Resistance to treatment poses a major challenge for cancer therapy, and oncoviral treatment encounters the issue of viral resistance as well. In this investigation, we introduce deterministic differential equation models to explore the effect of resistance on oncolytic viral therapy. Specifically, we classify tumor cells into resistant, sensitive, or infected with respect to oncolytic viruses for our analysis. Immune cells can eliminate both tumor cells and viruses. Our research shows that the introduction of immune cells into the tumor-virus interaction prevents all tumor cells from becoming resistant in the absence of conversion from resistance to sensitivity, given that the proliferation rate of immune cells exceeds their death rate. The inclusion of immune cells leads to an additional virus-free equilibrium when the immune cell recruitment rate is sufficiently high. The total tumor burden at this virus-free equilibrium is smaller than that at the virus-free and immune-free equilibrium. Therefore, immune cells are capable of reducing the tumor load under the condition of sufficient immune strength. Numerical investigations reveal that the virus transmission rate and parameters related to the immune response significantly impact treatment outcomes. However, monotherapy alone is insufficient for eradicating tumor cells, necessitating the implementation of additional therapies. Further numerical simulation shows that combination therapy with chimeric antigen receptor (CAR T-cell) therapy can enhance the success of treatment.
Citation: Prathibha Ambegoda, Hsiu-Chuan Wei, Sophia R-J Jang. The role of immune cells in resistance to oncolytic viral therapy[J]. Mathematical Biosciences and Engineering, 2024, 21(5): 5900-5946. doi: 10.3934/mbe.2024261
Resistance to treatment poses a major challenge for cancer therapy, and oncoviral treatment encounters the issue of viral resistance as well. In this investigation, we introduce deterministic differential equation models to explore the effect of resistance on oncolytic viral therapy. Specifically, we classify tumor cells into resistant, sensitive, or infected with respect to oncolytic viruses for our analysis. Immune cells can eliminate both tumor cells and viruses. Our research shows that the introduction of immune cells into the tumor-virus interaction prevents all tumor cells from becoming resistant in the absence of conversion from resistance to sensitivity, given that the proliferation rate of immune cells exceeds their death rate. The inclusion of immune cells leads to an additional virus-free equilibrium when the immune cell recruitment rate is sufficiently high. The total tumor burden at this virus-free equilibrium is smaller than that at the virus-free and immune-free equilibrium. Therefore, immune cells are capable of reducing the tumor load under the condition of sufficient immune strength. Numerical investigations reveal that the virus transmission rate and parameters related to the immune response significantly impact treatment outcomes. However, monotherapy alone is insufficient for eradicating tumor cells, necessitating the implementation of additional therapies. Further numerical simulation shows that combination therapy with chimeric antigen receptor (CAR T-cell) therapy can enhance the success of treatment.
