Cytotoxic T lymphocyte-associated protein 4 antibody aggrandizes antitumor immune response of oncolytic virus M1 via targeting regulatory T cells.
Administration, Intravenous
Animals
CD8-Positive T-Lymphocytes
/ metabolism
CTLA-4 Antigen
/ antagonists & inhibitors
Cell Line, Tumor
Combined Modality Therapy
Cytokines
/ metabolism
Female
Humans
Immune Checkpoint Inhibitors
/ administration & dosage
Male
Melanoma, Experimental
/ immunology
Mice
Oncolytic Virotherapy
Oncolytic Viruses
/ physiology
Prostatic Diseases
/ immunology
T-Lymphocytes, Regulatory
/ metabolism
Tumor Microenvironment
Xenograft Model Antitumor Assays
CTLA-4 Ab
cancer immunotherapy
oncolytic virus M1
regulatory T cells
Journal
International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124
Informations de publication
Date de publication:
15 09 2021
15 09 2021
Historique:
revised:
21
05
2021
received:
01
12
2020
accepted:
27
05
2021
pubmed:
5
6
2021
medline:
14
9
2021
entrez:
4
6
2021
Statut:
ppublish
Résumé
Oncolytic virotherapies are perceived as remarkable immunotherapies coming into view and represent highly promising cancer treatments, yet to figure out its specific immune responses and underlying barriers remains critical. Albeit recent studies have demonstrated that oncolytic viruses (OVs) could fine tune tumor microenvironment (TME) to elicit tumor suppression mainly due to effective T-cell responses, the interaction between suppressive T cells and OVs is barely undetermined. Herein, we found that regulatory T cells (Treg cells) were increased in the TME following systemic administration of oncolytic virus M1 along with the higher expression of relative cytokines and chemokines in both mouse RM-1 prostatic carcinoma model and mouse B16F10 melanoma model. Besides, Treg cells expressed high levels of CD25 post-M1 treatment, and its suppressive effect on CD8
Substances chimiques
CTLA-4 Antigen
0
CTLA4 protein, human
0
Cytokines
0
Immune Checkpoint Inhibitors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1369-1384Informations de copyright
© 2021 UICC.
Références
Kaufman HL, Kohlhapp FJ, Zloza A. Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov. 2015;14(9):642-662.
Macedo N, Miller DM, Haq R, Kaufman HL. Clinical landscape of oncolytic virus research in 2020. J Immunother Cancer. 2020;8(2):e001486.
Wen JS, Zhao WZ, Liu JW, et al. Genomic analysis of a Chinese isolate of Getah-like virus and its phylogenetic relationship with other Alphaviruses. Virus Genes. 2007;35(3):597-603.
Hu J, Cai XF, Yan G. Alphavirus M1 induces apoptosis of malignant glioma cells via downregulation and nucleolar translocation of p21WAF1/CIP1 protein. Cell Cycle. 2009;8(20):3328-3339.
Lin Y, Zhang H, Liang J, et al. Identification and characterization of alphavirus M1 as a selective oncolytic virus targeting ZAP-defective human cancers. Proc Natl Acad Sci U S A. 2014;111(42):E4504-E4512.
Xiao X, Liang J, Huang C, et al. DNA-PK inhibition synergizes with oncolytic virus M1 by inhibiting antiviral response and potentiating DNA damage. Nat Commun. 2018;9(1):4342.
Liang J, Guo L, Li K, et al. Inhibition of the mevalonate pathway enhances cancer cell oncolysis mediated by M1 virus. Nat Commun. 2018;9(1):1524.
Cai J, Lin Y, Zhang H, et al. Selective replication of oncolytic virus M1 results in a bystander killing effect that is potentiated by Smac mimetics. Proc Natl Acad Sci U S A. 2017;114(26):6812-6817.
Zhang H, Li K, Lin Y, et al. Targeting VCP enhances anticancer activity of oncolytic virus M1 in hepatocellular carcinoma. Sci Transl Med. 2017;9(404):eaam7996.
Puzanov I, Milhem MM, Minor D, et al. Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma. J Clin Oncol. 2016;34(22):2619-2626.
Ribas A, Dummer R, Puzanov I, et al. Oncolytic virotherapy promotes intratumoral T cell infiltration and improves anti-PD-1 immunotherapy. Cell. 2018;174(4):1031-1032.
Schechter B, Feldman M. Suppressor cells prevent host resistance to tumor growth. Naturwissenschaften. 1979;66(3):140-146.
Berendt MJ, North RJ. T-cell-mediated suppression of anti-tumor immunity. An explanation for progressive growth of an immunogenic tumor. J Exp Med. 1980;151(1):69-80.
Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299(5609):1057-1061.
Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol. 2003;4(4):330-336.
Rech AJ, Mick R, Martin S, et al. CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients. Sci Transl Med. 2012;4(134):134ra162.
Sutmuller RP, van Duivenvoorde LM, van Elsas A, et al. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med. 2001;194(6):823-832.
Belkaid Y, Blank RB, Suffia I. Natural regulatory T cells and parasites: a common quest for host homeostasis. Immunol Rev. 2006;212:287-300.
Wing K, Onishi Y, Prieto-Martin P, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008;322(5899):271-275.
Phan GQ, Yang JC, Sherry RM, et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci U S A. 2003;100(14):8372-8377.
