander, M.; Mikaelsson, E.; Nilsson, B.; Ojutkangas, M.L.; Österborg, A.; et al. NK-cell and T-cell functions in patients with breast cancer: Effects of surgery and adjuvant chemo- and radiotherapy. Br. J. Cancer 2007, 97, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Nakayama, Y.; Makino, S.; Fukuda, Y.; Ikemoto, T.; Shimizu, A. Varied Effects of Thoracic Irradiation on Peripheral Lymphocyte Subsets in Lung Cancer Patients. Intern. Med. 1995. [Google Scholar] [CrossRef] [PubMed]
- Belka, C.; Ottinger, H.; Kreuzfelder, E.; Weinmann, M.; Lindemann, M.; Lepple-Wienhues, A.; Budach, W.; Grosse-Wilde, H.; Bamberg, M. Impact of localized radiotherapy on blood immune cells counts and function in humans. Radiother. Oncol. 1999. [Google Scholar] [CrossRef]
- Domouchtsidou, A.; Barsegian, V.; Mueller, S.P.; Best, J.; Ertle, J.; Bedreli, S.; Horn, P.A.; Bockisch, A.; Lindemann, M. Impaired lymphocyte function in patients with hepatic malignancies after selective internal radiotherapy. Cancer Immunol. Immunother. 2018. [Google Scholar] [CrossRef]
- Yamaue, H.; Tanimura, H.; Aoki, Y.; Tsunoda, T.; Iwahashi, M.; Tani, M.; Tamai, M.; Noguchi, K.; Kashiwagi, H.; Sasaki, M.; et al. Clinical and immunological evaluation of intraoperative radiation therapy for patients with unresectable pancreatic cancer. J. Surg. Oncol. 1992. [Google Scholar] [CrossRef]
- Blomgren, H.; Baral, E.; Edsmyr, F.; Strender, L.E.; Petrini, B.; Wasserman, J. Natural killer activity in peripheral lymphocyte population following local radiation therapy. Acta Radiol. Oncol. Radiat. Phys. Biol. 1980, 19, 139–143. [Google Scholar] [CrossRef]
- Kim, J.Y.; Son, Y.O.; Park, S.W.; Bae, J.H.; Joo, S.C.; Hyung, H.K.; Chung, B.S.; Kim, S.H.; Kang, C.D. Increase of NKG2D ligands and sensitivity to NK cell-mediated cytotoxicity of tumor cells by heat shock and ionizing radiation. Exp. Mol. Med. 2006, 38, 474–484. [Google Scholar] [CrossRef]
- Fine, J.H.; Chen, P.; Mesci, A.; Allan, D.S.J.; Gasser, S.; Raulet, D.H.; Carlyle, J.R. Chemotherapy-induced genotoxic stress promotes sensitivity to natural killer cell cytotoxicity by enabling missing-self recognition. Cancer Res. 2010, 70, 7102–7113. [Google Scholar] [CrossRef]
- Balaji, G.R.; Aguilar, O.A.; Tanaka, M.; Shingu-Vazquez, M.A.; Fu, Z.; Gully, B.S.; Lanier, L.L.; Carlyle, J.R.; Rossjohn, J.; Berry, R. Recognition of host Clr-b by the inhibitory NKR-P1B receptor provides a basis for missing-self recognition. Nat. Commun. 2018, 9. [Google Scholar] [CrossRef]
- Heo, W.; Lee, Y.S.; Son, C.H.; Yang, K.; Park, Y.S.; Bae, J. Radiation-induced matrix metalloproteinases limit natural killer cell-mediated anticancer immunityin NCI-H23 lung cancer cells. Mol. Med. Rep. 2015, 1800–1806. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Kim, H.W.; Kim, J.E.; Hwang, M.H.; Jeon, Y.H.; Lee, S.W.; Lee, J.; Zeon, S.K.; Ahn, B.C. Enhancement of Natural Killer Cell Cytotoxicity by Sodium/Iodide Symporter Gene-Mediated Radioiodine Pretreatment in Breast Cancer Cells. PLoS ONE 2013, 8, e70194. [Google Scholar] [CrossRef] [PubMed]
- Garnett, C.T.; Palena, C.; Chakarborty, M.; Tsang, K.Y.; Schlom, J.; Hodge, J.W. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res. 2004, 64, 7985–7994. [Google Scholar] [CrossRef]
- Michelin, S.; Gallegos, C.E.; Dubner, D.; Favier, B.; Carosella, E.D. Ionizing radiation modulates the surface expression of human leukocyte antigen-G in a human melanoma cell line. Hum. Immunol. 2009, 70, 1010–1015. [Google Scholar] [CrossRef]
- Urosevic, M.; Kempf, W.; Zagrodnik, B.; Panizzon, R.; Burg, G.; Dummer, R. HLA-G expression in basal cell carcinomas of the skin recurring after radiotherapy. Clin. Exp. Derm. 2005, 422–425. [Google Scholar] [CrossRef]
- Jeong, J.U.; Uong, T.N.T.; Chung, W.K.; Nam, T.K.; Ahn, S.J.; Song, J.Y.; Kim, S.K.; Shin, D.J.; Cho, E.; Kim, K.W.; et al. Effect of irradiation-induced intercellular adhesion molecule-1 expression on natural killer cell-mediated cytotoxicity toward human cancer cells. Cytotherapy 2018, 20, 715–727. [Google Scholar] [CrossRef] [PubMed]
- Ames, E.; Canter, R.J.; Grossenbacher, S.K.; Mac, S.; Smith, R.C.; Monjazeb, A.M.; Chen, M.; Murphy, W.J. Enhanced targeting of stem-like solid tumor cells with radiation and natural killer cells. OncoImmunology 2015, 4, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Shen, M.J.; Xu, L.J.; Yang, L.; Tsai, Y.; Keng, P.C.; Chen, Y.; Lee, S.O.; Chen, Y. Radiation alters PD-L1/NKG2D ligand levels in lung cancer cells and leads to immune escape from NK cell cytotoxicity via IL-6- MEK/Erk signaling pathway. Oncotarget 2017, 8, 80506–80520. [Google Scholar] [CrossRef] [PubMed]
- Multhoff, G.; Botzler, C.; Jennen, L.; Schmidt, J.; Ellwart, J.; Issels, R. Heat shock protein 72 on tumor cells: A recognition structure for natural killer cells. J. Immunol. 1997, 4341–4350. [Google Scholar]
- Multhoff, G.; Pockley, A.G.; Schmid, T.E.; Schilling, D. The role of heat shock protein 70 (Hsp70) in radiation-induced immunomodulation. Cancer Lett. 2015, 179–184. [Google Scholar] [CrossRef]
- Calini, V.; Urani, C.; Camatini, M. Overexpression of HSP70 is induced by ionizing radiation in C3H 10T1/2 cells and protects from DNA damage. Toxicol. In Vitro 2003, 17, 561–566. [Google Scholar] [CrossRef]
- Gastpar, R.; Gross, C.; Rossbacher, L.; Ellwart, J.; Riegger, J.; Multhoff, G. The Cell Surface-Localized Heat Shock Protein 70 Epitope TKD Induces Migration and Cytolytic Activity Selectively in Human NK Cells. J. Immunol. 2004. [Google Scholar] [CrossRef]
- Multhoff, G.; Mizzen, L.; Winchester, C.C.; Milner, C.M.; Wenk, S.; Eissner, G.; Kampinga, H.H.; Laumbacher, B.; Johnson, J. Heat shock protein 70 (Hsp70) stimulates proliferation and cytolytic activity of natural killer cells. Exp. Hematol. 1999, 27, 1627–1636. [Google Scholar] [CrossRef]
- Stangl, S.; Gross, C.; Pockley, A.G.; Asea, A.A.; Multhoff, G. Influence of Hsp70 and HLA-E on the killing of leukemic blasts by cytokine/Hsp70 peptide-activated human natural killer (NK) cells. Cell Stress Chaperones 2008, 13, 221–230. [Google Scholar] [CrossRef] [PubMed]
- Vaupel, P.; Multhoff, G. Adenosine can thwart anti-tumor immune responses elicited by radiotherapy. Strahlenther. Und Onkol. 2016, 192, 279–287. [Google Scholar] [CrossRef]
- Young, A.; Ngiow, S.F.; Gao, Y.; Patch, A.M.; Barkauskas, D.S.; Messaoudene, M.; Lin, G.; Coudert, J.D.; Stannard, K.A.; Zitvogel, L.; et al. A2AR adenosine signaling suppresses natural killer cell maturation in the tumor microenvironment. Cancer Res. 2018, 78, 1003–1016. [Google Scholar] [CrossRef]
- Yoon, M.S.; Pham, C.T.; Phan, M.T.T.; Shin, D.J.; Jang, Y.Y.; Park, M.H.; Kim, S.K.; Kim, S.; Cho, D. Irradiation of breast cancer cells enhances CXCL16 ligand expression and induces the migration of natural killer cells expressing the CXCR6 receptor. Cytotherapy 2016, 18, 1532–1542. [Google Scholar] [CrossRef]
- Thandassery, R.B.; Goenka, U.; Goenka, M.K. Role of Local Ablative Therapy for hepatocellular carcinoma. J. Clin. Exp. Hepatol. 2014, 4, S104–S111. [Google Scholar] [CrossRef] [PubMed]
