Macrophage Polarization Contributes to Glioblastoma Eradication by Combination Immunovirotherapy and Immune Checkpoint Blockade

Dipongkor Saha ¹, Robert L Martuza ¹, Samuel D Rabkin ²

Affiliations

¹ Molecular Neurosurgery Laboratory and the Brain Tumor Research Center, Department of Neurosurgery, Massachusetts General Hospital, Boston, MA, USA; Department of Neurosurgery, Harvard Medical School, Boston, MA, USA.
² Molecular Neurosurgery Laboratory and the Brain Tumor Research Center, Department of Neurosurgery, Massachusetts General Hospital, Boston, MA, USA; Department of Neurosurgery, Harvard Medical School, Boston, MA, USA. Electronic address: rabkin@mgh.harvard.edu.

PMID: 28810147
69 References
208 citations

Abstract

Glioblastoma is an immunosuppressive, fatal brain cancer that contains glioblastoma stem-like cells (GSCs). Oncolytic herpes simplex virus (oHSV) selectively replicates in cancer cells while inducing anti-tumor immunity. oHSV G47Δ expressing murine IL-12 (G47Δ-mIL12), antibodies to immune checkpoints (CTLA-4, PD-1, PD-L1), or dual combinations modestly extended survival of a mouse glioma model. However, the triple combination of anti-CTLA-4, anti-PD-1, and G47Δ-mIL12 cured most mice in two glioma models. This treatment was associated with macrophage influx and M1-like polarization, along with increased T effector to T regulatory cell ratios. Immune cell depletion studies demonstrated that CD4+ and CD8+ T cells as well as macrophages are required for synergistic curative activity. This combination should be translatable to the clinic and other immunosuppressive cancers.

Keywords: HSV; cancer stem cells; glioma; immunotherapy; oncolytic virus.