[1] | H. Dong, S. Markovic, The Basics of Cancer Immunotherapy, Springer, 2018. |
[2] | R. A. Weinberg, The Biology of Cancer, 2$^{nd}$ edition, Garland Science: London, UK, 2013. |
[3] | G. Marelli, A. Howells, N. R. Lemoine, Y. Wang, Oncolytic viral therapy and the immune system: A double-edged sword against cancer, Front. Immunol., 9 (2018), 1–9. https://doi.org/10.3389/fimmu.2018.00866 doi: 10.3389/fimmu.2018.00866 |
[4] | M. Noll, S. Berchtold, J. Lampe, N. P. Malek, M. Bitzer, U. M. Lauer, Primary resistance phenomena to oncolytic measles vaccine viruses, Int. J. Oncol., 43 (2013), 103–112. https://doi.org/10.3892/ijo.2013.1914 doi: 10.3892/ijo.2013.1914 |
[5] | M. Bodnar, U. Forys, Modeling of drug resistance: Comparison of two hypotheses for slowly proliferating tumors on the example of low-grade gliomas, Math. Methods Appl. Sci., 45 (2022), 4161–4184. https://doi.org/10.1002/mma.7893 doi: 10.1002/mma.7893 |
[6] | M. Becker, D. Levy, Modeling the transfer of drug resistance in solid tumors, Bull. Math. Biol., 79 (2017), 2394–2412. https://doi.org/10.1007/s11538-017-0334-x doi: 10.1007/s11538-017-0334-x |
[7] | M. Bodnar, U. Forys, Two models of drug resistance for low grade gliomas: Comparison of the models dynamics, in Proceedings of the XXII National Conference on Mathematics Applied in Biology and Medicine, (2017), 37–42. |
[8] | A. Denes, S. Marzban, G. Rost, Global analysis of a cancer model with drug resistance due to Lamarckian induction and microvesicle transfer, J. Theor. Biol., 527 (2021), 110812. https://doi.org/10.1016/j.jtbi.2021.110812 doi: 10.1016/j.jtbi.2021.110812 |
[9] | J. M. Greene, S. Sanchez-Tapia, E. D. Sontag, Mathematical details on a cancer resistance model, Front. Bioeng. Biotechnol., 8 (2020), 501. https://doi.org/10.3389/fbioe.2020.00501 doi: 10.3389/fbioe.2020.00501 |
[10] | I. Kareva, Different costs of therapeutic resistance in cancer: Short- and long-term impact of population heterogeneity, Math. Biosci., 352 (2022), 108891. https://doi.org/10.1016/j.mbs.2022.108891 doi: 10.1016/j.mbs.2022.108891 |
[11] | K. Bao, An elementary mathematical modeling of drug resistance in cancer, Math. Biosci. Eng., 18 (2021), 339–353. https://doi.org/10.3934/mbe.2021018 doi: 10.3934/mbe.2021018 |
[12] | D. K. Bhatt, T. Janzen, T. Daemen, F. J. Weissing, Modelling the spatial dynamics of oncolytic virotherapy in the presence of virus-resistant tumour cells, PLoS Comput. Biol., 18 (2022), e1010076. https://doi.org/10.1371/journal.pcbi.1010076 doi: 10.1371/journal.pcbi.1010076 |
[13] | D. K. Bhatt, R. Chammas, T. Daemen, Resistance mechanisms influencing oncolytic virotherapy, a systematic analysis, Vaccines, 9 (2021), 1166. https://doi.org/10.3390/vaccines9101166 doi: 10.3390/vaccines9101166 |
[14] | S. J. Russell, K. W. Peng, J. C. Bell, Oncolytic virotherapy, Nat. Biotechnol., 30 (2012), 658–670. https://doi.org/10.1038/nbt.2287 doi: 10.1038/nbt.2287 |
[15] | P. Ambegoda, S. R. J. Jang, Resistance in oncolytic viral therapy for solid tumors, Appl. Math. Comput., 469 (2024), 128546. https://doi.org/10.1016/j.amc.2024.128546 doi: 10.1016/j.amc.2024.128546 |