- Smith, S.L.; Jennings, P.E. Lung radiofrequency and microwave ablation: A review of indications, techniques and post-procedural imaging appearances. Br. J. Radiol. 2015, 88. [Google Scholar] [CrossRef]
- Deng, Z.; Zhang, W.; Han, Y.; Zhang, S. Radiofrequency ablation inhibits lung metastasis ofbreast cancer in mice. Zhonghua Zhong Liu Za Zhi 2015, 37, 497–500. [Google Scholar] [PubMed]
- Mo, Z.; Lu, H.; Mo, S.; Fu, X.; Chang, S.; Yue, J. Ultrasound-guided radiofrequency ablation enhances natural killer-mediated antitumor immunity against liver cancer. Oncol. Lett. 2018, 15, 7014–7020. [Google Scholar] [CrossRef]
- Todorova, V.K.; Klimberg, V.S.; Hennings, L.; Kieber-Emmons, T.; Pashov, A. Immunomodulatory effects of radiofrequency ablation in a breast cancer model. Immunol. Investig. 2010, 39, 74–92. [Google Scholar] [CrossRef] [PubMed]
- Matuszewski, M.; Michajłowski, J.; Michajłowski, I.; Ruckermann-Dizurdzińska, K.; Witkowski, J.M.; Biernat, W.; Krajka, K. Impact of radiofrequency ablation on PBMC subpopulation in patients with renal cell carcinoma. Urol. Oncol. Semin. Orig. Investig. 2011, 29, 724–730. [Google Scholar] [CrossRef] [PubMed]
- Zerbini, A.; Pilli, M.; Laccabue, D.; Pelosi, G.; Molinari, A.; Negri, E.; Cerioni, S.; Fagnoni, F.; Soliani, P.; Ferrari, C.; et al. Radiofrequency Thermal Ablation for Hepatocellular Carcinoma Stimulates Autologous NK-Cell Response. Gastroenterology 2010, 138, 1931–1942.e2. [Google Scholar] [CrossRef] [PubMed]
- Guan, H.T.; Wang, J.; Yang, M.; Song, L.; Tong, X.Q.; Zou, Y.H. Changes in immunological function after treatment with transarterial chemoembolization plus radiofrequency ablation in hepatocellular carcinoma patients. Chin. Med. J. 2013, 126, 3651–3655. [Google Scholar] [CrossRef]
- Rochigneux, P.; Nault, J.C.; Mallet, F.; Chretien, A.S.; Barget, N.; Garcia, A.J.; del Pozo, L.; Bourcier, V.; Blaise, L.; Grando-Lemaire, V.; et al. Dynamic of systemic immunity and its impact on tumor recurrence after radiofrequency ablation of hepatocellular carcinoma. OncoImmunology 2019, 8, 1–11. [Google Scholar] [CrossRef]
- Lencioni, R. Loco-regional treatment of hepatocellular carcinoma. Hepatology 2010, 52, 762–773. [Google Scholar] [CrossRef]
- Yu, M.; Pan, H.; Che, N.; Li, L.; Wang, C.; Wang, Y.; Ma, G.; Qian, M.; Liu, J.; Zheng, M.; et al. Microwave ablation of primary breast cancer inhibits metastatic progression in model mice via activation of natural killer cells. Cell. Mol. Immunol. 2020, 1–12. [Google Scholar] [CrossRef]
- Dong, B.W.; Zhang, J.; Liang, P.; Yu, X.L.; Su, L.; Yu, D.J.; Ji, X.L.; Yu, G. Sequential pathological and immunologic analysis of percutaneous microwave coagulation therapy of hepatocellular carcinoma. Int. J. Hyperth. 2003, 19, 119–133. [Google Scholar] [CrossRef]
- Zhang, H.; Hou, X.; Cai, H.; Zhuang, X. Effects of microwave ablation on T-cell subsets and cytokines of patients with hepatocellular carcinoma. Minim. Invasive Allied Technol. 2017, 26, 207–211. [Google Scholar] [CrossRef]
- Szmigielski, S.; Sobczynski, J.; Sokolska, G.; Stawarz, B.; Zielinski, H.; Petrovich, Z. Effects of local prostatic hyperthermia on human NK and t cell function. Int. J. Hyperth. 1991, 7, 869–880. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Wang, Z.B. High-intensity focused ultrasound tumor ablation: Review of ten years of clinical experience. Front. Med. China 2010, 4, 294–302. [Google Scholar] [CrossRef]
- Wu, F.; Wang, Z.B.; Lu, P.; Xu, Z.L.; Chen, W.Z.; Zhu, H.; Jin, C.B. Activated anti-tumor immunity in cancer patients after high intensity focused ultrasound ablation. Ultrasound Med. Biol. 2004, 30, 1217–1222. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Qin, J.; Chen, J.; Wang, L.; Chen, W.; Tang, L. The effect of high-intensity focused ultrasound treatment on immune function in patients with uterine fibroids. Int. J. Hyperth. 2013, 29, 225–233. [Google Scholar] [CrossRef]
- Ma, B.; Liu, X.; Yu, Z. The effect of high intensity focused ultrasound on the treatment of liver cancer and patients’ immunity. Cancer Biomark. 2019, 24, 85–90. [Google Scholar] [CrossRef]
- Lu, P.; Zhu, X.Q.; Xu, Z.L.; Zhou, Q.; Zhang, J.; Wu, F. Increased infiltration of activated tumor-infiltrating lymphocytes after high intensity focused ultrasound ablation of human breast cancer. Surgery 2009, 145, 286–293. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, C.M.; White, M.J.; Goodier, M.R.; Riley, E.M. Functional significance of CD57 expression on human NK cells and relevance to disease. Front. Immunol. 2013, 4, 422. [Google Scholar] [CrossRef]
- Kim, N.; Kim, H.S. Targeting checkpoint receptors and molecules for therapeutic modulation of natural killer cells. Front. Immunol. 2018, 9, 2041. [Google Scholar] [CrossRef]
- Niu, C.; Li, M.; Zhu, S.; Chen, Y.; Zhou, L.; Xu, D.; Xu, J.; Li, Z.; Li, W.; Cui, J. Pd-1-positive natural killer cells have a weaker antitumor function than that of pd-1-negative natural killer cells in lung cancer. Int. J. Med. Sci. 2020, 17, 1964–1973. [Google Scholar] [CrossRef]
- Pesce, S.; Greppi, M.; Tabellini, G.; Rampinelli, F.; Parolini, S.; Olive, D.; Moretta, L.; Moretta, A.; Marcenaro, E. Identification of a subset of human natural killer cells expressing high levels of programmed death 1: A phenotypic and functional characterization. J. Allergy Clin. Immunol. 2017, 139, 335–346.e3. [Google Scholar] [CrossRef]
- Tumino, N.; Martini, S.; Munari, E.; Scordamaglia, F.; Besi, F.; Mariotti, F.R.; Bogina, G.; Mingari, M.C.; Vacca, P.; Moretta, L. Presence of innate lymphoid cells in pleural effusions of primary and metastatic tumors: Functional analysis and expression of PD-1 receptor. Int. J. Cancer 2019, 145, 1660–1668. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Cheng, Y.; Xu, Y.; Wang, Z.; Du, X.; Li, C.; Peng, J.; Gao, L.; Liang, X.; Ma, C. Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive cancers. Oncogene 2017, 36, 6143–6153. [Google Scholar] [CrossRef]
- Concha-Benavente, F.; Kansy, B.; Moskovitz, J.; Moy, J.; Chandran, U.; Ferris, R.L. PD-L1 Mediates Dysfunction in Activated PD-1+ NK Cells in Head and Neck Cancer Patients. Cancer Immunol. Res. 2018, 6, 1548–1560. [Google Scholar] [CrossRef]
- Trefny, M.P.; Kaiser, M.; Stanczak, M.A.; Herzig, P.; Savic, S.; Wiese, M.; Lardinois, D.; Läubli, H.; Uhlenbrock, F.; Zippelius, A. PD-1+ natural killer cells in human non-small cell lung cancer can be activated by PD-1/PD-L1 blockade. Cancer Immunol. Immunother. 2020, 69, 1505–1517. [Google Scholar] [CrossRef]
- Hsu, J.; Hodgins, J.J.; Marathe, M.; Nicolai, C.J.; Bourgeois-Daigneault, M.C.; Trevino, T.N.; Azimi, C.S.; Scheer, A.K.; Randolph, H.E.; Thompson, T.W.; et al. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J. Clin. Investig. 2018, 128, 4654–4668. [Google Scholar] [CrossRef] [PubMed]
- Oyer, J.L.; Gitto, S.B.; Altomare, D.A.; Copik, A.J. PD-L1 blockade enhances anti-tumor efficacy of NK cells. Oncoimmunology 2018, 7. [Google Scholar] [CrossRef]
