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Cancer Cell International
Published in: Cancer Cell International 1/2022

Open Access 01-12-2022 | CAR T-Cell Therapy | Review

Biological causes of immunogenic cancer cell death (ICD) and anti-tumor therapy; Combination of Oncolytic virus-based immunotherapy and CAR T-cell therapy for ICD induction

Authors: Amirhossein Mardi, Anastasia V. Shirokova, Rebar N. Mohammed, Ali Keshavarz, Angelina O. Zekiy, Lakshmi Thangavelu, Talar Ahmad Merza Mohamad, Faroogh Marofi, Navid Shomali, Amir Zamani, Morteza Akbari

Published in: Cancer Cell International | Issue 1/2022

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Abstract

Chimeric antigen receptor (CAR) T-cell therapy is a promising and rapidly expanding therapeutic option for a wide range of human malignancies. Despite the ongoing progress of CAR T-cell therapy in hematologic malignancies, the application of this therapeutic strategy in solid tumors has encountered several challenges due to antigen heterogeneity, suboptimal CAR T-cell trafficking, and the immunosuppressive features of the tumor microenvironment (TME). Oncolytic virotherapy is a novel cancer therapy that employs competent or genetically modified oncolytic viruses (OVs) to preferentially proliferate in tumor cells. OVs in combination with CAR T-cells are promising candidates for overcoming the current drawbacks of CAR T-cell application in tumors through triggering immunogenic cell death (ICD) in cancer cells. ICD is a type of cellular death in which danger-associated molecular patterns (DAMPs) and tumor-specific antigens are released, leading to the stimulation of potent anti-cancer immunity. In the present review, we discuss the biological causes of ICD, different types of ICD, and the synergistic combination of OVs and CAR T-cells to reach potent tumor-specific immunity.
Literature
1.
Bishnoi S, Tiwari R, Gupta S, Byrareddy SN, Nayak D. Oncotargeting by vesicular stomatitis virus (VSV): advances in cancer therapy. Viruses. 2018;10(2):90.PubMedCentralCrossRef
2.
Jayawardena N, Poirier JT, Burga LN, Bostina M. Virus-receptor interactions and virus neutralization: insights for oncolytic virus development. Oncolytic Virotherapy. 2020;9:1.PubMedPubMedCentralCrossRef
3.
4.
Galluzzi L, Vitale I, Warren S, Adjemian S, Agostinis P, Martinez AB, Chan TA, Coukos G, Demaria S, Deutsch E. Consensus guidelines for the definition, detection and interpretation of immunogenic cell death. J Immunother Cancer. 2020;8(1):e000337.PubMedPubMedCentralCrossRef
5.
Lin RA, Lin JK, Lin SY. Mechanisms of immunogenic cell death and immune checkpoint blockade therapy. Kaohsiung J Med Sci. 2021;37(6):448–58.PubMedCrossRef
6.
Galluzzi L, Humeau J, Buqué A, Zitvogel L, Kroemer G. Immunostimulation with chemotherapy in the era of immune checkpoint inhibitors. Nat Rev Clin Oncol. 2020;17(12):725–41.PubMedCrossRef
7.
Deutsch E, Chargari C, Galluzzi L, Kroemer G. Optimising efficacy and reducing toxicity of anticancer radioimmunotherapy. Lancet Oncol. 2019;20(8):e452–63.PubMedCrossRef
8.
Ye W, Gunti S, Allen CT, Hong Y, Clavijo PE, Van Waes C, Schmitt NC. ASTX660, an antagonist of cIAP1/2 and XIAP, increases antigen processing machinery and can enhance radiation-induced immunogenic cell death in preclinical models of head and neck cancer. Oncoimmunology. 2020;9(1):1710398.PubMedPubMedCentralCrossRef
9.
van Vloten JP, Workenhe ST, Wootton SK, Mossman KL, Bridle BW. Critical interactions between immunogenic cancer cell death, oncolytic viruses, and the immune system define the rational design of combination immunotherapies. J Immunol. 2018;200(2):450–8.PubMedCrossRef
10.
11.
Fucikova J, Moserova I, Truxova I, Hermanova I, Vancurova I, Partlova S, Fialova A, Sojka L, Cartron PF, Houska M. High hydrostatic pressure induces immunogenic cell death in human tumor cells. Int J Cancer. 2014;135(5):1165–77.PubMedCrossRef
12.
Miliotou AN, Papadopoulou LC. CAR T-cell therapy: a new era in cancer immunotherapy. Curr Pharm Biotechnol. 2018;19(1):5–18.PubMedCrossRef
13.
14.
Pikor LA, Bell JC, Diallo J-S. Oncolytic viruses: exploiting cancer’s deal with the devil. Trends in cancer. 2015;1(4):266–77.PubMedCrossRef
15.
16.
17.
Schmitt CA, Fridman JS, Yang M, Baranov E, Hoffman RM, Lowe SW. Dissecting p53 tumor suppressor functions in vivo. Cancer Cell. 2002;1(3):289–98.PubMedCrossRef
18.
Galluzzi L, Vitale I, Aaronson SA, Abrams JM, Adam D, Agostinis P, Alnemri ES, Altucci L, Amelio I, Andrews DW. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018;25(3):486–541.PubMedPubMedCentralCrossRef
19.
20.
Inoue H, Tani K. Multimodal immunogenic cancer cell death as a consequence of anticancer cytotoxic treatments. Cell Death Differ. 2014;21(1):39–49.PubMedCrossRef
21.
Burz C, Berindan-Neagoe I, Balacescu O, Irimie A. Apoptosis in cancer: key molecular signaling pathways and therapy targets. Acta Oncol. 2009;48(6):811–21.PubMedCrossRef
22.
Fearnhead HO, Rodriguez J, Govek E-E, Guo W, Kobayashi R, Hannon G, Lazebnik YA. Oncogene-dependent apoptosis is mediated by caspase-9. Proc Natl Acad Sci. 1998;95(23):13664–9.PubMedPubMedCentralCrossRef
23.
Brumatti G, Salmanidis M, Ekert PG. Crossing paths: interactions between the cell death machinery and growth factor survival signals. Cell Mol Life Sci. 2010;67(10):1619–30.PubMedCrossRef
24.
Roos WP, Thomas AD, Kaina B. DNA damage and the balance between survival and death in cancer biology. Nat Rev Cancer. 2016;16(1):20–33.PubMedCrossRef
25.
Pihán P, Carreras-Sureda A, Hetz C. BCL-2 family: integrating stress responses at the ER to control cell demise. Cell Death Differ. 2017;24(9):1478–87.PubMedPubMedCentralCrossRef
26.