[16] | K. J. Mahasa, A. Eladdadi, L. de Pillis, R. Ouifki, Oncolytic potency and reduced virus tumor specificity in oncolytic virotherapy. A mathematical modelling approach, PLoS One, 12 (2017), e0184347. https://doi.org/10.1371/journal.pone.0184347 doi: 10.1371/journal.pone.0184347 |
[17] | R. Vithanage, H. C. Wei, S. R. J. Jang, Bistability in a model of tumor-immune system interactions with an oncolytic viral therapy, Math. Biosci. Eng., 19 (2022), 1559–1587. https://doi.org/10.3934/mbe.2022072 doi: 10.3934/mbe.2022072 |
[18] | R. Vithanage, H. C. Wei, S. R. J. Jang, The Role of tumor activation and inhibition with saturation effects in a mathematical model of tumor and immune system interactions undergoing oncolytic viral therapy, Math. Meth. Appl. Sci., 46 (2023), 10787–10813. https://doi.org/10.1002/mma.9152 doi: 10.1002/mma.9152 |
[19] | R. Eftimie, G. Eftimie, Tumour-associated macrophages and oncolytic virotherapies: amathematical investigation into a complex dynamics, Lett. Biomath., 5 (2018), S6–S35. https://doi.org/10.30707/LiB5.2Eftimiea doi: 10.30707/LiB5.2Eftimiea |
[20] | P. Cordelier, M. Costa, J. Fehrenbach, Slow-fast model and therapy optimization for oncolytic treatment of tumors, Bull. Math. Biol., 84 (2022), 64. https://doi.org/10.1007/s11538-022-01025-3 doi: 10.1007/s11538-022-01025-3 |
[21] | K. Murphy, C. Weaver, L. J. Berg, Janeway's Immunobiology, 10$^{th}$ edition, Garland Science, 2022. |
[22] | K. M. Storey, E. L. Sean, T. L. Jackson, Modeling oncolytic viral therapy, immune checkpoint inhibition, and the complex dynamics of innate and adaptive immunity in glioblastoma treatment, Front. Physiol., 11 (2020), 151. https://doi.org/10.3389/fphys.2020.00151 doi: 10.3389/fphys.2020.00151 |
[23] | S. A. Felt, G. N. Droby, V. Z. Grdzelishvili, Ruxolitinib and polycation combination treatment overcomes multiple mechanisms of resistance of pancreatic cancer cells to oncolytic vesicular stomatitis virus, J. Virol., 91 (2017), e00461–17. https://doi.org/10.1128/JVI.00461-17 doi: 10.1128/JVI.00461-17 |
[24] | L. J. S. Allen, An Introduction to Mathematical Biology, Pearson/Prentice Hall, 2007. |
[25] | J. Hale, Theory of Functional Differential Equations, Springer, 1977. |
[26] | Y. Kuang, Delay Differential Equations: With Applications in Population Dynamics, Academic Press, 2012. |
[27] | H. L. Smith, An Introduction to Delay Differential Equations with Applications to the Life Sciences, Springer, 2011. |
[28] | T. Koujima, H. Tazawa, T. Ieda, H. Araki, T. Fushimi, R. Shoji, et al., Oncolytic virus-mediated targeting of the ERK signaling pathway inhibits invasive propensity in human pancreatic cancer, Mol. Ther. Oncolytics, 17 (2020), 107–117. https://doi.org/10.1016/j.omto.2020.03.016 doi: 10.1016/j.omto.2020.03.016 |
[29] | C. E. Engeland, C. Grossardt, R. Veinalde, S. Bossow, D. Lutz, J. K. Kaufmann, et al., CTLA-4 and PD-L1 checkpoint blockade enhances oncolytic measles virus therapy, Mol. Ther., 22 (2014), 1949–1959. https://doi.org/10.1038/mt.2014.160 doi: 10.1038/mt.2014.160 |
[30] | H. R. Thieme, Convergence results and a Poincare-Bendixson trichotomy for asymptotically autonomous differential equations, J. Math. Biol., 30 (1992), 755–763. |
[31] | A. Haseley, C. Alvarez-Breckenridge, A. R. Chaudhury, B. Kaur, Advances in oncolytic virus therapy for glioma, Recent Pat. CNS. Drug Discov., 4 (2009), 1–13. https://doi.org/10.2174/157488909787002573 doi: 10.2174/157488909787002573 |