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Oncolytic Virus Encoding a Master Pro-Inflammatory Cytokine Interleukin 12 in Cancer Immunotherapy. Hong-My Nguyen, Kirsten Guz-Montgomery, Dipongkor Saha. Cells, 2020 Feb 14; 9(2). PMID: 32050597 Free PMC article. Review.
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Valproic Acid-Like Compounds Enhance and Prolong the Radiotherapy Effect on Breast Cancer by Activating and Maintaining Anti-Tumor Immune Function. Zuchao Cai, David Lim, +9 authors, Zhihui Feng. less Front Immunol, 2021 Jun 01; 12. PMID: 34054811 Free PMC article.
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Intratumoral expression of interleukin 23 variants using oncolytic vaccinia virus elicit potent antitumor effects on multiple tumor models via tumor microenvironment modulation. Lingjuan Chen, Hongqi Chen, +10 authors, David L Bartlett. less Theranostics, 2021 Jun 08; 11(14). PMID: 34093846 Free PMC article.
Synergistic immunotherapy of glioblastoma by dual targeting of IL-6 and CD40. Fan Yang, Zhenqiang He, +15 authors, Yi Fan. less Nat Commun, 2021 Jun 10; 12(1). PMID: 34103524 Free PMC article.
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Positron emission tomography imaging with 89Zr-labeled anti-CD8 cys-diabody reveals CD8+ cell infiltration during oncolytic virus therapy in a glioma murine model. Benjamin B Kasten, Hailey A Houson, +10 authors, Anna G Sorace. less Sci Rep, 2021 Jul 30; 11(1). PMID: 34321569 Free PMC article.
The Heterogeneity of Infiltrating Macrophages in Metastatic Osteosarcoma and Its Correlation with Immunotherapy. Zhanchao Wang, Huiqiao Wu, +3 authors, Yu Chen, Huajiang Chen, Wen Yuan, Xinwei Wang. less J Oncol, 2021 Aug 03; 2021. PMID: 34335756 Free PMC article.
Tumor Associated Macrophages, as the Dominant Immune Cells, Are an Indispensable Target for Immunologically Cold Tumor-Glioma Therapy? Ni Tong, Zhenqiang He, +9 authors, Qirui Wang. less Front Cell Dev Biol, 2021 Aug 10; 9. PMID: 34368156 Free PMC article. Review.
Oncolytic Viruses for Malignant Glioma: On the Verge of Success? Yogesh R Suryawanshi, Autumn J Schulze. Viruses, 2021 Aug 11; 13(7). PMID: 34372501 Free PMC article. Review.
Interactions between cancer cells and immune cells drive transitions to mesenchymal-like states in glioblastoma. Toshiro Hara, Rony Chanoch-Myers, +18 authors, Itay Tirosh. less Cancer Cell, 2021 Jun 05; 39(6). PMID: 34087162 Free PMC article.
Crosstalk Between Tumor-Associated Microglia/Macrophages and CD8-Positive T Cells Plays a Key Role in Glioblastoma. Sheng Tu, Xu Lin, +8 authors, Anwen Shao. less Front Immunol, 2021 Aug 17; 12. PMID: 34394072 Free PMC article. Review.
PI3Kα inhibitor CYH33 triggers antitumor immunity in murine breast cancer by activating CD8+T cells and promoting fatty acid metabolism. Pu Sun, Xi Zhang, +9 authors, Ling-Hua Meng. less J Immunother Cancer, 2021 Aug 11; 9(8). PMID: 34373258 Free PMC article.
Cutting both ways: the innate immune response to oncolytic virotherapy. David Mealiea, J Andrea McCart. Cancer Gene Ther, 2021 Aug 29;. PMID: 34453122 Review.
The Multifaceted Role of Macrophages in Oncolytic Virotherapy. Laura Hofman, Sean E Lawler, Martine L M Lamfers. Viruses, 2021 Aug 29; 13(8). PMID: 34452439 Free PMC article. Review.
Mouse models of glioblastoma for the evaluation of novel therapeutic strategies. Alexander F Haddad, Jacob S Young, +4 authors, Nicholas A Butowski. less Neurooncol Adv, 2021 Sep 02; 3(1). PMID: 34466804 Free PMC article. Review.