Suliman A, Lam A, Datta R, Srivastava RK. Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and-independent pathways. Oncogene. 2001;20(17):2122–33.PubMedCrossRef
27.
Montico B, Nigro A, Casolaro V, Dal Col J. Immunogenic apoptosis as a novel tool for anticancer vaccine development. Int J Mol Sci. 2018;19(2):594.PubMedCentralCrossRef
28.
Wang M, Jiang S, Zhang Y, Li P, Wang K. The multifaceted roles of pyroptotic cell death pathways in cancer. Cancers. 2019;11(9):1313.PubMedCentralCrossRef
29.
Nagarajan K, Soundarapandian K, Thorne RF, Li D, Li D. Activation of pyroptotic cell death pathways in cancer: an alternative therapeutic approach. Transl Oncol. 2019;12(7):925–31.PubMedPubMedCentralCrossRef
30.
Stowe I, Lee B, Kayagaki N. Caspase-11: arming the guards against bacterial infection. Immunol Rev. 2015;265(1):75–84.PubMedCrossRef
31.
Kayagaki N, Warming S, Lamkanfi M, Walle LV, Louie S, Dong J, Newton K, Qu Y, Liu J, Heldens S. Non-canonical inflammasome activation targets caspase-11. Nature. 2011;479(7371):117–21.PubMedCrossRef
32.
Shomali N, Suliman Maashi M, Baradaran B, Daei Sorkhabi A, Sarkesh A, Mohammadi H, Hemmatzadeh M, Marofi F, Sandoghchian Shotorbani S, Jarahian M. Dysregulation of survivin-targeting microRNAs in autoimmune diseases: new perspectives for novel therapies. Front Immunol. 2022;13:848.CrossRef
33.
Choi ME, Price DR, Ryter SW, Choi AM. Necroptosis: a crucial pathogenic mediator of human disease. JCI insight. 2019;4(15):e128834.PubMedCentralCrossRef
34.
Qin X, Ma D, Tan Y-X, Wang H-Y, Cai Z. The role of necroptosis in cancer: a double-edged sword? Biochimica et Biophysica Acta (BBA) Rev Cancer. 2019;1871(2):259–66.CrossRef
35.
36.
Gong Y, Fan Z, Luo G, Yang C, Huang Q, Fan K, Cheng H, Jin K, Ni Q, Yu X. The role of necroptosis in cancer biology and therapy. Mol Cancer. 2019;18(1):100.PubMedPubMedCentralCrossRef
37.
Sprooten J, De Wijngaert P, Vanmeerbeek I, Martin S, Vangheluwe P, Schlenner S, Krysko DV, Parys JB, Bultynck G, Vandenabeele P. Necroptosis in immuno-oncology and cancer immunotherapy. Cells. 2020;9(8):1823.PubMedCentralCrossRef
38.
Wang T, Jin Y, Yang W, Zhang L, Jin X, Liu X, He Y, Li X. Necroptosis in cancer: an angel or a demon? Tumor Biol. 2017;39(6):1010428317711539.CrossRef
39.
Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–72.PubMedPubMedCentralCrossRef
40.
41.
Zhou B, Liu J, Kang R, Klionsky DJ, Kroemer G, Tang D. Ferroptosis is a type of autophagy-dependent cell death. In: Seminars in cancer biology. Elsevier; 2020. p. 89–100.
42.
Wen Q, Liu J, Kang R, Zhou B, Tang D. The release and activity of HMGB1 in ferroptosis. Biochem Biophys Res Commun. 2019;510(2):278–83.PubMedCrossRef
43.
Yamazaki T, Hannani D, Poirier-Colame V, Ladoire S, Locher C, Sistigu A, Prada N, Adjemian S, Catani JP, Freudenberg M. Defective immunogenic cell death of HMGB1-deficient tumors: compensatory therapy with TLR4 agonists. Cell Death Differ. 2014;21(1):69–78.PubMedCrossRef
44.
Liang C, Zhang X, Yang M, Dong X. Recent progress in ferroptosis inducers for cancer therapy. Adv Mater. 2019;31(51):1904197.CrossRef
45.
Angeli JPF, Krysko DV, Conrad M. Ferroptosis at the crossroads of cancer-acquired drug resistance and immune evasion. Nat Rev Cancer. 2019;19(7):405–14.CrossRef
46.
Wang W, Green M, Choi JE, Gijón M, Kennedy PD, Johnson JK, Liao P, Lang X, Kryczek I, Sell A. CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature. 2019;569(7755):270–4.PubMedPubMedCentralCrossRef
47.
Tang R, Xu J, Zhang B, Liu J, Liang C, Hua J, Meng Q, Yu X, Shi S. Ferroptosis, necroptosis, and pyroptosis in anticancer immunity. J Hematol Oncol. 2020;13(1):1–18.CrossRef
48.
Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol. 2013;31:51–72.PubMedCrossRef
49.
Galluzzi L, Buque A, Kepp O, Zitvogel L, Kroemer G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell. 2015;28(6):690–714.PubMedCrossRef
50.
Garg AD, More S, Rufo N, Mece O, Sassano ML, Agostinis P, Zitvogel L, Kroemer G, Galluzzi L. Trial watch: immunogenic cell death induction by anticancer chemotherapeutics. Oncoimmunology. 2017;6(12):e1386829.PubMedPubMedCentralCrossRef
51.
Krysko DV, Garg AD, Kaczmarek A, Krysko O, Agostinis P, Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer. 2012;12(12):860–75.PubMedCrossRef
52.
Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81(1):1–5.PubMedCrossRef
53.
Fucikova J, Kepp O, Kasikova L, Petroni G, Yamazaki T, Liu P, Zhao L, Spisek R, Kroemer G, Galluzzi L. Detection of immunogenic cell death and its relevance for cancer therapy. Cell Death Dis. 2020;11(11):1013.PubMedPubMedCentralCrossRef
54.
55.
Garg AD, Galluzzi L, Apetoh L, Baert T, Birge RB, Pedro B-S, Manuel J, Breckpot K, Brough D, Chaurio R. Molecular and translational classifications of DAMPs in immunogenic cell death. Front Immunol. 2015;6:588.PubMedPubMedCentralCrossRef
56.
Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunogenic cell death in cancer and infectious disease. Nat Rev Immunol. 2017;17(2):97–111.PubMedCrossRef
57.
Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini J-L, Castedo M, Mignot G, Panaretakis T, Casares N. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med. 2007;13(1):54–61.PubMedCrossRef
58.
Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 2002;418(6894):191–5.PubMedCrossRef
59.