[32] | S. Meerani, Y. Yao, Oncolytic viruses in cancer therapy, Eur. J. Sci. Res., 40 (2010), 156–171. |
[33] | A. Rasa, P. Alberts, Oncolytic virus preclinical toxicology studies, J. Appl. Toxicol., 43 (2023), 620–648. https://doi.org/10.1002/jat.4408 doi: 10.1002/jat.4408 |
[34] | K. James, E. Eisenhauer, M. Christian, M. Terenziani, D. Vena, A. Muldal, et al., Measuring response in solid tumors: unidimensional versus bidimensional measurement, J. Natl. Cancer Inst., 91 (1999), 523–528. https://doi.org/10.1093/jnci/91.6.523 doi: 10.1093/jnci/91.6.523 |
[35] | V. Naumenko, J. Rajwani, M. Turk et al., Repeated dosing improves oncolytic rhabdovirus therapy in mice via interactions with intravascular monocytes, Commun. Biol., 5 (2022), 1385. https://doi.org/10.1038/s42003-022-04254-3 doi: 10.1038/s42003-022-04254-3 |
[36] | V. A. Kuznetsov, I. A. Makalkin, N. A. Taylor, A. S. Perelson, Nonlinear dynamics of immunogenic tumors: parameter estimation and global bifurcation analysis, Bull. Math. Biol, 56 (1994), 295–321. https://doi.org/10.1007/BF02460644 doi: 10.1007/BF02460644 |
[37] | L. de Pillis, A. Radunskaya, C. Wiseman, A validated mathematical model of cell-mediated immune response to tumor growth, Cancer Res., 65 (2005), 7950–7958. https://doi.org/10.1158/0008-5472.CAN-05-0564 doi: 10.1158/0008-5472.CAN-05-0564 |
[38] | R. Eftimie, J. Dushoff, B. W. Bridle, J. L. Bramson, D. J. D. Earn, Multi-stability and multi-instability phenomena in a mathematical model of tumor-immune-virus interactions, Bull. Math. Biol., 73 (2011), 2932–2961. https://doi.org/10.1007/s11538-011-9653-5 doi: 10.1007/s11538-011-9653-5 |
[39] | M. R. Duran, A. Podolski-Reni, A. lvarez-Arenas, J. Dini, J. Belmonte-Beitia, M. Pesi, et al., Transfer of drug resistance characteristics between cancer cell subpopulations: a study using simple mathematical models, Bull. Math. Biol., 78 (2016), 1218–1237. https://doi.org/10.1007/s11538-016-0182-0 doi: 10.1007/s11538-016-0182-0 |
[40] | C. Macnamara, R. Eftimie, Memory versus effector immune responses in oncolytic virotherapies, J. Theor. Biol., 377 (2015), 1–9. https://doi.org/10.1016/j.jtbi.2015.04.004 doi: 10.1016/j.jtbi.2015.04.004 |
[41] | N. Komarova, D. Wodarz, Targeted Cancer Treatment in Silico: Small Molecule Inhibitors and Oncolytic Viruses, Birkhauser, Switzerland, 2013. |
[42] | B. Pulendran, J. Z. Oh, H. I. Nakaya, R. Ravindran, D. A. Kazmin, Immunity to viruses: learning from successful human vaccines, Immunol. Rev., 255 (2013), 243–255. https://doi.org/10.1111/imr.12099 doi: 10.1111/imr.12099 |
[43] | Z. Pancer, M. D. Cooper, The evolution of adaptive immunity, Annu. Rev. Immunol., 24 (2006), 497–518. https://doi.org/10.1146/annurev.immunol.24.021605.090542 doi: 10.1146/annurev.immunol.24.021605.090542 |
[44] | S. Marino, I. B. Hogue, C. J. Ray, D. E. Kirschner, A methodology for performing global uncertainty and sensitivity analysis in systems biology, J. Theor. Biol., 254 (2008), 178–196. https://doi.org/10.1016/j.jtbi.2008.04.011 doi: 10.1016/j.jtbi.2008.04.011 |
[45] | T. C. Liu, E. Galanis, D. Kirn, Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress, Nat. Clin. Pract. Oncol., 4 (2007), 101–117. https://doi.org/10.1038/ncponc0736 doi: 10.1038/ncponc0736 |