- Juliá, E.P.; Amante, A.; Pampena, M.B.; Mordoh, J.; Levy, E.M. Avelumab, an IgG1 anti-PD-L1 immune checkpoint inhibitor, triggers NK cell-mediated cytotoxicity and cytokine production against triple negative breast cancer cells. Front. Immunol. 2018, 9. [Google Scholar] [CrossRef]
- Boyerinas, B.; Jochems, C.; Fantini, M.; Heery, C.R.; Gulley, J.L.; Tsang, K.Y.; Schlom, J. Antibody-dependent cellular cytotoxicity activity of a Novel Anti-PD-L1 antibody avelumab (MSB0010718C) on human tumor cells. Cancer Immunol. Res. 2015, 3, 1148–1157. [Google Scholar] [CrossRef]
- Barry, K.C.; Hsu, J.; Broz, M.L.; Cueto, F.J.; Binnewies, M.; Combes, A.J.; Nelson, A.E.; Loo, K.; Kumar, R.; Rosenblum, M.D.; et al. A natural killer–dendritic cell axis defines checkpoint therapy–responsive tumor microenvironments. Nat. Med. 2018, 24, 1178–1191. [Google Scholar] [CrossRef]
- Deng, L.; Weichselbaum, R.R.; Fu, Y.; Deng, L.; Liang, H.; Burnette, B.; Beckett, M. Irradiation and anti—PD-L1 treatment synergistically promote antitumor immunity in mice Find the latest version: Irradiation and anti—PD-L1 treatment synergistically promote antitumor immunity in mice. J. Clin. Investig. 2014, 124, 687–695. [Google Scholar] [CrossRef]
- Makowska, A.; Meier, S.; Shen, L.; Busson, P.; Baloche, V.; Kontny, U. Anti-PD-1 antibody increases NK cell cytotoxicity towards nasopharyngeal carcinoma cells in the context of chemotherapy-induced upregulation of PD-1 and PD-L1. Cancer Immunol. Immunother. 2020. [Google Scholar] [CrossRef] [PubMed]
- Cameron, F.; Whiteside, G.; Perry, C. Ipilimumab: First global approval. Drugs 2011, 71, 1093–1104. [Google Scholar] [CrossRef] [PubMed]
- Patel, V.; Gandhi, H.; Upaganlawar, A. Ipilimumab: Melanoma and beyond. J. Pharm. Bioallied Sci. 2011, 3, 546. [Google Scholar]
- Cabel, L.; Loir, E.; Gravis, G.; Lavaud, P.; Massard, C.; Albiges, L.; Baciarello, G.; Loriot, Y.; Fizazi, K. Long-term complete remission with Ipilimumab in metastatic castrate-resistant prostate cancer: Case report of two patients. J. Immunother. Cancer 2017, 5. [Google Scholar] [CrossRef]
- Stojanovic, A.; Fiegler, N.; Brunner-Weinzierl, M.; Cerwenka, A. CTLA-4 Is Expressed by Activated Mouse NK Cells and Inhibits NK Cell IFN-γ Production in Response to Mature Dendritic Cells. J. Immunol. 2014, 192, 4184–4191. [Google Scholar] [CrossRef]
- Lang, S.; Vujanovic, N.L.; Wollenberg, B.; Whiteside, T.L. Absence of B7.1-CD28/CTLA-4-mediated co-stimulation in human NK cells. Eur. J. Immunol. 1998, 28, 780–786. [Google Scholar] [CrossRef]
- Hutmacher, C.; Nuñez, N.G.; Liuzzi, A.R.; Becher, B.; Neri, D. Targeted delivery of IL2 to the tumor stroma potentiates the action of immune checkpoint inhibitors by preferential activation of NK and CD8þ T cells. Cancer Immunol. Res. 2019, 7, 572–583. [Google Scholar] [CrossRef]
- Kohlhapp, F.J.; Broucek, J.R.; Hughes, T.; Huelsmann, E.J.; Lusciks, J.; Zayas, J.P.; Dolubizno, H.; Fleetwood, V.A.; Grin, A.; Hill, G.E.; et al. NK cells and CD8+ T cells cooperate to improve therapeutic responses in melanoma treated with interleukin-2 (IL-2) and CTLA-4 blockade. J. Immunother. Cancer 2015, 3. [Google Scholar] [CrossRef]
- Sanseviero, E.; Karras, J.R.; Shabaneh, T.B.; Arman, B.; Xu, W.; Zheng, C.; Yin, X.; Xu, X.; Karakousis, G.; Nam, B.T.; et al. Anti-CTLA4 activates intratumoral NK cells and combination with IL15/IL15Rα complexes enhances tumor control. Cancer Immunol. Res. 2020, 7, 1371–1380. [Google Scholar] [CrossRef]
- Tallerico, R.; Cristiani, C.M.; Staaf, E.; Garofalo, C.; Sottile, R.; Capone, M.; de Coaña, Y.P.; Madonna, G.; Palella, E.; Wolodarski, M.; et al. IL-15, TIM-3 and NK cells subsets predict responsiveness to anti-CTLA-4 treatment in melanoma patients. OncoImmunology 2017, 6. [Google Scholar] [CrossRef]
- Sottile, R.; Tannazi, M.; Johansson, M.H.; Cristiani, C.M.; Calabró, L.; Ventura, V.; Cutaia, O.; Chiarucci, C.; Covre, A.; Garofalo, C.; et al. NK- and T-cell subsets in malignant mesothelioma patients: Baseline pattern and changes in the context of anti-CTLA-4 therapy. Int. J. Cancer 2019, 145, 2238–2248. [Google Scholar] [CrossRef]
- Tietze, J.K.; Angelova, D.; Heppt, M.V.; Ruzicka, T.; Berking, C. Low baseline levels of NK cells may predict a positive response to ipilimumab in melanoma therapy. Exp. Derm. 2017, 26, 622–629. [Google Scholar] [CrossRef] [PubMed]
- Jie, H.B.; Schuler, P.J.; Lee, S.C.; Srivastava, R.M.; Argiris, A.; Ferrone, S.; Whiteside, T.L.; Ferris, R.L. CTLA-4+ regulatory t cells increased in cetuximab-treated head and neck cancer patients suppress nk cell cytotoxicity and correlate with poor prognosis. Cancer Res. 2015, 75, 2200–2210. [Google Scholar] [CrossRef] [PubMed]
- Romano, E.; Kusio-Kobialka, M.; Foukas, P.G.; Baumgaertner, P.; Meyer, C.; Ballabeni, P.; Michielin, O.; Weide, B.; Romero, P.; Speiser, D.E. Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients. Proc. Natl. Acad. Sci. USA 2015. [Google Scholar] [CrossRef]
- Simpson, T.R.; Li, F.; Montalvo-Ortiz, W.; Sepulveda, M.A.; Bergerhoff, K.; Arce, F.; Roddie, C.; Henry, J.Y.; Yagita, H.; Wolchok, J.D.; et al. Fc-dependent depletion of tumor-infiltrating regulatory t cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J. Exp. Med. 2013. [Google Scholar] [CrossRef]
- Vargas, F.A.; Furness, A.J.S.; Litchfield, K.; Joshi, K.; Rosenthal, R.; Ghorani, E.; Solomon, I.; Lesko, M.H.; Ruef, N.; Roddie, C.; et al. Fc Effector Function Contributes to the Activity of Human Anti-CTLA-4 Antibodies. Cancer Cell 2018, 33, 649–663.e4. [Google Scholar] [CrossRef]
- Laurent, S.; Queirolo, P.; Boero, S.; Salvi, S.; Piccioli, P.; Boccardo, S.; Minghelli, S.; Morabito, A.; Fontana, V.; Pietra, G.; et al. The engagement of CTLA-4 on primary melanoma cell lines induces antibody-dependent cellular cytotoxicity and TNF-α production. J. Transl. Med. 2013, 11, 1–13. [Google Scholar] [CrossRef]
- Da Silva, I.P.; Gallois, A.; Jimenez-Baranda, S.; Khan, S.; Anderson, A.C.; Kuchroo, V.K.; Osman, I.; Bhardwaj, N. Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol. Res. 2014, 2, 410–422. [Google Scholar] [CrossRef]
- Komita, H.; Koido, S.; Hayashi, K.; Kan, S.; Ito, M.; Kamata, Y.; Suzuki, M.; Homma, S. Expression of immune checkpoint molecules of T cell immunoglobulin and mucin protein 3/galectin-9 for NK cell suppression in human gastrointestinal stromal tumors. Oncol. Rep. 2015, 34, 2099–2105. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.; Huang, Y.; Tan, L.; Yu, W.; Chen, D.; Lu, C.; He, J.; Wu, G.; Liu, X.; Zhang, Y. Increased Tim-3 expression in peripheral NK cells predicts a poorer prognosis and Tim-3 blockade improves NK cell-mediated cytotoxicity in human lung adenocarcinoma. Int. Immunopharmacol. 2015, 29, 635–641. [Google Scholar] [CrossRef]
- Datar, I.; Sanmamed, M.F.; Wang, J.; Henick, B.S.; Choi, J.; Badri, T.; Dong, W.; Mani, N.; Toki, M.; Mejías, L.D.; et al. Expression analysis and significance of PD-1, LAG-3, and TIM-3 in human non-small cell lung cancer using spatially resolved and multiparametric single-cell analysis. Clin. Cancer Res. 2019, 25, 4663–4673. [Google Scholar] [CrossRef] [PubMed]