Conte A, Paladino S, Bianco G, Fasano D, Gerlini R, Tornincasa M, Renna M, Fusco A, Tramontano D, Pierantoni GM. High mobility group A1 protein modulates autophagy in cancer cells. Cell Death Differ. 2017;24(11):1948–62.PubMedPubMedCentralCrossRef
60.
Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature. 2009;461(7261):282–6.PubMedPubMedCentralCrossRef
61.
Vacchelli E, Ma Y, Baracco EE, Sistigu A, Enot DP, Pietrocola F, Yang H, Adjemian S, Chaba K, Semeraro M. Chemotherapy-induced antitumor immunity requires formyl peptide receptor 1. Science. 2015;350(6263):972–8.PubMedCrossRef
62.
Chiba S, Baghdadi M, Akiba H, Yoshiyama H, Kinoshita I, Dosaka-Akita H, Fujioka Y, Ohba Y, Gorman JV, Colgan JD. Tumor-infiltrating DCs suppress nucleic acid–mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol. 2012;13(9):832–42.PubMedPubMedCentralCrossRef
63.
Gong T, Liu L, Jiang W, Zhou R. DAMP-sensing receptors in sterile inflammation and inflammatory diseases. Nat Rev Immunol. 2020;20(2):95–112.PubMedCrossRef
64.
Vanpouille-Box C, Hoffmann JA, Galluzzi L. Pharmacological modulation of nucleic acid sensors—therapeutic potential and persisting obstacles. Nat Rev Drug Discovery. 2019;18(11):845–67.PubMedCrossRef
65.
Zhou J, Wang G, Chen Y, Wang H, Hua Y, Cai Z. Immunogenic cell death in cancer therapy: present and emerging inducers. J Cell Mol Med. 2019;23(8):4854–65.PubMedPubMedCentralCrossRef
66.
Pol J, Kroemer G, Galluzzi L. First oncolytic virus approved for melanoma immunotherapy. Oncoimmunology. 2016;5(1):e1115641.PubMedCrossRef
67.
Lawler SE, Speranza M-C, Cho C-F, Chiocca EA. Oncolytic viruses in cancer treatment: a review. JAMA Oncol. 2017;3(6):841–9.PubMedCrossRef
68.
Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discovery. 2015;14(9):642–62.PubMedCrossRef
69.
Prestwich RJ, Ilett EJ, Errington F, Diaz RM, Steele LP, Kottke T, Thompson J, Galivo F, Harrington KJ, Pandha HS. Immune-mediated antitumor activity of reovirus is required for therapy and is independent of direct viral oncolysis and replication. Clin Cancer Res. 2009;15(13):4374–81.PubMedPubMedCentralCrossRef
70.
Harrington K, Freeman DJ, Kelly B, Harper J, Soria J-C. Optimizing oncolytic virotherapy in cancer treatment. Nat Rev Drug Discovery. 2019;18(9):689–706.PubMedCrossRef
71.
Jin K-T, Tao X-H, Fan Y-B, Wang S-B. Crosstalk between oncolytic viruses and autophagy in cancer therapy. Biomed Pharmacother. 2021;134:110932.PubMedCrossRef
72.
Jhawar SR, Thandoni A, Bommareddy PK, Hassan S, Kohlhapp FJ, Goyal S, Schenkel JM, Silk AW, Zloza A. Oncolytic viruses—natural and genetically engineered cancer immunotherapies. Front Oncol. 2017;7:202.PubMedPubMedCentralCrossRef
73.
Stojdl DF, Lichty B, Knowles S, Marius R, Atkins H, Sonenberg N, Bell JC. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat Med. 2000;6(7):821–5.PubMedCrossRef
74.
Marelli G, Howells A, Lemoine NR, Wang Y. Oncolytic viral therapy and the immune system: a double-edged sword against cancer. Front Immunol. 2018;9:866.PubMedPubMedCentralCrossRef
75.
Puzanov I, Milhem MM, Minor D, Hamid O, Li A, Chen L, Chastain M, Gorski KS, Anderson A, Chou J. Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma. J Clin Oncol. 2016;34(22):2619.PubMedPubMedCentralCrossRef
76.
Andtbacka RHI, Curti B, Hallmeyer S, Feng Z, Paustian C, Bifulco C, Fox B, Grose M, Davies B, Karpathy R. Phase II CALM extension study: enhanced immune-cell infiltration within the tumour micro-environment of patients with advanced melanoma following intralesional delivery of Coxsackievirus A21. Eur J Cancer. 2015;51:S677.CrossRef
77.
Andtbacka RH, Curti BD, Hallmeyer S, Feng Z, Paustian C, Bifulco C, Fox B, Grose M, Shafren D. Phase II calm extension study: Coxsackievirus A21 delivered intratumorally to patients with advanced melanoma induces immune-cell infiltration in the tumor microenvironment. J Immunother Cancer. 2015;3(2):P343.PubMedCentralCrossRef
78.
Tai C-K, Kasahara N. Replication-competent retrovirus vectors for cancer gene therapy. Front Biosci. 2008;13:3083–95.PubMedCrossRef
79.
Beljanski V, Chiang C, Hiscott J. The intersection between viral oncolysis, drug resistance, and autophagy. Biol Chem. 2015;396(12):1269–80.PubMedCrossRef
80.
Jin K-T, Lu Z-B, Lv J-Q, Zhang J-G. The role of long non-coding RNAs in mediating chemoresistance by modulating autophagy in cancer. RNA Biol. 2020;17(12):1727–40.PubMedPubMedCentralCrossRef
81.
Shahverdi M, Hajiasgharzadeh K, Sorkhabi AD, Jafarlou M, Shojaee M, Tabrizi NJ, Alizadeh N, Santarpia M, Brunetti O, Safarpour H. The regulatory role of autophagy-related miRNAs in lung cancer drug resistance. Biomed Pharmacother. 2022;148:112735.PubMedCrossRef
82.
Keshavarz M, Solaymani-Mohammadi F, Miri SM, Ghaemi A. Oncolytic paramyxoviruses-induced autophagy; a prudent weapon for cancer therapy. J Biomed Sci. 2019;26(1):1–11.
83.
Ebrahimi S, Ghorbani E, Khazaei M, Avan A, Ryzhikov M, Azadmanesh K, Hassanian SM. Interferon-mediated tumor resistance to oncolytic virotherapy. J Cell Biochem. 2017;118(8):1994–9.PubMedCrossRef
84.
Yokoyama T, Iwado E, Kondo Y, Aoki H, Hayashi Y, Georgescu M, Sawaya R, Hess K, Mills G, Kawamura H. Autophagy-inducing agents augment the antitumor effect of telerase-selve oncolytic adenovirus OBP-405 on glioblastoma cells. Gene Ther. 2008;15(17):1233–9.PubMedCrossRef
85.