[46] | A. De Matos, L. S. Franco, G. McFadden, Oncolytic viruses and the immune system: the dynamic duo, Mol. Ther. Methods Clin. Dev., 17 (2020), 349–358. https://doi.org/10.1016/j.omtm.2020.01.001 doi: 10.1016/j.omtm.2020.01.001 |
[47] | C. J. Breitbach, Targeted inflammation during oncolytic virus therapy severely compromises tumor blood flow, Mol. Ther., 15 (2007), 1686–1693. https://doi.org/10.1038/sj.mt.6300215 doi: 10.1038/sj.mt.6300215 |
[48] | M. C. Speranza, K. Kasai, S. E. Lawler, Preclinical mouse models for analysis of the therapeutic potential of engineered oncolytic herpes viruses, ILAR J. 1 (2016), 63–72. https://doi.org/10.1093/ilar/ilw002 doi: 10.1093/ilar/ilw002 |
[49] | M. Kozak, What is strong correlation?, Teach. Stat., 31 (2009), 85–86. https://doi.org/10.1111/j.1467-9639.2009.00387.x doi: 10.1111/j.1467-9639.2009.00387.x |
[50] | L. Sun, Y. Su, A. Jiao, X. Wang, B. Zhang, T cells in health and disease, Signal Transduct. Target. Ther., 8 (2023), 235. https://doi.org/10.1038/s41392-023-01471-y doi: 10.1038/s41392-023-01471-y |
[51] | D. F. Hale, T. J. Vreeland, G. E. Peoples, Arming the immune system through vaccination to prevent cancer recurrence, Am. Soc. Clin. Oncol. Educ. Book, 36 (2016), e159–e167. https://doi.org/10.1200/EDBK_158946 doi: 10.1200/EDBK_158946 |
[52] | H. C. Wei, Numerical revisit to a class of one-predator, two-prey models, Int. J. Bifurcation Chaos, 20 (2010), 2521–2536. https://doi.org/10.1142/S0218127410027143 doi: 10.1142/S0218127410027143 |
[53] | H. C. Wei, The dynamics of the Luo-Rudy model, Int. J. Bifurcation Chaos, 20 (2010), 4055–4066. https://doi.org/10.1142/S0218127410028185 doi: 10.1142/S0218127410028185 |
[54] | M. H. Andersen, D. Schrama, P. Straten, J. C. Becker, Cytotoxic T cells, J. Invest. Dermatol., 126 (2006), 32–41. https://doi.org/10.1038/sj.jid.5700001 doi: 10.1038/sj.jid.5700001 |
[55] | C. M. Rollings, L. V. Sinclair, H. J. M. Brady, D. A. Cantrell, S. H. Ross, Interleukin-2 shapes the cytotoxic T cell proteome and immune environment-sensing programs, Sci. Signal., 11 (2018), eaap8112. https://doi.org/10.1126/scisignal.aap8112 doi: 10.1126/scisignal.aap8112 |
[56] | S. Banerjee, S. Khajanchi, S. Chaudhuri, A mathematical model to elucidate brain tumor abrogation by immunotherapy with T11 target structure, PLoS One, 10 (2015), e0123611. https://doi.org/10.1371/journal.pone.0123611 doi: 10.1371/journal.pone.0123611 |
[57] | P. A. Abrams, Adaptive foraging by predators as a cause of predator-prey cycles, Evol. Ecol., 6 (1992), 56–72. https://doi.org/10.1007/BF02285334 doi: 10.1007/BF02285334 |
[58] | A. Y. Morozov, Incorporating complex foraging of zooplankton in models: role of micro-and mesoscale processes in macroscale patterns, in Dispersal, Individual Movement and Spatial Ecology: A Mathematical Perspective, Springer, New York, (2013), 1–10. |
[59] | H. C. Wei, A mathematical model of intraguild predation with prey switching, Math. Comput. Simul., 165 (2019), 107–118. https://doi.org/10.1016/j.matcom.2019.03.004 doi: 10.1016/j.matcom.2019.03.004 |
[60] | S. Ruan, Absolute stability, conditional stability and bifurcation in Kolmogorov-type predator-prey systems with discrete delays, Quart. Appl. Math., 59 (2001), 159–173. https://doi.org/10.1090/qam/1811101 doi: 10.1090/qam/1811101 |