Oncolytic herpes virus G47Δ works synergistically with CTLA-4 inhibition via dynamic intratumoral immune modulation. Kotaro Sugawara, Miwako Iwai, +3 authors, Tomoki Todo. less Mol Ther Oncolytics, 2021 Sep 14; 22. PMID: 34514094 Free PMC article.
Phenotypic plasticity of myeloid cells in glioblastoma development, progression, and therapeutics. Zengpanpan Ye, Xiaolin Ai, +3 authors, Linjie Zhao, Fan Fei, Ping Wang, Shengtao Zhou. less Oncogene, 2021 Sep 25; 40(42). PMID: 34556813 Review.
Oncolytic herpes virus G47Δ injected into tongue cancer swiftly traffics in lymphatics and suppresses metastasis. Toshihiro Uchihashi, Hirokazu Nakahara, +6 authors, Tomoki Todo. less Mol Ther Oncolytics, 2021 Sep 24; 22. PMID: 34553027 Free PMC article.
Treatment of glioblastoma with current oHSV variants reveals differences in efficacy and immune cell recruitment. Joseph W Jackson, Bonnie L Hall, +7 authors, Joseph C Glorioso. less Mol Ther Oncolytics, 2021 Sep 24; 22. PMID: 34553031 Free PMC article.
The Immune Privilege of Cancer Stem Cells: A Key to Understanding Tumor Immune Escape and Therapy Failure. Claudia Galassi, Martina Musella, +2 authors, Nicoletta Manduca, Ester Maccafeo, Antonella Sistigu. less Cells, 2021 Sep 29; 10(9). PMID: 34572009 Free PMC article. Review.
In Situ Cancer Vaccination and Immunovirotherapy Using Oncolytic HSV. Nusrat Jahan, Shanawaz M Ghouse, Robert L Martuza, Samuel D Rabkin. Viruses, 2021 Sep 29; 13(9). PMID: 34578321 Free PMC article. Review.
An oncolytic virus expressing a full-length antibody enhances antitumor innate immune response to glioblastoma. Bo Xu, Lei Tian, +10 authors, Jianhua Yu. less Nat Commun, 2021 Oct 10; 12(1). PMID: 34625564 Free PMC article.
Clinical Value of TXNDC12 Combined With IDH and 1p19q as Biomarkers for Prognosis of Glioma. Xinzhuang Wang, Quan Yang, +3 authors, Nan Liu, Qilong Bian, Ming Gao, Xu Hou. less Pathol Oncol Res, 2021 Oct 12; 27. PMID: 34629960 Free PMC article.
Immunovirotherapy for the Treatment of Glioblastoma and Other Malignant Gliomas. Dagoberto Estevez-Ordonez, Gustavo Chagoya, +8 authors, James M Markert. less Neurosurg Clin N Am, 2021 Mar 31; 32(2). PMID: 33781507 Free PMC article. Review.
Oncolytic Viro-Immunotherapy: An Emerging Option in the Treatment of Gliomas. Jiayi Zeng, Xiangxue Li, +3 authors, Yuan Lin. less Front Immunol, 2021 Oct 23; 12. PMID: 34675919 Free PMC article. Review.
Phosphor-IWS1-dependent U2AF2 splicing regulates trafficking of CAR-E-positive intronless gene mRNAs and sensitivity to viral infection. Georgios I Laliotis, Adam D Kenney, +10 authors, Philip N Tsichlis. less Commun Biol, 2021 Oct 13; 4(1). PMID: 34635782 Free PMC article.
Harnessing nanomedicine for enhanced immunotherapy for breast cancer brain metastases. Christine P Carney, Nikhil Pandey, +3 authors, Anthony J Kim. less Drug Deliv Transl Res, 2021 Oct 31; 11(6). PMID: 34716900 Free PMC article. Review.
Synergy between Toxoplasma gondii type I ΔGRA17 immunotherapy and PD-L1 checkpoint inhibition triggers the regression of targeted and distal tumors. Yu-Chao Zhu, Hany M Elsheikha, +4 authors, Jia Chen. less J Immunother Cancer, 2021 Nov 03; 9(11). PMID: 34725213 Free PMC article.
Dendritic Cell Vaccination of Glioblastoma: Road to Success or Dead End. Angeliki Datsi, Rüdiger V Sorg. Front Immunol, 2021 Nov 20; 12. PMID: 34795675 Free PMC article. Review.
Neurosurgery at the crossroads of immunology and nanotechnology. New reality in the COVID-19 pandemic. Vladimir A Ljubimov, Arshia Ramesh, +3 authors, Keith L Black. less Adv Drug Deliv Rev, 2021 Nov 23; 181. PMID: 34808227 Free PMC article. Review.