86.
Liikanen I, Ahtiainen L, Hirvinen ML, Bramante S, Cerullo V, Nokisalmi P, Hemminki O, Diaconu I, Pesonen S, Koski A. Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients. Mol Ther. 2013;21(6):1212–23.PubMedPubMedCentralCrossRef
87.
Tazawa H, Yano S, Yoshida R, Yamasaki Y, Sasaki T, Hashimoto Y, Kuroda S, Ouchi M, Onishi T, Uno F. Genetically engineered oncolytic adenovirus induces autophagic cell death through an E2F1-microRNA-7-epidermal growth factor receptor axis. Int J Cancer. 2012;131(12):2939–50.PubMedCrossRef
88.
Ma J, Ramachandran M, Jin C, Quijano-Rubio C, Martikainen M, Yu D, Essand M. Characterization of virus-mediated immunogenic cancer cell death and the consequences for oncolytic virus-based immunotherapy of cancer. Cell Death Dis. 2020;11(1):48.PubMedPubMedCentralCrossRef
89.
Koks CA, Garg AD, Ehrhardt M, Riva M, Vandenberk L, Boon L, Vleeschouwer SD, Agostinis P, Graf N, Van Gool SW. Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death. Int J Cancer. 2015;136(5):E313–25.PubMedCrossRef
90.
Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity. 2013;38(2):209–23.PubMedCrossRef
91.
Chen W-Y, Chen Y-L, Lin H-W, Chang C-F, Huang B-S, Sun W-Z, Cheng W-F. Stereotactic body radiation combined with oncolytic vaccinia virus induces potent anti-tumor effect by triggering tumor cell necroptosis and DAMPs. Cancer Lett. 2021;523:149–61.PubMedCrossRef
92.
Ahn DH, Bekaii-Saab T. The continued promise and many disappointments of oncolytic Virotherapy in gastrointestinal malignancies. Biomedicines. 2017;5(1):10.PubMedCentralCrossRef
93.
94.
Washburn B, Schirrmacher V. Human tumor cell infection by Newcastle Disease Virus leads to upregulation of HLA and cell adhesion molecules and to induction of interferons, chemokines and finally apoptosis. Int J Oncol. 2002;21(1):85–93.PubMed
95.
Miyagawa Y, Araki K, Yamashita T, Tanaka S, Tanaka Y, Tomifuji M, Ueda Y, Yonemitsu Y, Shimada H, Shiotani A. Induction of cell fusion/apoptosis in anaplastic thyroid carcinoma in orthotopic mouse model by urokinase-specific oncolytic Sendai virus. Head Neck. 2019;41(9):2873–82.PubMedCrossRef
96.
Douzandegan Y, Tahamtan A, Gray Z, Nikoo HR, Tabarraei A, Moradi A. Cell death mechanisms in esophageal squamous cell carcinoma induced by vesicular stomatitis virus matrix protein. Osong Public Health Res Perspect. 2019;10(4):246.PubMedPubMedCentralCrossRef
97.
Zhang J, Lai W, Li Q, Yu Y, Jin J, Guo W, Zhou X, Liu X, Wang Y. A novel oncolytic adenovirus targeting Wnt signaling effectively inhibits cancer-stem like cell growth via metastasis, apoptosis and autophagy in HCC models. Biochem Biophys Res Commun. 2017;491(2):469–77.PubMedCrossRef
98.
Loktev V, Ivan’kina TY, Netesov S, Chumakov P. Oncolytic parvoviruses. A new approaches for cancer therapy. Ann Russ Acad Med Sci. 2012;67(2):42–7.CrossRef
99.
Holze C, Michaudel C, Mackowiak C, Haas DA, Benda C, Hubel P, Pennemann FL, Schnepf D, Wettmarshausen J, Braun M. Oxeiptosis, a ROS-induced caspase-independent apoptosis-like cell-death pathway. Nat Immunol. 2018;19(2):130–40.PubMedCrossRef
100.
Innao V, Rizzo V, Allegra AG, Musolino C, Allegra A. Oncolytic viruses and hematological malignancies: a new class of immunotherapy drugs. Curr Oncol. 2021;28(1):159–83.CrossRef
101.
Kabiljo J, Laengle J, Bergmann M. From threat to cure: understanding of virus-induced cell death leads to highly immunogenic oncolytic influenza viruses. Cell Death Discovery. 2020;6(1):48.PubMedPubMedCentralCrossRef
102.
Wang Q, Imamura R, Motani K, Kushiyama H, Nagata S, Suda T. Pyroptotic cells externalize eat-me and release find-me signals and are efficiently engulfed by macrophages. Int Immunol. 2013;25(6):363–72.PubMedCrossRef
103.
Colunga AG, Laing JM, Aurelian L. The HSV-2 mutant ΔpK induces melanoma oncolysis through nonredundant death programs and associated with autophagy and pyroptosis proteins. Gene Ther. 2010;17(3):315–27.PubMedCrossRef
104.
Wang B, Zhu J, Li D, Wang Y, Zhan Y, Tan L, Qiu X, Sun Y, Song C, Meng C. Newcastle disease virus infection induces activation of the NLRP3 inflammasome. Virology. 2016;496:90–6.PubMedCrossRef
105.
Takasu A, Masui A, Hamada M, Imai T, Iwai S, Yura Y. Immunogenic cell death by oncolytic herpes simplex virus type 1 in squamous cell carcinoma cells. Cancer Gene Ther. 2016;23(4):107–13.PubMedCrossRef
106.
107.
Marchini A, Daeffler L, Pozdeev VI, Angelova A, Rommelaere J. Immune conversion of tumor microenvironment by oncolytic viruses: the protoparvovirus H-1PV case study. Front Immunol. 1848;2019:10.
108.
Cassady KA, Haworth KB, Jackson J, Markert JM, Cripe TP. To infection and beyond: the multi-pronged anti-cancer mechanisms of oncolytic viruses. Viruses. 2016;8(2):43.PubMedCentralCrossRef
109.
Zhang B, Wang X, Cheng P. Remodeling of tumor immune microenvironment by oncolytic viruses. Front Oncol. 2021;10:3478.CrossRef
110.
Li X, Wang P, Li H, Du X, Liu M, Huang Q, Wang Y, Wang S. The efficacy of oncolytic adenovirus is mediated by T-cell responses against virus and tumor in Syrian hamster model. Clin Cancer Res. 2017;23(1):239–49.PubMedCrossRef
111.
Sostoa JD, Dutoit V, Migliorini D. Oncolytic viruses as a platform for the treatment of malignant brain tumors. Int J Mol Sci. 2020;21(20):7449.PubMedCentralCrossRef
112.