[61] | J. A. Nelder, R. Mead, A simplex method for function minimization, Comput. J., 7 (1965), 308–313. https://doi.org/10.1093/comjnl/7.4.308 doi: 10.1093/comjnl/7.4.308 |
[62] | X. Fu, L. Tao, X. Zhang, Genetically coating oncolytic herpes simplex virus with CD47 allows efficient systemic delivery and prolongs virus persistence at tumor site, Oncotarget, 9 (2018), 34543–34553. https://doi.org/10.18632/oncotarget.26167 doi: 10.18632/oncotarget.26167 |
[63] | I. Kareva, K. A. Luddy, C. O'Farrelly, R. A. Gatenby, J. S. Brown, Predator-prey in tumor-immune interactions: A wrong model or just an incomplete one?, Front. Immunol., 12 (2021), 668221. https://doi.org/10.3389/fimmu.2021.668221 doi: 10.3389/fimmu.2021.668221 |
[64] | H. Fukuhara, Y. Ino, T. Todo, Oncolytic virus therapy: a new era of cancer treatment at dawn, Cancer Sci., 107 (2016), 1373–1379. https://doi.org/10.1111/cas.13027 doi: 10.1111/cas.13027 |
[65] | Z. S. Guo, Z. Liu, S. Kowalsky, M. Feist, P. Kalinski, B. Lu, et al., Oncolytic immunotherapy: conceptual evolution, current strategies, and future perspectives, Front. Immunol., 8 (2017), 1–15. https://doi.org/10.3389/fimmu.2017.00555 doi: 10.3389/fimmu.2017.00555 |
[66] | L. Aurelian, Oncolytic viruses as immunotherapy: progress and remaining challenges, OncoTargets Ther., 9 (2016), 2627–2637. https://doi.org/10.2147/OTT.S63049 doi: 10.2147/OTT.S63049 |
[67] | S. Guedan, R. Alemany, CAR-T cells and oncolytic viruses: joining forces to overcome the solid tumor challenge, Front. Immunol., 89 (2018), 1–10. https://doi.org/10.3389/fimmu.2018.02460 doi: 10.3389/fimmu.2018.02460 |
[68] | R. Mohanty, C. R. Chowdhury, S. Arega, P. Sen, P. Ganguly, N. Ganguly, CAR T cell therapy: A new era for cancer treatment, Oncol. Rep., 42 (2019), 2183–2195. https://doi.org/10.3892/or.2019.7335 doi: 10.3892/or.2019.7335 |
[69] | S. Feins, W. Kong, E. F. Williams, M. C. Milone, J. A. Fraietta, An introduction to chimeric antigen receptor (CAR) T-cell immunotherapy for human cancer, Am. J. Hematol., 94 (2019), S3–S9. https://doi.org/10.1002/ajh.25418 doi: 10.1002/ajh.25418 |
[70] | A. Turdo, C. M. Cristiani, N. Schaft, CAR T-cells: novel therapeutic approaches in the new era of cancer immunotherapy, Front. Mol. Med., 3 (2023), 1239013. https://doi.org/10.3389/fmmed.2023.1239013 doi: 10.3389/fmmed.2023.1239013 |
[71] | M. Al-Haideri, S. B. Tondok, S. H. Safa, A. H. maleki, S. Rostami, A. T. Jalil, et al., CAR-T cell combination therapy: the next revolution in cancer treatment, Cancer Cell Int., 22 (2022). https://doi.org/10.1186/s12935-022-02778-6 doi: 10.1186/s12935-022-02778-6 |
[72] | A. M. Malfitano, S. D. Somma, C. A. Iannuzzi, F. Pentimalli, G. Portella, Virotherapy: From single agents to combinatorial treatments, Biochem. Pharmacol., 177 (2020), 113986. https://doi.org/10.1016/j.bcp.2020.113986 doi: 10.1016/j.bcp.2020.113986 |
[73] | I. Gruber, N. Landenberger, A. Staebler, M. Hahn, D. Wallwiener, T. Fehm, Relationship between circulating tumor cells and peripheral T-cells in patients with primary breast cancer, Anticancer Res., 33 (2013), 2233–2238. |