- Tan, S.; Xu, Y.; Wang, Z.; Wang, T.; Du, X.; Song, X.; Guo, X.; Peng, J.; Zhang, J.; Liang, Y.; et al. Tim-3 hampers tumor surveillance of liver-resident and conventional NK cells by disrupting PI3K signaling. Cancer Res. 2020, 80, 1130–1142. [Google Scholar] [CrossRef]
- Seo, H.; Kim, B.S.; Bae, E.A.; Min, B.S.; Han, Y.D.; Shin, S.J.; Kang, C.Y. IL21 therapy combined with PD-1 and Tim-3 blockade provides enhanced NK cell antitumor activity against MHC class I-deficient tumors. Cancer Immunol. Res. 2018, 6, 685–695. [Google Scholar] [CrossRef]
- Gleason, M.K.; Lenvik, T.R.; McCullar, V.; Felices, M.; O’Brien, M.S.; Cooley, S.A.; Verneris, M.R.; Cichocki, F.; Holman, C.J.; Panoskaltsis-Mortari, A.; et al. Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 2012, 119, 3064–3072. [Google Scholar] [CrossRef] [PubMed]
- So, E.C.; Khaladj-Ghom, A.; Ji, Y.; Amin, J.; Song, Y.; Burch, E.; Zhou, H.; Sun, H.; Chen, S.; Bentzen, S.; et al. NK cell expression of Tim-3: First impressions matter. Immunobiology 2019, 224, 362–370. [Google Scholar] [CrossRef] [PubMed]
- Sarhan, D.; Cichocki, F.; Zhang, B.; Yingst, A.; Spellman, S.R.; Cooley, S.; Verneris, M.R.; Blazar, B.R.; Miller, J.S. Adaptive NK cells with low TIGIT expression are inherently resistant to myeloid-derived suppressor cells. Cancer Res. 2016, 76, 5696–5706. [Google Scholar] [CrossRef] [PubMed]
- Blake, S.J.; Stannard, K.; Liu, J.; Allen, S.; Yong, M.C.R.; Mittal, D.; Aguilera, A.R.; Miles, J.J.; Lutzky, V.P.; de Andrade, L.F.; et al. Suppression of metastases using a new lymphocyte checkpoint target for cancer immunotherapy. Cancer Discov. 2016, 6, 446–459. [Google Scholar] [CrossRef]
- Wang, F.; Hou, H.; Wu, S.; Tang, Q.; Liu, W.; Huang, M.; Yin, B.; Huang, J.; Mao, L.; Lu, Y.; et al. TIGIT expression levels on human NK cells correlate with functional heterogeneity among healthy individuals. Eur. J. Immunol. 2015, 45, 2886–2897. [Google Scholar] [CrossRef]
- Peng, Y.P.; Xi, C.H.; Zhu, Y.; di Yin, L.; Wei, J.S.; Zhang, J.J.; Liu, X.C.; Guo, S.; Fu, Y.; Miao, Y. Altered expression of CD226 and CD96 on natural killer cells in patients with pancreatic cancer. Oncotarget 2016, 7, 66586–66594. [Google Scholar] [CrossRef]
- Zhang, Q.; Bi, J.; Zheng, X.; Chen, Y.; Wang, H.; Wu, W.; Wang, Z.; Wu, Q.; Peng, H.; Wei, H.; et al. Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat. Immunol. 2018, 19, 723–732. [Google Scholar] [CrossRef]
- Stanietsky, N.; Simic, H.; Arapovic, J.; Toporik, A.; Levy, O.; Novik, A.; Levine, Z.; Beiman, M.; Dassa, L.; Achdout, H.; et al. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc. Natl. Acad. Sci. USA 2009, 106, 17858–17863. [Google Scholar] [CrossRef]
- Sun, H.; Huang, Q.; Huang, M.; Wen, H.; Lin, R.; Zheng, M.; Qu, K.; Li, K.; Wei, H.; Xiao, W.; et al. Human CD96 Correlates to Natural Killer Cell Exhaustion and Predicts the Prognosis of Human Hepatocellular Carcinoma. Hepatology 2019, 70. [Google Scholar] [CrossRef] [PubMed]
- Chan, C.J.; Martinet, L.; Gilfillan, S.; Souza-Fonseca-Guimaraes, F.; Chow, M.T.; Town, L.; Ritchie, D.S.; Colonna, M.; Andrews, D.M.; Smyth, M.J. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat. Immunol. 2014, 15, 431–438. [Google Scholar] [CrossRef]
- Brooks, J.; Fleischmann-Mundt, B.; Woller, N.; Niemann, J.; Ribback, S.; Peters, K.; Demir, I.E.; Armbrecht, N.; Ceyhan, G.O.; Manns, M.P.; et al. Perioperative, spatiotemporally coordinated activation of T and NK cells prevents recurrence of pancreatic cancer. Cancer Res. 2018, 78, 475–488. [Google Scholar] [CrossRef]
- Roman Aguilera, A.; Lutzky, V.P.; Mittal, D.; Li, X.Y.; Stannard, K.; Takeda, K.; Bernhardt, G.; Teng, M.W.L.; Dougall, W.C.; Smyth, M.J. CD96 targeted antibodies need not block CD96-CD155 interactions to promote NK cell anti-metastatic activity. OncoImmunology 2018, 7. [Google Scholar] [CrossRef] [PubMed]
- Baixeras, E.; Huard, B.; Miossec, C.; Jitsukawa, S.; Martin, M.; Hercend, T.; Auffray, C.; Triebel, F.; Piatier-Tonneau, D. Characterization of the Lymphocyte Activation Gene 3-Encoded Protein. A New Ligand for Human Leukocy Antigen Class H Antigens. J. Exp. Med. 1992, 176, 327–337. [Google Scholar] [CrossRef] [PubMed]
- Huard, B.; Tournier, M.; Triebel, F. LAG-3 does not define a specific mode of natural killing in human. Immunol. Lett. 1998, 61, 109–112. [Google Scholar] [CrossRef]
- Zingoni, A.; Fionda, C.; Borrelli, C.; Cippitelli, M.; Santoni, A.; Soriani, A. Natural Killer Cell Response to Chemotherapy-Stressed Cancer Cells: Role in Tumor Immunosurveillance. Front. Immunol. 2017, 8, 1194. [Google Scholar] [CrossRef] [PubMed]
- Zitvogel, L.; Apetoh, L.; Ghiringhelli, F.; Kroemer, G. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 2008, 8, 59–73. [Google Scholar] [CrossRef] [PubMed]
- Carson, W.E., 3rd; Shapiro, C.L.; Crespin, T.R.; Thornton, L.M.; Andersen, B.L. Cellular immunity in breast cancer patients completing taxane treatment. Clin. Cancer Res. 2004, 10, 3401–3409. [Google Scholar] [CrossRef] [PubMed]
- Verma, C.; Kaewkangsadan, V.; Eremin, J.M.; Cowley, G.P.; Ilyas, M.; El-Sheemy, M.A.; Eremin, O. Natural killer (NK) cell profiles in blood and tumour in women with large and locally advanced breast cancer (LLABC) and their contribution to a pathological complete response (PCR) in the tumour following neoadjuvant chemotherapy (NAC): Differential rest. J. Transl. Med. 2015, 13, 180. [Google Scholar] [CrossRef]
- Krysko, D.V.; Garg, A.D.; Kaczmarek, A.; Krysko, O.; Agostinis, P.; Vandenabeele, P. Immunogenic cell death and DAMPs in cancer therapy. Nat. Rev. Cancer 2012, 12, 860–875. [Google Scholar] [CrossRef]
- Swift, L.H.; Golsteyn, R.M. Genotoxic Anti-Cancer Agents and Their Relationship to DNA Damage, Mitosis, and Checkpoint Adaptation in Proliferating Cancer Cells. Int. J. Mol. Sci. 2014, 15, 3403–3431. [Google Scholar] [CrossRef]
- Markasz, L.; Stuber, G.; Vanherberghen, B.; Flaberg, E.; Olah, E.; Carbone, E.; Eksborg, S.; Klein, E.; Skribek, H.; Szekely, L. Effect of frequently used chemotherapeutic drugs on the cytotoxic activity of human natural killer cells. Mol. Cancer 2007, 6, 644. [Google Scholar] [CrossRef]
- Multhoff, G.; Meier, T.; Botzler, C.; Wiesnet, M.; Allenbacher, A.; Wilmanns, W.; Issels, R.D. Differential effects of ifosfamide on the capacity of cytotoxic T lymphocytes and natural killer cells to lyse their target cells correlate with intracellular glutathione levels. Blood 1995, 85, 2124–2131. [Google Scholar] [CrossRef]
- Botzler, C.; Kis, K.; Issels, R.; Multhoff, G. A comparison of the effects of ifosfamide vs. mafosfamide treatment on intracellular glutathione levels and immunological functions of immunocompetent lymphocyte subsets. Exp. Hematol. 1997, 25, 338–344. [Google Scholar]
- Kuppner, M.C.; Bleifuß, E.; Noessner, E.; Mocikat, R.; von Hesler, C.; Mayerhofer, C.; Issels, R.D. Differential effects of ifosfamide on dendritic cell-mediated stimulation of T cell interleukin-2 production, natural killer cell cytotoxicity and interferon-γ production. Clin. Exp. Immunol. 2008, 153, 429–438. [Google Scholar] [CrossRef]