Efficacy and safety of a third-generation oncolytic herpes virus G47Δ in models of human esophageal carcinoma. Shoh Yajima, Kotaro Sugawara, +3 authors, Tomoki Todo. less Mol Ther Oncolytics, 2021 Dec 03; 23. PMID: 34853811 Free PMC article.
Oncolytic Virotherapy: From Bench to Bedside. Ludi Yang, Xiang Gu, +2 authors, Jie Yu, Shengfang Ge, Xianqun Fan. less Front Cell Dev Biol, 2021 Dec 14; 9. PMID: 34901031 Free PMC article. Review.
Oncolytic measles vaccines encoding PD-1 and PD-L1 checkpoint blocking antibodies to increase tumor-specific T cell memory. Rūta Veinalde, Gemma Pidelaserra-Martí, +6 authors, Christine E Engeland. less Mol Ther Oncolytics, 2022 Jan 04; 24. PMID: 34977341 Free PMC article.
Combination therapy with immune checkpoint inhibitors (ICIs); a new frontier. Somayeh Vafaei, Angelina O Zekiy, +4 authors, Majid Zamani. less Cancer Cell Int, 2022 Jan 05; 22(1). PMID: 34980128 Free PMC article. Review.
TMEM158 promotes the proliferation and migration of glioma cells via STAT3 signaling in glioblastomas. Jiabo Li, Xuya Wang, +20 authors, Xuejun Yang. less Cancer Gene Ther, 2022 Jan 08;. PMID: 34992215
Cancer stem cells: a major culprit of intra-tumor heterogeneity. Faiza Naz, Mengran Shi, +2 authors, Salvia Sajid, Zhao Yang, Changyuan Yu. less Am J Cancer Res, 2022 Jan 13; 11(12). PMID: 35018226 Free PMC article. Review.
Interleukin-12 as an in situ cancer vaccine component: a review. Emily M Cheng, Noah W Tsarovsky, Paul M Sondel, Alexander L Rakhmilevich. Cancer Immunol Immunother, 2022 Jan 14;. PMID: 35024897 Review.
Successful treatment of a 19-year-old patient with locally advanced clear cell adenocarcinoma of the uterine cervix using recombinant human adenovirus type 5 (Oncorine) combined with chemoradiotherapy: a case report. Jing Zhang, Zi Liu, +5 authors, Tuo-Tuo Gong. less Ann Transl Med, 2022 Jan 25; 9(23). PMID: 35071441 Free PMC article.
Immunotherapy for glioblastoma: the promise of combination strategies. Mathilde Bausart, Véronique Préat, Alessio Malfanti. J Exp Clin Cancer Res, 2022 Jan 27; 41(1). PMID: 35078492 Free PMC article. Review.
Fatty Acids, CD36, Thrombospondin-1, and CD47 in Glioblastoma: Together and/or Separately? Cristiana Tanase, Ana Maria Enciu, +7 authors, Mihail Eugen Hinescu. less Int J Mol Sci, 2022 Jan 22; 23(2). PMID: 35054787 Free PMC article. Review.
Dual role of ARPC1B in regulating the network between tumor-associated macrophages and tumor cells in glioblastoma. Tianqi Liu, Chen Zhu, +8 authors, Anhua Wu. less Oncoimmunology, 2022 Feb 04; 11(1). PMID: 35111386 Free PMC article.
ERK1/2 phosphorylation predicts survival following anti-PD-1 immunotherapy in recurrent glioblastoma. Víctor A Arrieta, Andrew X Chen, +39 authors, Adam M Sonabend. less Nat Cancer, 2022 Feb 06; 2(12). PMID: 35121903 Free PMC article.
Immune Activity and Response Differences of Oncolytic Viral Therapy in Recurrent Glioblastoma: Gene Expression Analyses of a Phase IB Study. Katherine E Miller, Kevin A Cassady, +11 authors, James M Markert. less Clin Cancer Res, 2022 Feb 03; 28(3). PMID: 35105718 Free PMC article.
Tumor-Associated Macrophages/Microglia in Glioblastoma Oncolytic Virotherapy: A Double-Edged Sword. Sarah E Blitz, Ari D Kappel, +8 authors, Joshua D Bernstock. less Int J Mol Sci, 2022 Feb 16; 23(3). PMID: 35163730 Free PMC article. Review.