Berkey SE, Thorne SH, Bartlett DL. Oncolytic virotherapy and the tumor microenvironment. Tumor Immune Microenviron Cancer Progress Cancer Ther 2017:157–172.
113.
Tosic V, Thomas DL, Kranz DM, Liu J, McFadden G, Shisler JL, MacNeill AL, Roy EJ. Myxoma virus expressing a fusion protein of interleukin-15 (IL15) and IL15 receptor alpha has enhanced antitumor activity. PLoS ONE. 2014;9(10):e109801.PubMedPubMedCentralCrossRef
114.
Lindau D, Gielen P, Kroesen M, Wesseling P, Adema GJ. The immunosuppressive tumour network: myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology. 2013;138(2):105–15.PubMedPubMedCentralCrossRef
115.
116.
Gurusamy D, Clever D, Eil R, Restifo NP. Novel “elements” of immune suppression within the tumor microenvironment. Cancer Immunol Res. 2017;5(6):426–33.PubMedPubMedCentralCrossRef
117.
118.
Ma J, Ramachandran M, Jin C, Quijano-Rubio C, Martikainen M, Yu D, Essand M. Characterization of virus-mediated immunogenic cancer cell death and the consequences for oncolytic virus-based immunotherapy of cancer. Cell Death Dis. 2020;11(1):1–15.CrossRef
119.
Berwin B, Delneste Y, Lovingood RV, Post SR, Pizzo SV. SREC-I, a type F scavenger receptor, is an endocytic receptor for calreticulin. J Biol Chem. 2004;279(49):51250–7.PubMedCrossRef
120.
Huang F-Y, Wang J-Y, Dai S-Z, Lin Y-Y, Sun Y, Zhang L, Lu Z, Cao R, Tan G-H. A recombinant oncolytic Newcastle virus expressing MIP-3α promotes systemic antitumor immunity. J Immunother Cancer. 2020;8(2):e000330.PubMedPubMedCentralCrossRef
121.
Donnelly OG, Errington-Mais F, Steele L, Hadac E, Jennings V, Scott K, Peach H, Phillips RM, Bond J, Pandha H. Measles virus causes immunogenic cell death in human melanoma. Gene Ther. 2013;20(1):7–15.PubMedCrossRef
122.
Andtbacka R, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, Delman KA, Spitler LE, Puzanov I, Agarwala SS. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015;33(25):2780–8.PubMedCrossRef
123.
Delaunay T, Violland M, Boisgerault N, Dutoit S, Vignard V, Münz C, Gannage M, Dréno B, Vaivode K, Pjanova D. Oncolytic viruses sensitize human tumor cells for NY-ESO-1 tumor antigen recognition by CD4+ effector T cells. Oncoimmunology. 2018;7(3):e1407897.PubMedCrossRef
124.
Shao X, Wang X, Guo X, Jiang K, Ye T, Chen J, Fang J, Gu L, Wang S, Zhang G. STAT3 contributes to oncolytic newcastle disease virus-induced immunogenic cell death in melanoma cells. Front Oncol. 2019;9:436.PubMedPubMedCentralCrossRef
125.
Wang X, Shao X, Gu L, Jiang K, Wang S, Chen J, Fang J, Guo X, Yuan M, Shi J. Targeting STAT3 enhances NDV-induced immunogenic cell death in prostate cancer cells. J Cell Mol Med. 2020;24(7):4286–97.PubMedPubMedCentralCrossRef
126.
Park B-H, Hwang T, Liu T-C, Sze DY, Kim J-S, Kwon H-C, Oh SY, Han S-Y, Yoon J-H, Hong S-H. Use of a targeted oncolytic poxvirus, JX-594, in patients with refractory primary or metastatic liver cancer: a phase I trial. Lancet Oncol. 2008;9(6):533–42.PubMedCrossRef
127.
Noonan AM, Farren MR, Geyer SM, Huang Y, Tahiri S, Ahn D, Mikhail S, Ciombor KK, Pant S, Aparo S. Randomized phase 2 trial of the oncolytic virus pelareorep (Reolysin) in upfront treatment of metastatic pancreatic adenocarcinoma. Mol Ther. 2016;24(6):1150–8.PubMedPubMedCentralCrossRef
128.
Zhu M, Wang Y, Qu C, Liu R, Zhang C, Wang J, Zhou D, Gu W, Chen P, Wu B. Recombinant Chinese Hu191 measles virus exhibits a significant antitumor activity against nephroblastoma mediated by immunogenic form of apoptosis. Am J Transl Res. 2021;13(4):2077.PubMedPubMedCentral
129.
Di Somma S, Iannuzzi CA, Passaro C, Forte IM, Iannone R, Gigantino V, Indovina P, Botti G, Giordano A, Formisano P. The oncolytic virus dl922-947 triggers immunogenic cell death in mesothelioma and reduces xenograft growth. Front Oncol. 2019;9:564.PubMedPubMedCentralCrossRef
130.
De Matos AL, Franco LS, McFadden G. Oncolytic viruses and the immune system: the dynamic duo. Mol Ther Methods Clin Dev. 2020;17:349–58.CrossRef
131.
132.
133.
Benmebarek M-R, Karches CH, Cadilha BL, Lesch S, Endres S, Kobold S. Killing mechanisms of chimeric antigen receptor (CAR) T cells. Int J Mol Sci. 2019;20(6):1283.PubMedCentralCrossRef
134.
Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor–modified T cells in chronic lymphoid leukemia. N Engl J Med. 2011;365:725–33.PubMedPubMedCentralCrossRef
135.
Guedan S, Chen X, Madar A, Carpenito C, McGettigan SE, Frigault MJ, Lee J, Posey AD Jr, Scholler J, Scholler N. ICOS-based chimeric antigen receptors program bipolar TH17/TH1 cells. Blood J Am Soc Hematol. 2014;124(7):1070–80.
136.
Kerkar SP, Muranski P, Kaiser A, Boni A, Sanchez-Perez L, Yu Z, Palmer DC, Reger RN, Borman ZA, Zhang L. Tumor-specific CD8+ T cells expressing interleukin-12 eradicate established cancers in lymphodepleted hosts. Can Res. 2010;70(17):6725–34.CrossRef
137.
Chmielewski M, Hombach AA, Abken H. Of CAR s and TRUCK s: chimeric antigen receptor (CAR) T cells engineered with an inducible cytokine to modulate the tumor stroma. Immunol Rev. 2014;257(1):83–90.PubMedCrossRef
138.
Habib R, Nagrial A, Micklethwaite K, Gowrishankar K. Chimeric antigen receptors for the tumour microenvironment. Tumor Microenviron 2020:117–143.