- Ghiringhelli, F.; Menard, C.; Puig, P.E.; Ladoire, S.; Roux, S.; Martin, F.; Solary, E.; le Cesne, A.; Zitvogel, L.; Chauffert, B. Metronomic cyclophosphamide regimen selectively depletes CD4+ CD25+ regulatory T cells and restores T and NK effector functions in end stage cancer patients. Cancer Immunol. Immunother. 2007, 56, 641–648. [Google Scholar] [CrossRef]
- Siew, Y.Y.; Neo, S.Y.; Yew, H.C.; Lim, S.W.; Ng, Y.C.; Lew, S.M.; Seetoh, W.G.; Seow, S.V.; Koh, H.L. Oxaliplatin regulates expression of stress ligands in ovarian cancer cells and modulates their susceptibility to natural killer cell-mediated cytotoxicity. Int. Immunol. 2015, 27, 621–632. [Google Scholar] [CrossRef] [PubMed]
- Veneziani, I.; Brandetti, E.; Ognibene, M.; Pezzolo, A.; Pistoia, V.; Cifaldi, L. Neuroblastoma cell lines are refractory to genotoxic drug-mediated induction of ligands for NK cell-activating receptors. J. Immunol. Res. 2018, 2018. [Google Scholar] [CrossRef] [PubMed]
- Tesniere, A.; Schlemmer, F.; Boige, V.; Kepp, O.; Martins, I.; Ghiringhelli, F.; Aymeric, L.; Michaud, M.; Apetoh, L.; Barault, L.; et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010, 29, 482–491. [Google Scholar] [CrossRef] [PubMed]
- Okita, R.; Yukawa, T.; Nojima, Y.; Maeda, A.; Saisho, S.; Shimizu, K.; Nakata, M. MHC class I chain-related molecule A and B expression is upregulated by cisplatin and associated with good prognosis in patients with non-small cell lung cancer. Cancer Immunol. Immunother. 2016, 65, 499–509. [Google Scholar] [CrossRef]
- Okita, R.; Maeda, A.; Shimizu, K.; Nojima, Y.; Saisho, S.; Nakata, M. Effect of platinum-based chemotherapy on the expression of natural killer group 2 member D ligands, programmed cell death-1 ligand 1 and HLA class i in non-small cell lung cancer. Oncol. Rep. 2019, 42, 839–848. [Google Scholar] [CrossRef]
- Shi, L.; Lin, H.; Li, G.; Sun, Y.; Shen, J.; Xu, J.; Lin, C.; Yeh, S.; Cai, X.; Chang, C. Cisplatin enhances NK cells immunotherapy efficacy to suppress HCC progression via altering the androgen receptor (AR)-ULBP2 signals. Cancer Lett. 2016, 373, 45–56. [Google Scholar] [CrossRef]
- Cao, G.; Wang, J.; Zheng, X.; Wei, H.; Tian, Z.; Sun, R. Tumor Therapeutics Work as Stress Inducers to Enhance Tumor Sensitivity to Natural Killer (NK) Cell Cytolysis by Up-regulating NKp30 Ligand B7-H6. J. Biol. Chem. 2015, 290, 29964–29973. [Google Scholar] [CrossRef]
- Guerriero, J.L.; Ditsworth, D.; Catanzaro, J.M.; Sabino, G.; Furie, M.B.; Kew, R.R.; Crawford, H.C.; Zong, W.-X. DNA Alkylating Therapy Induces Tumor Regression through an HMGB1-Mediated Activation of Innate Immunity. J. Immunol. 2011, 186, 3517–3526. [Google Scholar] [CrossRef] [PubMed]
- Martins, I.; Tesniere, A.; Kepp, O.; Michaud, M.; Schlemmer, F.; Senovilla, L.; Séror, C.; Métivier, D.; Perfettini, J.-L.; Zitvogel, L.; et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 2009, 8, 3723–3728. [Google Scholar] [CrossRef] [PubMed]
- Čermák, V.; Dostál, V.; Jelínek, M.; Libusová, L.; Kovář, J.; Rösel, D.; Brábek, J. Microtubule-targeting agents and their impact on cancer treatment. Eur. J. Cell Biol. 2020, 99, 151075. [Google Scholar] [CrossRef]
- Sako, T.; Burioka, N.; Yasuda, K.; Tomita, K.; Miyata, M.; Kurai, J.; Chikumi, H.; Watanabe, M.; Suyama, H.; Fukuoka, Y.; et al. Cellular Immune Profile in Patients with Non-small Cell Lung Cancer after Weekly Paclitaxel Therapy. Acta Oncol. 2004, 43, 15–19. [Google Scholar] [CrossRef]
- Tong, A.W.; Seamour, B.; Lawson, J.M.; Ordonez, G.; Vukelja, S.; Hyman, W.; Richards, D.; Stein, L.; Maples, P.B.; Nemunaitis, J. Cellular immune profile of patients with advanced cancer before and after taxane treatment. Am. J. Clin. Oncol. Cancer Clin. Trials 2000, 23, 463–472. [Google Scholar] [CrossRef]
- Wu, X.; Feng, Q.M.; Wang, Y.; Shi, J.; Ge, H.L.; Di, W. The immunologic aspects in advanced ovarian cancer patients treated with paclitaxel and carboplatin chemotherapy. Cancer Immunol. Immunother. 2010, 59, 279–291. [Google Scholar] [CrossRef] [PubMed]
- Acebes-Huerta, A.; Lorenzo-Herrero, S.; Folgueras, A.R.; Huergo-Zapico, L.; Lopez-Larrea, C.; López-Soto, A.; Gonzalez, S. Drug-induced hyperploidy stimulates an antitumor NK cell response mediated by NKG2D and DNAM-1 receptors. OncoImmunology 2016, 5. [Google Scholar] [CrossRef] [PubMed]
- di Modica, M.; Sfondrini, L.; Regondi, V.; Varchetta, S.; Oliviero, B.; Mariani, G.; Bianchi, G.V.; Generali, D.; Balsari, A.; Triulzi, T.; et al. Taxanes enhance trastuzumab-mediated ADCC on tumor cells through NKG2D-mediated NK cell recognition. Oncotarget 2016, 7, 255–265. [Google Scholar] [CrossRef]
- Luengo, A.; Gui, D.Y.; van der Heiden, M.G. Targeting Metabolism for Cancer Therapy. Cell Chem. Biol. 2017, 24, 1161–1180. [Google Scholar] [CrossRef]
- Soriani, A.; Zingoni, A.; Cerboni, C.; Iannitto, M.L.; Ricciardi, M.R.; di Gialleonardo, V.; Cippitelli, M.; Fionda, C.; Petrucci, M.T.; Guarini, A.; et al. ATM-ATR–dependent up-regulation of DNAM-1 and NKG2D ligands on multiple myeloma cells by therapeutic agents results in enhanced NK-cell susceptibility and is associated with a senescent phenotype. Blood 2009, 113, 3503–3511. [Google Scholar] [CrossRef]
- Soriani, A.; Iannitto, M.L.; Ricci, B.; Fionda, C.; Malgarini, G.; Morrone, S.; Peruzzi, G.; Ricciardi, M.R.; Petrucci, M.T.; Cippitelli, M.; et al. Reactive oxygen species–and DNA damage response–dependent NK cell activating ligand upregulation occurs at transcriptional levels and requires the transcriptional factor E2F1. J. Immunol. 2014. [Google Scholar] [CrossRef] [PubMed]
- Rayner, D.M.; Cutts, S.M. Anthracyclines. In Side Effects of Drugs Annual; Elsevier B.V.: Amsterdam, The Netherlands, 2014; Volume 36, pp. 683–694. [Google Scholar]
- Feng, H.; Dong, Y.; Wu, J.; Qiao, Y.; Zhu, G.; Jin, H.; Cui, J.; Li, W.; Liu, Y.J.; Chen, J.; et al. Epirubicin pretreatment enhances NK cell-mediated cytotoxicity against breast cancer cells in vitro. Am. J. Transl. Res. 2016, 8, 473–484. [Google Scholar]
- Wennerberg, E.; Sarhan, D.; Carlsten, M.; Kaminskyy, V.O.; D’Arcy, P.; Zhivotovsky, B.; Childs, R.; Lundqvist, A. Doxorubicin sensitizes human tumor cells to NK cell- and T-cell-mediated killing by augmented TRAIL receptor signaling. Int. J. Cancer 2013, 133, 1643–1652. [Google Scholar] [CrossRef] [PubMed]
- Hull, E.E.; Montgomery, M.R.; Leyva, K.J. HDAC Inhibitors as Epigenetic Regulators of the Immune System: Impacts on Cancer Therapy and Inflammatory Diseases. BioMed Res. Int. 2016, 2016, 1–15. [Google Scholar] [CrossRef]
- Ogbomo, H.; Michaelis, M.; Kreuter, J.; Doerr, H.W.; Cinatl, J. Histone deacetylase inhibitors suppress natural killer cell cytolytic activity. Febs Lett. 2007, 581, 1317–1322. [Google Scholar] [CrossRef]
- Ni, L.; Wang, L.; Yao, C.; Ni, Z.; Liu, F.; Gong, C.; Zhu, X.; Yan, X.; Watowich, S.S.; Lee, D.A.; et al. The histone deacetylase inhibitor valproic acid inhibits NKG2D expression in natural killer cells through suppression of STAT3 and HDAC3. Sci. Rep. 2017, 7. [Google Scholar] [CrossRef] [PubMed]
- Kelly-Sell, M.J.; Kim, Y.H.; Straus, S.; Benoit, B.; Harrison, C.; Sutherland, K.; Armstrong, R.; Weng, W.-K.; Showe, L.C.; Wysocka, M.; et al. The histone deacetylase inhibitor, romidepsin, suppresses cellular immune functions of cutaneous T-cell lymphoma patients. Am. J. Hematol. 2012, 87, 354–360. [Google Scholar] [CrossRef] [PubMed]