Combining nanomedicine and immune checkpoint therapy for cancer immunotherapy. Christine E Boone, Lu Wang, +2 authors, Aayushma Gautam, Isabel G Newton, Nicole F Steinmetz. less Wiley Interdiscip Rev Nanomed Nanobiotechnol, 2021 Jul 24; 14(1). PMID: 34296535 Free PMC article. Review.
Tumor-Associated Macrophages in Gliomas-Basic Insights and Treatment Opportunities. Johannes K Andersen, Hrvoje Miletic, Jubayer A Hossain. Cancers (Basel), 2022 Mar 11; 14(5). PMID: 35267626 Free PMC article. Review.
Oncolytic Virotherapy in Peritoneal Metastasis Gastric Cancer: The Challenges and Achievements. Su Shao, Xue Yang, +5 authors, Pei-Yang Hu. less Front Mol Biosci, 2022 Mar 18; 9. PMID: 35295845 Free PMC article. Review.
NOTCH-Induced MDSC Recruitment after oHSV Virotherapy in CNS Cancer Models Modulates Antitumor Immunotherapy. Yoshihiro Otani, Ji Young Yoo, +19 authors, Balveen Kaur. less Clin Cancer Res, 2022 Jan 14; 28(7). PMID: 35022322 Free PMC article.
Implications of immune cells in oncolytic herpes simplex virotherapy for glioma. Yoshihiro Otani, Ji Young Yoo, +3 authors, Balveen Kaur. less Brain Tumor Pathol, 2022 Apr 07; 39(2). PMID: 35384530 Review.
Engineering strategies to enhance oncolytic viruses in cancer immunotherapy. Yaomei Tian, Daoyuan Xie, Li Yang. Signal Transduct Target Ther, 2022 Apr 08; 7(1). PMID: 35387984 Free PMC article. Review.
Tumor immunotherapies by immune checkpoint inhibitors (ICIs); the pros and cons. Adel Naimi, Rebar N Mohammed, +11 authors, Ehsan Razeghian. less Cell Commun Signal, 2022 Apr 09; 20(1). PMID: 35392976 Free PMC article. Review.
The Role of Immune Checkpoint Molecules on Macrophages in Cancer, Infection, and Autoimmune Pathologies. Victoria C Brom, Christof Burger, Dieter C Wirtz, Frank A Schildberg. Front Immunol, 2022 Apr 15; 13. PMID: 35418973 Free PMC article. Review.
Association between high immune activity and worse prognosis in uveal melanoma and low-grade glioma in TCGA transcriptomic data. Hitoshi Matsuo, Takashi Kamatani, +2 authors, Yu Hamba, Keith A Boroevich, Tatsuhiko Tsunoda. less BMC Genomics, 2022 May 08; 23(1). PMID: 35525921 Free PMC article.
Characterization of the Ferroptosis-Related Genes for Prognosis and Immune Infiltration in Low-Grade Glioma. Xiuwei Yan, Hang Ji, +11 authors, Shaoshan Hu. less Front Genet, 2022 May 14; 13. PMID: 35559020 Free PMC article.
Rat and Mouse Brain Tumor Models for Experimental Neuro-Oncology Research. Upasana Sahu, Rolf F Barth, +2 authors, Yoshihiro Otani, Ryan McCormack, Balveen Kaur. less J Neuropathol Exp Neurol, 2022 Apr 22; 81(5). PMID: 35446393 Free PMC article. Review.
Genome Instability-Associated Long Non-Coding RNAs Reveal Biomarkers for Glioma Immunotherapy and Prognosis. Xinzhuang Wang, Hong Zhang, +10 authors, Dayong Han. less Front Genet, 2022 May 17; 13. PMID: 35571034 Free PMC article.
Roles for macrophage-polarizing interleukins in cancer immunity and immunotherapy. Keywan Mortezaee, Jamal Majidpoor. Cell Oncol (Dordr), 2022 May 20; 45(3). PMID: 35587857 Review.
Oncolytic viral vectors in the era of diversified cancer therapy: from preclinical to clinical. Chao Tang, Lan Li, +8 authors, Liping Zhong. less Clin Transl Oncol, 2022 May 26;. PMID: 35612653 Review.
Translational landscape of glioblastoma immunotherapy for physicians: guiding clinical practice with basic scientific evidence. Daniel Kreatsoulas, Chelsea Bolyard, +3 authors, Bill X Wu, Hakan Cam, Pierre Giglio, Zihai Li. less J Hematol Oncol, 2022 Jun 12; 15(1). PMID: 35690784 Review.

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