139.
140.
Schubert M-L, Hückelhoven A, Hoffmann J-M, Schmitt A, Wuchter P, Sellner L, Hofmann S, Ho AD, Dreger P, Schmitt M. Chimeric antigen receptor T cell therapy targeting CD19-positive leukemia and lymphoma in the context of stem cell transplantation. Hum Gene Ther. 2016;27(10):758–71.PubMedCrossRef
141.
Wang X, Wu Z, Qiu W, Chen P, Xu X, Han W. Programming CAR T cells to enhance anti-tumor efficacy through remodeling of the immune system. Front Med. 2020;14:726–45.PubMedCrossRef
142.
Tahmasebi S, Elahi R, Esmaeilzadeh A. Solid tumors challenges and new insights of CAR T cell engineering. Stem Cell Rev Rep. 2019;15(5):619–36.PubMedCrossRef
143.
Wu L, Wei Q, Brzostek J, Gascoigne NR. Signaling from T cell receptors (TCRs) and chimeric antigen receptors (CARs) on T cells. Cell Mol Immunol. 2020;17(6):600–12.PubMedPubMedCentralCrossRef
144.
Rodriguez-Garcia A, Palazon A, Noguera-Ortega E, Powell DJ Jr, Guedan S. CAR-T cells hit the tumor microenvironment: strategies to overcome tumor escape. Front Immunol. 2020;11:1109.PubMedPubMedCentralCrossRef
145.
Abreu TR, Fonseca NA, Gonçalves N, Moreira JN. Current challenges and emerging opportunities of CAR-T cell therapies. J Control Release. 2020;319:246–61.PubMedCrossRef
146.
Keppler SJ, Rosenits K, Koegl T, Vucikuja S, Aichele P. Signal 3 cytokines as modulators of primary immune responses during infections: the interplay of type I IFN and IL-12 in CD8 T cell responses. PLoS ONE. 2012;7(7):e40865.PubMedPubMedCentralCrossRef
147.
148.
149.
150.
Labarta-Bajo L, Nilsen SP, Humphrey G, Schwartz T, Sanders K, Swafford A, Knight R, Turner JR, Zúñiga EI. Type I IFNs and CD8 T cells increase intestinal barrier permeability after chronic viral infection. J Exp Med. 2020;217(12):e20192276.PubMedPubMedCentralCrossRef
151.
Twumasi-Boateng K, Pettigrew JL, Kwok YE, Bell JC, Nelson BH. Oncolytic viruses as engineering platforms for combination immunotherapy. Nat Rev Cancer. 2018;18(7):419–32.PubMedCrossRef
152.
Fry TJ, Shah NN, Orentas RJ, Stetler-Stevenson M, Yuan CM, Ramakrishna S, Wolters P, Martin S, Delbrook C, Yates B. CD22-targeted CAR T cells induce remission in B-ALL that is naive or resistant to CD19-targeted CAR immunotherapy. Nat Med. 2018;24(1):20–8.PubMedCrossRef
153.
VanSeggelen H, Tantalo DG, Afsahi A, Hammill JA, Bramson JL. Chimeric antigen receptor–engineered T cells as oncolytic virus carriers. Mol Ther Oncolytics. 2015;2:15014.PubMedPubMedCentralCrossRef
154.
Cole C, Qiao J, Kottke T, Diaz RM, Ahmed A, Sanchez-Perez L, Brunn G, Thompson J, Chester J, Vile RG. Tumor-targeted, systemic delivery of therapeutic viral vectors using hitchhiking on antigen-specific T cells. Nat Med. 2005;11(10):1073–81.PubMedCrossRef
155.
Tang X-Y, Ding Y-S, Zhou T, Wang X, Yang Y. Tumor-tagging by oncolytic viruses: a novel strategy for CAR-T therapy against solid tumors. Cancer Lett. 2021;503:69–74.PubMedCrossRef
156.
Aalipour A, Le Boeuf F, Tang M, Murty S, Simonetta F, Lozano AX, Shaffer TM, Bell JC, Gambhir SS. Viral delivery of CAR targets to solid tumors enables effective cell therapy. Mol Ther Oncolytics. 2020;17:232–40.PubMedPubMedCentralCrossRef
157.
Tang X, Li Y, Ma J, Wang X, Zhao W, Hossain MA, Yang Y. Adenovirus-mediated specific tumor tagging facilitates CAR-T therapy against antigen-mismatched solid tumors. Cancer Lett. 2020;487:1–9.PubMedCrossRef
158.
Park AK, Fong Y, Kim S-I, Yang J, Murad JP, Lu J, Jeang B, Chang W-C, Chen NG, Thomas SH. Effective combination immunotherapy using oncolytic viruses to deliver CAR targets to solid tumors. Sci Transl Med. 2020;12(559):eaaz1863.PubMedCrossRef
159.
160.
Corrales L, Matson V, Flood B, Spranger S, Gajewski TF. Innate immune signaling and regulation in cancer immunotherapy. Cell Res. 2017;27(1):96–108.PubMedCrossRef
161.
McKenna MK, Englisch A, Brenner B, Smith T, Hoyos V, Suzuki M, Brenner MK. Mesenchymal stromal cell delivery of oncolytic immunotherapy improves CAR-T cell antitumor activity. Mol Ther. 2021;29(5):1808–20.PubMedCrossRef
162.
Li Y, Xiao F, Zhang A, Zhang D, Nie W, Xu T, Han B, Seth P, Wang H, Yang Y. Oncolytic adenovirus targeting TGF-β enhances anti-tumor responses of mesothelin-targeted chimeric antigen receptor T cell therapy against breast cancer. Cell Immunol. 2020;348:104041.PubMedCrossRef
163.
Springuel L, Lonez C, Alexandre B, Van Cutsem E, Machiels JPH, Van Den Eynde M, Prenen H, Hendlisz A, Shaza L, Carrasco J. Chimeric antigen receptor-T cells for targeting solid tumors: current challenges and existing strategies. BioDrugs. 2019;33(5):515–37.PubMedPubMedCentralCrossRef
164.
Watanabe K, Luo Y, Da T, Guedan S, Ruella M, Scholler J, Keith B, Young RM, Engels B, Sorsa S, et al. Pancreatic cancer therapy with combined mesothelin-redirected chimeric antigen receptor T cells and cytokine-armed oncolytic adenoviruses. JCI Insight 2018; 3(7).
165.
Liu Z, Ravindranathan R, Li J, Kalinski P, Guo ZS, Bartlett DL. CXCL11-Armed oncolytic poxvirus elicits potent antitumor immunity and shows enhanced therapeutic efficacy. Oncoimmunology. 2016;5(3):e1091554.PubMedCrossRef
166.
