Immune landscape and response to oncolytic virus-based immunotherapy

doi:10.1007/s11684-023-1048-0

Front. Med.

2024, Vol. 18

Issue (3) : 411-429 https://doi.org/10.1007/s11684-023-1048-0

Immune landscape and response to oncolytic virus-based immunotherapy

Chaolong Lin^1,², Wenzhong Teng^1,², Yang Tian^1,², Shaopeng Li^1,², Ningshao Xia^1,²(

), Chenghao Huang^1,²(

)

¹. State Key Laboratory of Vaccines for Infectious Diseases, Xiang An Biomedicine Laboratory, Department of Laboratory Medicine, School of Public Health, Xiamen University, Xiamen 361102, China
². National Institute of Diagnostics and Vaccine Development in Infectious Diseases, State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, Xiamen University, Xiamen 361102, China

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Abstract

Oncolytic virus (OV)-based immunotherapy has emerged as a promising strategy for cancer treatment, offering a unique potential to selectively target malignant cells while sparing normal tissues. However, the immunosuppressive nature of tumor microenvironment (TME) poses a substantial hurdle to the development of OVs as effective immunotherapeutic agents, as it restricts the activation and recruitment of immune cells. This review elucidates the potential of OV-based immunotherapy in modulating the immune landscape within the TME to overcome immune resistance and enhance antitumor immune responses. We examine the role of OVs in targeting specific immune cell populations, including dendritic cells, T cells, natural killer cells, and macrophages, and their ability to alter the TME by inhibiting angiogenesis and reducing tumor fibrosis. Additionally, we explore strategies to optimize OV-based drug delivery and improve the efficiency of OV-mediated immunotherapy. In conclusion, this review offers a concise and comprehensive synopsis of the current status and future prospects of OV-based immunotherapy, underscoring its remarkable potential as an effective immunotherapeutic agent for cancer treatment.

Keywords oncolytic virus immunotherapy immunotherapeutic agents immune landscape

Corresponding Author(s): Ningshao Xia,Chenghao Huang

Just Accepted Date: 10 January 2024 Online First Date: 08 March 2024 Issue Date: 17 June 2024

Cite this article:

Chaolong Lin,Wenzhong Teng,Yang Tian, et al. Immune landscape and response to oncolytic virus-based immunotherapy[J]. Front. Med., 2024, 18(3): 411-429.

URL:

https://academic.hep.com.cn/fmd/EN/10.1007/s11684-023-1048-0
https://academic.hep.com.cn/fmd/EN/Y2024/V18/I3/411

Fig.1 The mechanisms by which oncolytic viruses exert their antitumor effects. (A) OVs designed to selectively replicate in and lyse tumor cells are a promising agent for cancer therapy. By targeting tumor cells specifically, oncolytic viruses can minimize toxicity to healthy tissues while maximizing antitumor effects. (B) OVs can also stimulate the immune system to mount a systemic antitumor response. (C) OVs can target and destroy tumor blood vessels, leading to tumor cell starvation and eventual death. (D) OVs can selectively target and break down fibrous tissues in the TME, thereby improving the penetration of other cancer therapies and enhancing their efficacy.

Fig.2 OVs induce multimodal ICD and elicit antitumor immune responses. OVs can trigger a wide spectrum of ICD pathways, including several modalities of cell death, such as apoptosis, necroptosis, pyroptosis, and autophagy. ICD induces the release of multiple DAMPs, which subsequently trigger multifaceted immune responses. These immune responses include crucial processes involving in the recruitment, activation, maturation, antigen-phagocytosis and cross-presentation by APCs, ultimately leading to robust antitumor immune responses. ATP, adenosine 5′-triphosphate; TAAs, tumor-associated antigens; APCs, antigen-presenting cells; ANXA1, annexin A1; HMGB1, high-mobility group box 1; CRT, calreticulin.

Fig.3 Oncolytic viruses reshape the TME in multiple dimensions. Tumor cells infected with an oncolytic virus are surrounded by various types of immune cells, such as neutrophils, dendritic cells, natural killer cells, and T cells. Viral infection triggers the release of cytokines, chemokines, and DAMPs from the tumor cells, leading to activation of an innate immune response. The released signaling molecules recruit and activate immune cells, which converge toward the tumor cells. The oncolytic virus causes tumor cell lysis, which exposes TAAs and viral PAMPs to the immune system. Dendritic cells in the TME capture TAAs and migrate to the draining lymph nodes, where they present the antigens to T cells. This process activates an adaptive immune response and leads to the recruitment of additional T cells to the tumor site. The joint actions of innate and adaptive immunity reshape the TME and overcome immunosuppression. The upregulation of MHC-I expression on the surface of tumor cells enables T cells to recognize and efficiently kill the tumor cells, ultimately leading to tumor regression.

Fig.4 Oncolytic viruses can improve antitumor efficacy by enhancing the immune response against cancer. They can carry immunostimulatory cytokines and chemokines, costimulatory molecules, immune checkpoint inhibitors, BiTEs, and tumor-associated antigens. (A) Immunostimulatory cytokines and chemokines (e.g., IL-2, IL-12, IL-7, TNF-α, IL-15, and CXCL9) can activate and recruit T cells, antigen-presenting cells, and natural killer cells, improving the antitumor activity of oncolytic viruses. (B) Costimulatory molecules (e.g., CD40L and 4-1BBL) promote T cell activity and enhance the immune effect mediated by oncolytic viruses. (C) Immune checkpoint inhibitors (e.g., anti-PD-1, anti-TIGIT, and extracellular domain protein of PD-1) are specifically delivered to tumors by OVs, which cannot only mitigate T cell exhaustion but also enhance the efficacy of virotherapy. (D) BiTEs, which are fusion proteins consisting of two single-chain antibody fragments (e.g., anti-CD19/CD3, anti-PD-L1/CD3 and anti-EGFR/CD3) reorient T cells toward tumor cells and activate them to initiate an antitumor immune response. (E) OVs treatment can enhance the recognition of tumor-specific antigens by the immune system and promote a specific antitumor immune response.

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