[74] | A. Rotte, M. J. Frigault, A. Ansari, B. Gliner, Dose-response correlation for CAR-T cells: a systematic review of clinical studies, J. Immunother. Cancer, 10 (2022). https://doi.org/10.1136/jitc-2022-005678 doi: 10.1136/jitc-2022-005678 |
[75] | M. Frigault, A. Rotte, A. Ansari, B. Gliner, C. Heery, Dose fractionation of CAR-T cells. A systematic review of clinical outcomes, J. Exp. Clin. Cancer Res., 42 (2023). https://doi.org/10.1186/s13046-022-02540-w doi: 10.1186/s13046-022-02540-w |
[76] | M. G. McCartney, Total blood and corpuscular volume in turkey hens, Poult. Sci., 31 (1952), 184–185. https://doi.org/10.3382/ps.0310184 doi: 10.3382/ps.0310184 |
[77] | Z. Z. Zhang, T. Wang, X. F. Wang, Y. Q. Zhang, Improving the ability of CAR-T cells to hit solid tumors: Challenges and strategies, Pharmacol. Res., 175 (2022). https://doi.org/10.1016/j.phrs.2021.106036 doi: 10.1016/j.phrs.2021.106036 |
[78] | R. Bhat, J. Rommelaere, Emerging role of Natural killer cells in oncolytic virotherapy, ImmunoTargets Ther., 4 (2015), 65–77. https://doi.org/10.2147/ITT.S55549 doi: 10.2147/ITT.S55549 |
[79] | H. Wu, Y. Y. Deng, L. Liu, Q. H. Tan, C. H. Wang, M. M. Guo, et al., Intestinal ischemia-reperfusion of macaques triggers a strong innate immune response, World J Gastroenterol., 20 (2014), 15327. https://doi.org/10.3748/wjg.v20.i41.15327 doi: 10.3748/wjg.v20.i41.15327 |
[80] | J. B. Swann, M. J. Smyth, Immune surveillance of tumors, J. Clin. Invest., 117 (2007), 1137–1146. https://doi.org/10.1172/JCI31405 doi: 10.1172/JCI31405 |
[81] | A. Eldar-Boock, D. Polyak, A. Scomparin, R. Satchi-Fainaro, Nano-sized polymers and liposomes designed to deliver combination therapy for cancer, Curr. Opin. Biotechnol., 24 (2013), 682–689. https://doi.org/10.1016/j.copbio.2013.04.014 doi: 10.1016/j.copbio.2013.04.014 |
[82] | W. Ratajczak, P. Niedźwiedzka-Rystwej, B. Tokarz-Deptula, W.Deptula, Immunological memory cells, Cent. Eur. J. Immunol., 43 (2018), 194–203. https://doi.org/10.5114/ceji.2018.77390 doi: 10.5114/ceji.2018.77390 |
[83] | D. H. Raulet, Interplay of natural killer cells and their receptors with the adaptive immune response, Nat. Immunol., 5 (2004), 996–1002. https://doi.org/10.1038/ni1114 doi: 10.1038/ni1114 |
[84] | M. J. D. Esmatabadi, B. Bakhshinejad, F. M. Motlagh, S. Babashah, M. Sadeghizadeh, Therapeutic resistance and cancer recurrence mechanisms: Unfolding the story of tumor coming back, J. Biosci., 41 (2016), 497–506. https://doi.org/10.1007/s12038-016-9624-y doi: 10.1007/s12038-016-9624-y |
[85] | E. Binz, U. M. Lauer, Chemovirotherapy: Combining chemotherapeutic treatment with oncolytic virotherapy, Oncolytic Virother., 4 (2015), 39–48. https://doi.org/10.2147/OV.S54780 doi: 10.2147/OV.S54780 |
[86] | H. M. Nguyen, P. K. Bommareddy, A. W. Silk, D. Daha, Optimal timing of PD-1 blockade in combination with oncolytic virus therapy, Semin. Cancer Biol., 86 (2022), 971–980. https://doi.org/10.1016/j.semcancer.2021.05.019 doi: 10.1016/j.semcancer.2021.05.019 |
[87] | L. Aurelian, Oncolytic virotherapy: The questions and the promise, Oncolytic Virother. 2, (2013), 19–29. https://doi.org/10.2147/OV.S39609 doi: 10.2147/OV.S39609 |
[88] | M. P. F. Damen, J.van Rheenen, C. L. G. J. Scheele, Targeting dormant tumor cells to prevent cancer recurrence, FEBS J., 288 (2021), 6286–6330. https://doi.org/10.1111/febs.15626 doi: 10.1111/febs.15626 |