Moon EK, Wang L-CS, Bekdache K, Lynn RC, Lo A, Thorne SH, Albelda SM. Intra-tumoral delivery of CXCL11 via a vaccinia virus, but not by modified T cells, enhances the efficacy of adoptive T cell therapy and vaccines. Oncoimmunology. 2018;7(3):e1395997.PubMedPubMedCentralCrossRef
167.
Nishio N, Diaconu I, Liu H, Cerullo V, Caruana I, Hoyos V, Bouchier-Hayes L, Savoldo B, Dotti G. Armed oncolytic virus enhances immune functions of chimeric antigen receptor–modified T cells in solid tumors. Can Res. 2014;74(18):5195–205.CrossRef
168.
Nishio N, Dotti G. Oncolytic virus expressing RANTES and IL-15 enhances function of CAR-modified T cells in solid tumors. Oncoimmunology. 2015;4(2):e988098.PubMedPubMedCentralCrossRef
169.
Huang J, Zheng M, Zhang Z, Tang X, Chen Y, Peng A, Peng X, Tong A, Zhou L. Interleukin-7-loaded oncolytic adenovirus improves CAR-T cell therapy for glioblastoma. Cancer Immunol Immunother. 2021;70:2453–65.PubMedCrossRef
170.
Shaw AR, Porter CE, Watanabe N, Tanoue K, Sikora A, Gottschalk S, Brenner MK, Suzuki M. Adenovirotherapy delivering cytokine and checkpoint inhibitor augments CAR T cells against metastatic head and neck cancer. Mol Ther. 2017;25(11):2440–51.CrossRef
171.
Tanoue K, Shaw AR, Watanabe N, Porter C, Rana B, Gottschalk S, Brenner M, Suzuki M. Armed oncolytic adenovirus–expressing PD-L1 mini-body enhances antitumor effects of chimeric antigen receptor T cells in solid tumors. Can Res. 2017;77(8):2040–51.CrossRef
172.
Suryadevara CM, Gedeon PC, Sanchez-Perez L, Verla T, Alvarez-Breckenridge C, Choi BD, Fecci PE, Sampson JH. Are BiTEs the “missing link” in cancer therapy? Oncoimmunology. 2015;4(6):e1008339.PubMedPubMedCentralCrossRef
173.
Wang X, Gottschalk S, Song X-T. Synergistic antitumor effects of Chimeric antigen receptor-modified T cells and Oncolytic Virotherapy. Washington, DC: American Society of Hematology; 2014.CrossRef
174.
Yu F, Wang X, Guo ZS, Bartlett DL, Gottschalk SM, Song XT. T-cell engager-armed oncolytic vaccinia virus significantly enhances antitumor therapy. Mol Ther. 2014;22(1):102–11.PubMedCrossRef
175.
Yu F, Hong B, Song X-T. A T-cell engager-armed oncolytic vaccinia virus to target the tumor stroma. Cancer Transl Med. 2017;3(4):122–32.CrossRef
176.
Porter CE, Shaw AR, Jung Y, Yip T, Castro PD, Sandulache VC, Sikora A, Gottschalk S, Ittman MM, Brenner MK. Oncolytic adenovirus armed with BiTE, cytokine, and checkpoint inhibitor enables CAR T cells to control the growth of heterogeneous tumors. Mol Ther. 2020;28(5):1251–62.PubMedPubMedCentralCrossRef
177.
Shaw AR, Porter CE, Yip T, Mah W-C, McKenna MK, Dysthe M, Jung Y, Parihar R, Brenner MK, Suzuki M. Oncolytic adeno-immunotherapy modulates the immune system enabling CAR T-cells to cure pancreatic tumors. Commun Biol. 2021;4(1):368.CrossRef
178.
Wing A, Fajardo CA, Posey AD, Shaw C, Da T, Young RM, Alemany R, June CH, Guedan S. Improving CART-cell therapy of solid tumors with oncolytic virus–driven production of a bispecific T-cell engager. Cancer Immunol Res. 2018;6(5):605–16.PubMedPubMedCentralCrossRef
179.
Krabbe T, Marek J, Groll T, Steiger K, Schmid RM, Krackhardt AM, Altomonte J. Adoptive T Cell therapy is complemented by oncolytic virotherapy with fusogenic VSV-NDV in combination treatment of murine melanoma. Cancers. 2021;13(5):1044.PubMedPubMedCentralCrossRef
180.
Abdullahi S, Jäkel M, Behrend SJ, Steiger K, Topping G, Krabbe T, Colombo A, Sandig V, Schiergens TS, Thasler WE. A novel chimeric oncolytic virus vector for improved safety and efficacy as a platform for the treatment of hepatocellular carcinoma. J Virol. 2018;92(23):e01386-e11318.PubMedPubMedCentralCrossRef
181.
Wenthe J, Naseri S, Labani-Motlagh A, Enblad G, Wikström KI, Eriksson E, Loskog A, Lövgren T. Boosting CAR T-cell responses in lymphoma by simultaneous targeting of CD40/4-1BB using oncolytic viral gene therapy. Cancer Immunol Immunother. 2021;70(10):2851–65.PubMedPubMedCentralCrossRef
182.
Heinzerling L, Künzi V, Oberholzer PA, Kündig T, Naim H, Dummer R. Oncolytic measles virus in cutaneous T-cell lymphomas mounts antitumor immune responses in vivo and targets interferon-resistant tumor cells. Blood. 2005;106(7):2287–94.PubMedCrossRef
183.
Garcia-Carbonero R, Salazar R, Duran I, Osman-Garcia I, Paz-Ares L, Bozada JM, Boni V, Blanc C, Seymour L, Beadle J, et al. Phase 1 study of intravenous administration of the chimeric adenovirus enadenotucirev in patients undergoing primary tumor resection. J Immunother Cancer. 2017;5(1):71.PubMedPubMedCentralCrossRef
184.
Kochneva G, Sivolobova G, Tkacheva A, Gorchakov A, Kulemzin S. Combination of oncolytic virotherapy and car t/nk cell therapy for the treatment of cancer. Mol Biol. 2020;54(1):1–12.CrossRef
185.
Akram A, Inman RD. Immunodominance: a pivotal principle in host response to viral infections. Clin Immunol. 2012;143(2):99–115.PubMedCrossRef
186.
Galivo F, Diaz RM, Thanarajasingam U, Jevremovic D, Wongthida P, Thompson J, Kottke T, Barber GN, Melcher A, Vile RG. Interference of CD40L-mediated tumor immunotherapy by oncolytic vesicular stomatitis virus. Hum Gene Ther. 2010;21(4):439–50.PubMedPubMedCentralCrossRef
187.