- Armeanu, S.; Bitzer, M.; Lauer, U.M.; Venturelli, S.; Pathil, A.; Krusch, M.; Kaiser, S.; Jobst, J.; Smirnow, I.; Wagner, A.; et al. Natural killer cell-mediated lysis of hepatoma cells via specific induction of NKG2D ligands by the histone deacetylase inhibitor sodium valproate. Cancer Res. 2005, 65, 6321–6329. [Google Scholar] [CrossRef]
- Shi, P.; Yin, T.; Zhou, F.; Cui, P.; Gou, S.; Wang, C. Valproic acid sensitizes pancreatic cancer cells to natural killer cell-mediated lysis by upregulating MICA and MICB via the PI3K/Akt signaling pathway. BMC Cancer 2014, 14. [Google Scholar] [CrossRef]
- Diermayr, S.; Himmelreich, H.; Durovic, B.; Mathys-Schneeberger, A.; Siegler, U.; Langenkamp, U.; Hofsteenge, J.; Gratwohl, A.; Tichelli, A.; Paluszewska, M.; et al. NKG2D ligand expression in AML increases in response to HDAC inhibitor valproic acid and contributes to allorecognition by NK-cell lines with single KIR-HLA class I specificities. Blood 2008, 111, 1428–1436. [Google Scholar] [CrossRef] [PubMed]
- Kato, N.; Tanaka, J.; Sugita, J.; Toubai, T.; Miura, Y.; Ibata, M.; Syono, Y.; Ota, S.; Kondo, T.; Asaka, M.; et al. Regulation of the expression of MHC class I-related chain A, B (MICA, MICB) via chromatin remodeling and its impact on the susceptibility of leukemic cells to the cytotoxicity of NKG2D-expressing cells. Leukemia 2007, 21, 2103–2108. [Google Scholar] [CrossRef]
- Fiegler, N.; Textor, S.; Arnold, A.; Rölle, A.; Oehme, I.; Breuhahn, K.; Moldenhauer, G.; Witzens-Harig, M.; Cerwenka, A. Downregulation of the activating NKp30 ligand B7-H6 by HDAC inhibitors impairs tumor cell recognition by NK cells. Blood 2013, 122, 684–693. [Google Scholar] [CrossRef]
- Nakata, S.; Yoshida, T.; Horinaka, M.; Shiraishi, T.; Wakada, M.; Sakai, T. Histone deacetylase inhibitors upregulate death receptor 5/TRAIL-R2 and sensitize apoptosis induced by TRAIL/APO2-L in human malignant tumor cells. Oncogene 2004, 23, 6261–6271. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.-H. Sodium butyrate sensitizes TRAIL-mediated apoptosis by induction of transcription from the DR5 gene promoter through Sp1 sites in colon cancer cells. Carcinogenesis 2004, 25, 1813–1820. [Google Scholar] [CrossRef] [PubMed]
- Insinga, A.; Monestiroli, S.; Ronzoni, S.; Gelmetti, V.; Marchesi, F.; Viale, A.; Altucci, L.; Nervi, C.; Minucci, S.; Pelicci, P.G. Inhibitors of histone deacetylases induce tumor-selective apoptosis through activation of the death receptor pathway. Nat. Med. 2005, 11, 71–76. [Google Scholar] [CrossRef] [PubMed]
- Manasanch, E.E.; Orlowski, R.Z. Proteasome Inhibitors in Cancer Therapy HHS Public Access. Nat. Rev. Clin. Oncol. 2017, 14, 417–433. [Google Scholar] [CrossRef]
- Armeanu, S.; Krusch, M.; Baltz, K.M.; Weiss, T.S.; Smirnow, I.; Steinle, A.; Lauer, U.M.; Bitzer, M.; Salih, H.R. Direct and natural killer cell-mediated antitumor effects of low-dose bortezomib in hepatocellular carcinoma. Clin. Cancer Res. 2008, 14, 3520–3528. [Google Scholar] [CrossRef]
- Niu, C.; Jin, H.; Li, M.; Zhu, S.; Zhou, L.; Jin, F.; Zhou, Y.; Xu, D.; Xu, J.; Zhao, L.; et al. Low-dose bortezomib increases the expression of NKG2D and DNAM-1 ligands and enhances induced NK and γδ T cellmediated lysis in multiple myeloma. Oncotarget 2017, 8, 5954–5964. [Google Scholar] [CrossRef]
- Shi, J.; Tricot, G.J.; Garg, T.K.; Malaviarachchi, P.A.; Szmania, S.M.; Kellum, R.E.; Storrie, B.; Mulder, A.; Shaughnessy, J.D.; Barlogie, B.; et al. Bortezomib down-regulates the cell-surface expression of HLA class I and enhances natural killer cell-mediated lysis of myeloma. Blood 2008, 111, 1309–1317. [Google Scholar] [CrossRef]
- Lundqvist, A.; Abrams, S.I.; Schrump, D.S.; Alvarez, G.; Suffredini, D.; Berg, M.; Childs, R. Bortezomib and depsipeptide sensitize tumors to tumor necrosis factor-related apoptosis-inducing ligand: A novel method to potentiate natural killer cell tumor cytotoxicity. Cancer Res. 2006, 66, 7317–7325. [Google Scholar] [CrossRef]
- Kabore, A.F.; Sun, J.; Hu, X.; McCrea, K.; Johnston, J.B.; Gibson, S.B. The TRAIL apoptotic pathway mediates proteasome inhibitor induced apoptosis in primary chronic lymphocytic leukemia cells. Apoptosis 2006, 11, 1175–1193. [Google Scholar] [CrossRef]
- Liu, X.; Yue, P.; Chen, S.; Hu, L.; Lonial, S.; Khuri, F.R.; Sun, S.Y. The proteasome inhibitor PS-341 (bortezomib) up-regulates DR5 expression leading to induction of apoptosis and enhancement of TRAIL-induced apoptosis despite up-regulation of c-FLIP and survivin expression in human NSCLC cells. Cancer Res. 2007, 67, 4981–4988. [Google Scholar] [CrossRef] [PubMed]
- Massa, C.; Karn, T.; Denkert, C.; Schneeweiss, A.; Hanusch, C.; Blohmer, J.U.; Zahm, D.M.; Jackisch, C.; van Mackelenbergh, M.; Thomalla, J.; et al. Differential effect on different immune subsets of neoadjuvant chemotherapy in patients with TNBC. J. Immunother. Cancer 2020, 8. [Google Scholar] [CrossRef] [PubMed]
- Aldarouish, M.; Su, X.; Qiao, J.; Gao, C.; Chen, Y.; Dai, A.; Zhang, T.; Shu, Y.; Wang, C. Immunomodulatory effects of chemotherapy on blood lymphocytes and survival of patients with advanced non-small cell lung cancer. Int. J. Immunopathol. Pharmacol. 2019, 33, 2058738419839592. [Google Scholar] [CrossRef] [PubMed]
- Shinko, D.; McGuire, H.M.; Diakos, C.I.; Pavlakis, N.; Clarke, S.J.; Byrne, S.N.; Charles, K.A. Mass Cytometry Reveals a Sustained Reduction in CD16+ Natural Killer Cells Following Chemotherapy in Colorectal Cancer Patients. Front. Immunol. 2019, 10. [Google Scholar] [CrossRef]
- Beitsch, P.; Lotzová, E.; Hortobagyi, G.; Pollock, R. Natural immunity in breast cancer patients during neoadjuvant chemotherapy and after surgery. Surg. Oncol. 1994, 3, 211–219. [Google Scholar] [CrossRef]
- Sewell, H.F.; Halbert, C.F.; Robins, R.A.; Galvin, A.; Chan, S.; Blamey, R.W. Chemotherapy-induced differential changes in lymphocyte subsets and natural-killer-cell function in patients with advanced breast cancer. Int. J. Cancer 1993, 55, 735–738. [Google Scholar] [CrossRef]
- Brenner, B.G.; Margolese, R.G. The relationship of chemotherapeutic and endocrine intervention on natural killer cell activity in human breast cancer. Cancer 1991, 68, 482–488. [Google Scholar] [CrossRef]
- Ogura, M.; Ishida, T.; Tsukasaki, K.; Takahashi, T.; Utsunomiya, A. Effects of first-line chemotherapy on natural killer cells in adult T-cell leukemia–lymphoma and peripheral T-cell lymphoma. Cancer Chemother. Pharm. 2016, 78, 199–207. [Google Scholar] [CrossRef] [PubMed]
- Wullschleger, S.; Loewith, R.; Hall, M.N. TOR Signaling in Growth and Metabolism. Cell 2006, 124, 471–484. [Google Scholar] [CrossRef] [PubMed]
- Bhullar, K.S.; Lagarón, N.O.; McGowan, E.M.; Parmar, I.; Jha, A.; Hubbard, B.P.; Rupasinghe, H.P.V. Kinase-targeted cancer therapies: Progress, challenges and future directions. Mol. Cancer 2018, 17, 48. [Google Scholar] [CrossRef]