Weber J, Mandala M, Del Vecchio M, et al. Adjuvant nivolumab versus ipilimumab in resected stage III or IV melanoma. N Engl J Med. 2017;377(19):1824-1835.
Larkin J, Chiarion-Sileni V, Gonzalez R, et al. Five-year survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 2019;381(16):1535-1546.
Sakaguchi S, Powrie F. Emerging challenges in regulatory T cell function and biology. Science. 2007;317(5838):627-629.
Wang H, Franco F, Tsui YC, et al. CD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors. Nat Immunol. 2020;21(3):298-308.
Hatzioannou A, Banos A, Sakelaropoulos T, et al. An intrinsic role of IL-33 in Treg cell-mediated tumor immunoevasion. Nat Immunol. 2020;21(1):75-85.
Salomon B, Lenschow DJ, Rhee L, et al. B7/CD28 costimulation is essential for the homeostasis of the CD4(+)CD25(+) immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000;12(4):431-440.
Chen C, Rowell EA, Thomas RM, Hancock WW, Wells AD. Transcriptional regulation by Foxp3 is associated with direct promoter occupancy and modulation of histone acetylation. J Biol Chem. 2006;281(48):36828-36834.
Korman AJ, Peggs KS, Allison JP. Checkpoint blockade in cancer immunotherapy. Adv Immunol. 2006;90:297-339.
Wei SC, Duffy CR, Allison JP. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 2018;8(9):1069-1086.
Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271(5256):1734-1736.
Sanmamed MF, Chen L. A paradigm shift in cancer immunotherapy: from enhancement to normalization. Cell. 2018;175(2):313-326.
Liu Y, Zheng P. Preserving the CTLA-4 checkpoint for safer and more effective cancer immunotherapy. Trends Pharmacol Sci. 2020;41(1):4-12.
Zhang Y, Du X, Liu M, et al. Hijacking antibody-induced CTLA-4 lysosomal degradation for safer and more effective cancer immunotherapy. Cell Res. 2019;29(8):609-627.
Du X, Liu M, Su J, et al. Uncoupling therapeutic from immunotherapy-related adverse effects for safer and effective anti-CTLA-4 antibodies in CTLA4 humanized mice. Cell Res. 2018;28(4):433-447.
Mosely SI, Prime JE, Sainson RC, et al. Rational selection of syngeneic preclinical tumor models for immunotherapeutic drug discovery. Cancer Immunol Res. 2017;5(1):29-41.
Wang H, Franco F, Ho PC. Metabolic regulation of Tregs in cancer: opportunities for immunotherapy. Trends Cancer. 2017;3(8):583-592.
Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006;6(4):295-307.
Boyman O, Sprent J. The role of interleukin-2 during homeostasis and activation of the immune system. Nat Rev Immunol. 2012;12(3):180-190.
Gao DN, Yang ZX, Qi QH. Roles of PD-1, Tim-3 and CTLA-4 in immunoregulation in regulatory T cells among patients with sepsis. Int J Clin Exp Med. 2015;8(10):18998-19005.
Liu Y, Cai J, Liu W, et al. Intravenous injection of the oncolytic virus M1 awakens antitumor T cells and overcomes resistance to checkpoint blockade. Cell Death Dis. 2020;11(12):1062.
Calabrese LH, Calabrese C, Cappelli LC. Rheumatic immune-related adverse events from cancer immunotherapy. Nat Rev Rheumatol. 2018;14(10):569-579.
Jiang H, Shin DH, Nguyen TT, et al. Localized treatment with oncolytic adenovirus delta-24-RGDOX induces systemic immunity against disseminated subcutaneous and intracranial melanomas. Clin Cancer Res. 2019;25(22):6801-6814.
Koske I, Rossler A, Pipperger L, et al. Oncolytic virotherapy enhances the efficacy of a cancer vaccine by modulating the tumor microenvironment. Int J Cancer. 2019;145(7):1958-1969.
Mostafa AA, Meyers DE, Thirukkumaran CM, et al. Oncolytic reovirus and immune checkpoint inhibition as a novel immunotherapeutic strategy for breast cancer. Cancers. 2018;10(6):205.
Scherwitzl I, Hurtado A, Pierce CM, Vogt S, Pampeno C, Meruelo D. Systemically administered Sindbis virus in combination with immune checkpoint blockade induces curative anti-tumor immunity. Mol Ther Oncolytics. 2018;9:51-63.
Dan J, Nie L, Jia X, et al. Visualization of the oncolytic alphavirus M1 life cycle in cancer cells. Virol Sin. 2021. https://doi.org/10.1007/s12250-020-00339-7
Russell SJ, Barber GN. Oncolytic viruses as antigen-agnostic cancer vaccines. Cancer Cell. 2018;33(4):599-605.
Hwang JK, Hong J, Yun CO. Oncolytic viruses and immune checkpoint inhibitors: preclinical developments to clinical trials. Int J Mol Sci. 2020;21(22):8627.
Zhang Y, Lazarus J, Steele NG, et al. Regulatory T-cell depletion alters the tumor microenvironment and accelerates pancreatic carcinogenesis. Cancer Discov. 2020;10(3):422-439.
Hou W, Sampath P, Rojas JJ, Thorne SH. Oncolytic virus-mediated targeting of PGE2 in the tumor alters the immune status and sensitizes established and resistant tumors to immunotherapy. Cancer Cell. 2016;30(1):108-119.