Frahm N, DeCamp AC, Friedrich DP, Carter DK, Defawe OD, Kublin JG, Casimiro DR, Duerr A, Robertson MN, Buchbinder SP. Human adenovirus-specific T cells modulate HIV-specific T cell responses to an Ad5-vectored HIV-1 vaccine. J Clin Investig. 2012;122(1):359–67.PubMedCrossRef
188.
Rodríguez-García A, Svensson E, Gil-Hoyos R, Fajardo C, Rojas L, Arias-Badia M, Loskog A, Alemany R. Insertion of exogenous epitopes in the E3–19K of oncolytic adenoviruses to enhance TAP-independent presentation and immunogenicity. Gene Ther. 2015;22(7):596–601.PubMedCrossRef
189.
Evgin L, Huff AL, Wongthida P, Thompson J, Kottke T, Tonne J, Schuelke M, Ayasoufi K, Driscoll CB, Shim KG, et al. Oncolytic virus-derived type I interferon restricts CAR T cell therapy. Nat Commun. 2020;11(1):3187.PubMedPubMedCentralCrossRef
190.
Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol. 2014;15(1):49–63.PubMedCrossRef
191.
Bezu L, Gomes-da-Silva LC, Dewitte H, Breckpot K, Fucikova J, Spisek R, Galluzzi L, Kepp O, Kroemer G. Combinatorial strategies for the induction of immunogenic cell death. Front Immunol. 2015;6:187.PubMedPubMedCentral
192.
Galluzzi L, Bravo-San Pedro JM, Demaria S, Formenti SC, Kroemer G. Activating autophagy to potentiate immunogenic chemotherapy and radiation therapy. Nat Rev Clin Oncol. 2017;14(4):247–58.PubMedCrossRef
193.
Hongmei Z. Extrinsic and intrinsic apoptosis signal pathway review. InTechOpen; 2012.CrossRef
194.
Nagata S. DNA degradation in development and programmed cell death. Annu Rev Immunol. 2005;23:853–75.PubMedCrossRef
195.
Naito M, Nagashima K, Mashima T, Tsuruo T. Phosphatidylserine externalization is a downstream event of interleukin-1β–converting enzyme family protease activation during apoptosis. Blood J Am Soc Hematol. 1997;89(6):2060–6.
196.
Martin SJ, Finucane DM, Amarante-Mendes GP, O’Brien GA, Green DR. Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J Biol Chem. 1996;271(46):28753–6.PubMedCrossRef
197.
Sebbagh M, Renvoizé C, Hamelin J, Riché N, Bertoglio J, Bréard J. Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat Cell Biol. 2001;3(4):346–52.PubMedCrossRef
198.
Tang D, Chen X, Kang R, Kroemer G. Ferroptosis: molecular mechanisms and health implications. Cell Res. 2021;31(2):107–25.PubMedCrossRef
199.
Hayashi K, Nikolos F, Lee Y, Jain A, Tsouko E, Gao H, Kasabyan A, Leung H, Osipov A, Jung S. Tipping the immunostimulatory and inhibitory DAMP balance to harness immunogenic cell death. Nat Commun. 2020;11(1):6299.PubMedPubMedCentralCrossRef
200.
201.
Garg AD, Agostinis P. Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol Rev. 2017;280(1):126–48.PubMedCrossRef
202.
Hasei J, Sasaki T, Tazawa H, Osaki S, Yamakawa Y, Kunisada T, Yoshida A, Hashimoto Y, Onishi T, Uno F. Dual programmed cell death pathways induced by p53 transactivation overcome resistance to oncolytic adenovirus in human osteosarcoma cells. Mol Cancer Ther. 2013;12(3):314–25.PubMedCrossRef
203.
Endo Y, Sakai R, Ouchi M, Onimatsu H, Hioki M, Kagawa S, Uno F, Watanabe Y, Urata Y, Tanaka N. Virus-mediated oncolysis induces danger signal and stimulates cytotoxic T-lymphocyte activity via proteasome activator upregulation. Oncogene. 2008;27(17):2375–81.PubMedCrossRef
204.
Klein SR, Jiang H, Hossain MB, Fan X, Gumin J, Dong A, Alonso MM, Gomez-Manzano C, Fueyo J. Critical role of autophagy in the processing of adenovirus capsid-incorporated cancer-specific antigens. PLoS ONE. 2016;11(4):e0153814.PubMedPubMedCentralCrossRef
205.
206.
Ye T, Jiang K, Wei L, Barr MP, Xu Q, Zhang G, Ding C, Meng S, Piao H. Oncolytic Newcastle disease virus induces autophagy-dependent immunogenic cell death in lung cancer cells. Am J Cancer Res. 2018;8(8):1514–27.PubMedPubMedCentral
207.
Nejad ASM, Fotouhi F, Mehrbod P, Keshavarz M, Alikhani MY, Ghaemi A. Oncolytic effects of Hitchner B1 strain of newcastle disease virus against cervical cancer cell proliferation is mediated by the increased expression of cytochrome C, autophagy and apoptotic pathways. Microb Pathog. 2020;147:104438.CrossRef
208.
Jiang K, Li Y, Zhu Q, Xu J, Wang Y, Deng W, Liu Q, Zhang G, Meng S. Pharmacological modulation of autophagy enhances Newcastle disease virus-mediated oncolysis in drug-resistant lung cancer cells. BMC Cancer. 2014;14(1):551.PubMedPubMedCentralCrossRef
209.
Baird S, Aerts J, Eddaoudi A, Lockley M, Lemoine N, McNeish I. Oncolytic adenoviral mutants induce a novel mode of programmed cell death in ovarian cancer. Oncogene. 2008;27(22):3081–90.PubMedCrossRef
210.
Uratsuji H, Tada Y, Kawashima T, Kamata M, Hau CS, Asano Y, Sugaya M, Kadono T, Asahina A, Sato S. P2Y6 receptor signaling pathway mediates inflammatory responses induced by monosodium urate crystals. J Immunol. 2012;188(1):436–44.PubMedCrossRef
Metadata
Title
Biological causes of immunogenic cancer cell death (ICD) and anti-tumor therapy; Combination of Oncolytic virus-based immunotherapy and CAR T-cell therapy for ICD induction
Authors
Amirhossein Mardi
Anastasia V. Shirokova
Rebar N. Mohammed
Ali Keshavarz
Angelina O. Zekiy
Lakshmi Thangavelu
Talar Ahmad Merza Mohamad
Faroogh Marofi
Navid Shomali
Amir Zamani
Morteza Akbari
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2022
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-022-02585-z

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