- Adams, J.A. Kinetic and catalytic mechanisms of protein kinases. Chem. Rev. 2001, 101, 2271–2290. [Google Scholar] [CrossRef]
- Johnson, L.N.; Lewis, R.J. Structural basis for control by phosphorylation. Chem. Rev. 2001, 101, 2209–2242. [Google Scholar] [CrossRef] [PubMed]
- DiDonato, J.A.; Mercurio, F.; Karin, M. NF-κB and the link between inflammation and cancer. Immunol. Rev. 2012, 246, 379–400. [Google Scholar] [CrossRef]
- Sun, C.; Bernards, R. Feedback and redundancy in receptor tyrosine kinase signaling: Relevance to cancer therapies. Trends Biochem. Sci. 2014, 39, 465–474. [Google Scholar] [CrossRef] [PubMed]
- Huang, M.; Shen, A.; Ding, J.; Geng, M. Molecularly targeted cancer therapy: Some lessons from the past decade. Trends Pharm. Sci. 2014, 35, 41–50. [Google Scholar] [CrossRef]
- Kreutzman, A.; Porkka, K.; Mustjoki, S. Immunomodulatory effects of tyrosine kinase inhibitors. Int. Trends Immun. 2013, 1, 17–28. [Google Scholar]
- Blake, S.J.; Lyons, A.B.; Fraser, C.K.; Hayball, J.D.; Hughes, T.P. Dasatinib suppresses in vitro natural killer cell cytotoxicity. Blood 2008, 111, 4415–4416. [Google Scholar] [CrossRef]
- Mustjoki, S.; Auvinen, K.; Kreutzman, A.; Rousselot, P.; Hernesniemi, S.; Melo, T.; Lahesmaa-Korpinen, A.-M.; Hautaniemi, S.; Bouchet, S.; Molimard, M.; et al. Rapid mobilization of cytotoxic lymphocytes induced by dasatinib therapy. Leukemia 2013, 27, 914–924. [Google Scholar] [CrossRef]
- Hayashi, Y.; Nakamae, H.; Katayama, T.; Nakane, T.; Koh, H.; Nakamae, M.; Hirose, A.; Hagihara, K.; Terada, Y.; Nakao, Y.; et al. Different immunoprofiles in patients with chronic myeloid leukemia treated with imatinib, nilotinib or dasatinib. Leuk. Lymphoma 2012, 53, 1084–1089. [Google Scholar] [CrossRef]
- Kreutzman, A.; Yadav, B.; Brummendorf, T.H.; Gjertsen, B.T.; Lee, M.H.; Janssen, J.; Kasanen, T.; Koskenvesa, P.; Lotfi, K.; Markevärn, B.; et al. Immunological monitoring of newly diagnosed CML patients treated with bosutinib or imatinib first-line. Oncoimmunology 2019, 8. [Google Scholar] [CrossRef] [PubMed]
- Ilander, M.; Olsson-Strömberg, U.; Schlums, H.; Guilhot, J.; Brück, O.; Lähteenmäki, H.; Kasanen, T.; Koskenvesa, P.; Söderlund, S.; Höglund, M.; et al. Increased proportion of mature NK cells is associated with successful imatinib discontinuation in chronic myeloid leukemia. Leukemia 2017, 31, 1108–1116. [Google Scholar] [CrossRef]
- Rea, D.; Henry, G.; Khaznadar, Z.; Etienne, G.; Guilhot, F.; Nicolini, F.; Guilhot, J.; Rousselot, P.; Huguet, F.; Legros, L.; et al. Natural killer-cell counts are associated with molecular relapse-free survival after imatinib discontinuation in chronic myeloid leukemia: The IMMUNOSTIM study. Haematologica 2017, 102, 1368–1377. [Google Scholar] [CrossRef] [PubMed]
- Roberts, P.J.; Der, C.J. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26, 3291–3310. [Google Scholar] [CrossRef]
- Subbiah, V.; Baik, C.; Kirkwood, J.M. Clinical Development of BRAF plus MEK Inhibitor Combinations. Trends Cancer 2020, 6, 797–810. [Google Scholar] [CrossRef]
- Kannaiyan, R.; Mahadevan, D. A comprehensive review of protein kinase inhibitors for cancer therapy HHS Public Access. Expert Rev. Anticancer 2018, 18, 1249–1270. [Google Scholar] [CrossRef] [PubMed]
- Shirley, M. Encorafenib and Binimetinib: First Global Approvals. Drugs 2018, 78, 1277–1284. [Google Scholar] [CrossRef] [PubMed]
- De Andrade, L.F.; Ngiow, S.F.; Stannard, K.; Rusakiewicz, S.; Kalimutho, M.; Khanna, K.K.; Tey, S.K.; Takeda, K.; Zitvogel, L.; Martinet, L.; et al. Natural killer cells are essential for the ability of BRAF inhibitors to control BRAFV600E-mutant metastatic melanoma. Cancer Res. 2014, 74, 7298–7308. [Google Scholar] [CrossRef]
- Frazao, A.; Colombo, M.; Fourmentraux-Neves, E.; Messaoudene, M.; Rusakiewicz, S.; Zitvogel, L.; Vivier, E.; Vély, F.; Faure, F.; Dréno, B.; et al. Shifting the Balance of Activating and Inhibitory Natural Killer Receptor Ligands on BRAF(V600E) Melanoma Lines with Vemurafenib. Cancer Immunol. Res. 2017, 5, 582–593. [Google Scholar] [CrossRef] [PubMed]
- López-Cobo, S.; Pieper, N.; Campos-Silva, C.; García-Cuesta, E.M.; Reyburn, H.T.; Paschen, A.; Valés-Gómez, M. Impaired NK cell recognition of vemurafenib-treated melanoma cells is overcome by simultaneous application of histone deacetylase inhibitors. OncoImmunology 2018, 7. [Google Scholar] [CrossRef]
- Frazao, A.; Rethacker, L.; Jeudy, G.; Colombo, M.; Pasmant, E.; Avril, M.-F.; Toubert, A.; Moins-Teisserenc, H.; Roelens, M.; Dalac, S.; et al. BRAF inhibitor resistance of melanoma cells triggers increased susceptibility to natural killer cell-mediated lysis. J. Immunother. Cancer 2020, 8, e000275. [Google Scholar] [CrossRef]
- Sottile, R.; Pangigadde, P.N.; Tan, T.; Anichini, A.; Sabbatino, F.; Trecroci, F.; Favoino, E.; Orgiano, L.; Roberts, J.; Ferrone, S.; et al. HLA class I downregulation is associated with enhanced NK-cell killing of melanoma cells with acquired drug resistance to BRAF inhibitors. Eur. J. Immunol. 2016, 46, 409–419. [Google Scholar] [CrossRef] [PubMed]
- Augello, G.; Emma, M.R.; Cusimano, A.; Azzolina, A.; Montalto, G.; McCubrey, J.A.; Cervello, M. The Role of GSK-3 in Cancer Immunotherapy: GSK-3 Inhibitors as a New Frontier in Cancer Treatment. Cells 2020, 9, 1427. [Google Scholar] [CrossRef]
- Parameswaran, R.; Ramakrishnan, P.; Moreton, S.A.; Xia, Z.; Hou, Y.; Lee, D.A.; Gupta, K.; Delima, M.; Beck, R.C.; Wald, D.N. Repression of GSK3 restores NK cell cytotoxicity in AML patients. Nat. Commun. 2016, 7. [Google Scholar] [CrossRef] [PubMed]
- Cichocki, F.; Valamehr, B.; Bjordahl, R.; Zhang, B.; Rezner, B.; Rogers, P.; Gaidarova, S.; Moreno, S.; Tuininga, K.; Dougherty, P.; et al. GSK3 inhibition drives maturation of NK cells and enhances their antitumor activity. Cancer Res. 2017, 77, 5664–5675. [Google Scholar] [CrossRef]
- Cosman, D.; Müllberg, J.; Sutherland, C.L.; Chin, W.; Armitage, R.; Fanslow, W.; Kubin, M.; Chalupny, N.J. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 2001, 14, 123–133. [Google Scholar] [CrossRef]
- Fionda, C.; Malgarini, G.; Soriani, A.; Zingoni, A.; Cecere, F.; Iannitto, M.L.; Ricciardi, M.R.; Federico, V.; Petrucci, M.T.; Santoni, A.; et al. Inhibition of glycogen synthase kinase-3 increases NKG2D ligand MICA expression and sensitivity to NK cell-mediated cytotoxicity in multiple myeloma cells: Role of STAT3. J. Immunol. 2013, 190, 6662–6672. [Google Scholar] [CrossRef]
- Krusch, M.; Salih, J.; Schlicke, M.; Baessler, T.; Kampa, K.M.; Mayer, F.; Salih, H.R. The Kinase Inhibitors Sunitinib and Sorafenib Differentially Affect NK Cell Antitumor Reactivity In Vitro. J. Immunol. 2009, 183, 8286–8294. [Google Scholar] [CrossRef]
- Lohmeyer, J.; Nerreter, T.; Dotterweich, J.; Einsele, H.; Seggewiss-Bernhardt, R. Sorafenib paradoxically activates the RAS/RAF/ERK pathway in polyclonal human NK cells during expansion and thereby enhances effector functions in a dose- and time-dependent manner. Clin. Exp. Immunol. 2018, 193, 64–72. [Google Scholar] [CrossRef]
- Huang, Y.X.; Chen, X.T.; Guo, K.Y.; Li, Y.H.; Wu, B.Y.; Song, C.Y.; He, Y.J. Sunitinib induces NK-κB-dependent NKG2D ligand expression in nasopharyngeal carcinoma and hepatoma cells. J. Immunother. 2017, 40, 164–174. [Google Scholar] [CrossRef]
- Huang, Y.; Wang, Y.; Li, Y.; Guo, K.; He, Y. Role of sorafenib and sunitinib in the induction of expressions of NKG2D ligands in nasopharyngeal carcinoma with high expression of ABCG2. J. Cancer Res. Clin. Oncol. 2011, 137, 829–837. [Google Scholar] [CrossRef]
- Harrison, D.A. The JAK/STAT pathway. Cold Spring Harb. Perspect. Biol. 2012, 4. [Google Scholar] [CrossRef]
- Schönberg, K.; Rudolph, J.; Wolf, D. NK cell modulation by JAK inhibition. Oncoscience 2015, 2, 677. [Google Scholar] [CrossRef]
- Xu, L.J.; Chen, X.D.; Shen, M.J.; Yang, D.R.; Fang, L.; Weng, G.; Tsai, Y.; Keng, P.C.; Chen, Y.; Lee, S.O. Inhibition of IL-6-JAK/Stat3 signaling in castration-resistant prostate cancer cells enhances the NK cell-mediated cytotoxicity via alteration of PD-L1/NKG2D ligand levels. Mol. Oncol. 2018, 12, 269–286. [Google Scholar] [CrossRef] [PubMed]
- Zhu, C.; Wei, Y.; Wei, X. AXL receptor tyrosine kinase as a promising anti-cancer approach: Functions, molecular mechanisms and clinical applications. Mol. Cancer 2019, 18. [Google Scholar] [CrossRef] [PubMed]
- Lutz-Nicoladoni, C.; Wolf, D.; Sopper, S.; Sharabi, A.; Palmer, D. Modulation of immune cell functions by the E3 ligase Cbl-b. Front. Oncol. 2015, 5. [Google Scholar] [CrossRef] [PubMed]
- Paolino, M.; Choidas, A.; Wallner, S.; Pranjic, B.; Uribesalgo, I.; Loeser, S.; Jamieson, A.M.; Langdon, W.Y.; Ikeda, F.; Fededa, J.P.; et al. The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells. Nature 2014, 507, 508–512. [Google Scholar] [CrossRef]
- Kaufman, H.L.; Kohlhapp, F.J.; Zloza, A. Oncolytic viruses: A new class of immunotherapy drugs. Nat. Rev. Drug Discov. 2015, 14, 642–662. [Google Scholar] [CrossRef] [PubMed]
- Fukuhara, H.; Ino, Y.; Todo, T. Oncolytic virus therapy: A new era of cancer treatment at dawn. Cancer Sci. 2016, 107, 1373–1379. [Google Scholar] [CrossRef] [PubMed]
- Hamid, O.; Ismail, R.; Puzanov, I. Intratumoral Immunotherapy—Update 2019. Oncologist 2020, 25. [Google Scholar] [CrossRef]
- Samudio, I.; Hofs, E.; Cho, B.; Li, M.; Bolduc, K.; Bu, L.; Liu, G.; Lam, V.; Rennie, P.; Jia, W.; et al. UV Light-inactivated HSV-1 Stimulates Natural Killer Cell-induced Killing of Prostate Cancer Cells. J. Immunother. 2019, 42, 162–174. [Google Scholar] [CrossRef] [PubMed]
- Bhat, R.; Rommelaere, J. NK-cell-dependent killing of colon carcinoma cells is mediated by natural cytotoxicity receptors (NCRs) and stimulated by parvovirus infection of target cells. BMC Cancer 2013, 13. [Google Scholar] [CrossRef] [PubMed]
- Ogbomo, H.; Michaelis, M.; Geiler, J.; van Rikxoort, M.; Muster, T.; Egorov, A.; Doerr, H.W.; Cinatl, J. Tumor cells infected with oncolytic influenza a virus prime natural killer cells for lysis of resistant tumor cells. Med. Microbiol. Immunol. 2010, 199, 93–101. [Google Scholar] [CrossRef] [PubMed]
- Jarahian, M.; Watzl, C.; Fournier, P.; Arnold, A.; Djandji, D.; Zahedi, S.; Cerwenka, A.; Paschen, A.; Schirrmacher, V.; Momburg, F. Activation of Natural Killer Cells by Newcastle Disease Virus Hemagglutinin-Neuraminidase. J. Virol. 2009, 83, 8108–8121. [Google Scholar] [CrossRef] [PubMed]
- Ogbomo, H.; Zemp, F.J.; Lun, X.; Zhang, J.; Stack, D.; Rahman, M.M.; Mcfadden, G.; Mody, C.H.; Forsyth, P.A. Myxoma Virus Infection Promotes NK Lysis of Malignant Gliomas In Vitro and In Vivo. PLoS ONE 2013, 8. [Google Scholar] [CrossRef]
- Bhat, R.; Rommelaere, J. Emerging role of Natural killer cells in oncolytic virotherapy. Immuno Targets Ther. 2015, 4, 65–77. [Google Scholar] [CrossRef]
- Diaz, R.M.; Galivo, F.; Kottke, T.; Wongthida, P.; Qiao, J.; Thompson, J.; Valdes, M.; Barber, G.; Vile, R.G. Oncolytic immunovirotherapy for melanoma using vesicular stomatitis virus. Cancer Res. 2007, 67, 2840–2848. [Google Scholar] [CrossRef]
- Miller, C.G.; Fraser, N.W. Requirement of an integrated immune response for successful neuroattenuated HSV-1 therapy in an intracranial metastatic melanoma model. Mol. Ther. 2003, 7, 741–747. [Google Scholar] [CrossRef]
- Tai, L.H.; de Souza, C.T.; Bélanger, S.; Ly, L.; Alkayyal, A.A.; Zhang, J.; Rintoul, J.L.; Ananth, A.A.; Lam, T.; Breitbach, C.J.; et al. Preventing postoperative metastatic disease by inhibiting surgery-induced dysfunction in natural killer cells. Cancer Res. 2013, 73, 97–107. [Google Scholar] [CrossRef]
- Altomonte, J.; Wu, L.; Chen, L.; Meseck, M.; Ebert, O.; García-Sastre, A.; Fallon, J.; Woo, S.L. Exponential enhancement of oncolytic vesicular stomatitis virus potency by vector-mediated suppression of inflammatory responses in vivo. Mol. Ther. 2008, 16, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.; Ma, R.; Russell, L.; Yoo, J.Y.; Han, J.; Cui, H.; Yi, P.; Zhang, J.; Nakashima, H.; Dai, H.; et al. An oncolytic herpesvirus expressing E-cadherin improves survival in mouse models of glioblastoma. Nat. Biotechnol. 2019, 37, 45–54. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Breckenridge, C.A.; Yu, J.; Price, R.; Wojton, J.; Pradarelli, J.; Mao, H.; Wei, M.; Wang, Y.; He, S.; Hardcastle, J.; et al. NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat. Med. 2012, 18, 1827–1834. [Google Scholar] [CrossRef] [PubMed]
- Alvarez-Breckenridge, C.A.; Yu, J.; Price, R.; Wei, M.; Wang, Y.; Nowicki, M.O.; Ha, Y.P.; Bergin, S.; Hwang, C.; Fernandez, S.A.; et al. The Histone Deacetylase Inhibitor Valproic Acid Lessens NK Cell Action against Oncolytic Virus-Infected Glioblastoma Cells by Inhibition of STAT5/T-BET Signaling and Generation of Gamma Interferon. J. Virol. 2012, 86, 4566–4577. [Google Scholar] [CrossRef] [PubMed]
- Kim, Y.; Yoo, J.Y.; Lee, T.J.; Liu, J.; Yu, J.; Caligiuri, M.A.; Kaur, B.; Friedman, A. Complex role of NK cells in regulation of oncolytic virus–bortezomib therapy. Proc. Natl. Acad. Sci. USA 2018, 115, 4927–4932. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Toffoli, E.C.; Sheikhi, A.; Höppner, Y.D.; de Kok, P.; Yazdanpanah-Samani, M.; Spanholtz, J.; Verheul, H.M.W.; van der Vliet, H.J.; de Gruijl, T.D. Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response. Cancers 2021, 13, 711. https://doi.org/10.3390/cancers13040711
Toffoli EC, Sheikhi A, Höppner YD, de Kok P, Yazdanpanah-Samani M, Spanholtz J, Verheul HMW, van der Vliet HJ, de Gruijl TD. Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response. Cancers. 2021; 13(4):711. https://doi.org/10.3390/cancers13040711
Chicago/Turabian StyleToffoli, Elisa C., Abdolkarim Sheikhi, Yannick D. Höppner, Pita de Kok, Mahsa Yazdanpanah-Samani, Jan Spanholtz, Henk M. W. Verheul, Hans J. van der Vliet, and Tanja D. de Gruijl. 2021. "Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response" Cancers 13, no. 4: 711. https://doi.org/10.3390/cancers13040711
APA StyleToffoli, E. C., Sheikhi, A., Höppner, Y. D., de Kok, P., Yazdanpanah-Samani, M., Spanholtz, J., Verheul, H. M. W., van der Vliet, H. J., & de Gruijl, T. D. (2021). Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response. Cancers, 13(4), 711. https://doi.org/10.3390/cancers13040711