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Table of Contents
REVIEW
Year : 2023  |  Volume : 6  |  Issue : 1  |  Page : 9-14

Research progress in the treatment of glioblastoma by an oncolytic virus: A narrative review


Department of Neurosurgery, The Third Affiliated Hospital of Kunming Medical University and Yunnan Cancer, Kunming, Yunnan Province, China

Date of Submission09-Feb-2023
Date of Decision04-Mar-2023
Date of Acceptance10-Mar-2023
Date of Web Publication30-Mar-2023

Correspondence Address:
Dr. Wei Ni
No. 519, Kunzhou Road, Xishan, Kunming 650000, Yunnan Province
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/glioma.glioma_3_23

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  Abstract 


Glioblastoma is the most common malignant tumor in the adult primary central nervous system. It has a strong proliferative ability, high recurrence rate, and high malignant degree. Despite standard radiotherapy combined with temozolomide chemotherapy, the prognosis was poor, with a 5-year survival of <10%. Therefore, more effective treatments need to be explored. Oncolytic viruses (OVs) have attracted the attention of researchers because of their unique targeting, safety, and antitumor effects. OV therapy has achieved remarkable efficacy in the treatment of many kinds of malignant tumors, and it has also made great progress in the treatment of glioblastoma. This article reviews the recent clinical research progress of OVs in the treatment of glioblastoma.

Keywords: Glioblastoma, mechanism, oncolytic treatment, oncolytic virus, progress


How to cite this article:
Shao X, Ni W, Xu X, Luo Y. Research progress in the treatment of glioblastoma by an oncolytic virus: A narrative review. Glioma 2023;6:9-14

How to cite this URL:
Shao X, Ni W, Xu X, Luo Y. Research progress in the treatment of glioblastoma by an oncolytic virus: A narrative review. Glioma [serial online] 2023 [cited 2023 Jun 9];6:9-14. Available from: http://www.jglioma.com/text.asp?2023/6/1/9/372823




  Introduction Top


Glioblastoma multiforme (GBM World Health Organization Grade IV glioma) is the most common malignant glioma, with a median survival of only 15 months when treated with maximum safe surgical resection, supplemented by concurrent radiation therapy and temozolomide (TMZ) chemotherapy as standard treatment.[1] The causes of poor prognosis in malignant gliomas are (i) resistance to conventional radiotherapy; (ii) the presence of the blood–brain barrier; (iii) the strong infiltrative nature of the tumor, which cannot be completely removed; (iv) the immune protective state of the brain; and (v) tumor stem cells that have a strong capacity for self-renewal and evade conventional treatment.[2],[3],[4] To overcome these difficult challenges, new therapies targeting the tumor microenvironment have emerged, and oncolytic viruses (OVs) for malignant gliomas are a series of antitumor responses targeting the tumor microenvironment.

OVs therapy has become the frontier of tumor biotherapy, with more prominent results in the field of oncology treatment in the past two decades.[5] 1991 preclinical animal trials reported that genetically engineered herpes simplex virus type I (HSV-1) could inhibit the growth of glioma cells in mice, demonstrating the effectiveness of lytic viruses for the treatment of malignant gliomas.[6] It was reported that the OV therapy Delytact (teserpaturev/G47Δ) received conditional time-limited approval from the Japanese Ministry of Health, Labour and Welfare for the treatment of malignant glioma, making it the first OV therapy approved for the treatment of primary glioma in the world.[7] Several viruses, including cowpox virus, coxsackievirus, adenovirus, enterovirus, HSV, and measles virus (MeV), are currently being studied extensively, including in ongoing clinical trials for the treatment of various types of advanced tumors.[8] This review describes the mechanisms and effects of various OVs on glioma lysis, including clinical studies of various OVs.


  Database Search Strategy Top


The authors used the following search strategy: lytic virus therapy in the treatment of glioma. The authors searched relevant articles published up to February 2023 in China Knowledge Network and PubMed databases, and the literature search strategy was as follows: search keywords glioma, tumor therapy, OVs, mechanism, and review, and randomly combine each keyword to find relevant literature. The characteristics of various lytic viruses and the mechanism of lysis were extracted.


  Mechanism of Oncolytic Virus Therapy Top


OVs are usually naturally occurring or genetically engineered viruses that selectively recognize tumor cells and replicate in tumor cells to kill them without harming normal cells. Similar to other immunotherapies, OVs have multiple mechanisms of action, the main ones being: (i) the virus infects tumor cells and replicates selectively in tumor cells, leading directly to tumor cell lysis; in addition, the viral capsid protein can cause direct tumor cell lysis.[9] (ii) Tumor cell lysis and apoptosis release tumor-associated antigens (TAAs), and tumor-specific immune responses increase, enhancing systemic antitumor effects and breaking tumor vasculature,[10] thus killing tumors. (iii) Most of the OVs are genetically modified to carry or express the corresponding OV drugs or molecules, which are released into tumor tissues to kill tumor cells and enhance the tumorolytic effect.[11],[12] In conclusion, most lysing viruses are genetically engineered to enhance their tumor targeting and reduce the toxic side effects on normal tissue cells, and the invasion of tumor cells by lysing viruses promotes the release of cytokines and pathogen-associated molecular patterns, DAMPs damage-associated molecular patterns, and TAAs from tumor cells, further activating the immune system, causing T-cells, natural killer cells, macrophages, and other immune-related cells to activate, accumulate toward tumor cells and kill them [Figure 1].
Figure 1: Infection of tumor cells by the lymphoma virus causes them to release a large number of cytokines, which activates immune cells such as microglia, NK cells, and T-cells. Moreover, the lymphoma virus can induce tumor cells to release molecules such as PAMPs, DAMPs, and TAAs, which further activate the immune system, causing microglia to release chemokines, and NK cells and T-cells to accumulate toward tumor cells and kill them. DAMPs: Damage-associated molecular patterns, ER: Endoplasmic reticulum, IFN-γ: Interferon γ, IL-2: Interleukin-2, IL-6: Interleukin-6, MHC: Major histocompatibility complex, NK: Natural killer, PAMPs: Pathogen-associated molecular patterns, PD-1: Programmed death 1, PD-L1: Programmed cell death-ligand 1, TAAs: Tumor-associated antigens, TCR: T cell receptor, TGF-α: Transforming growth factor-α, TGF-β: Transforming growth factor-β

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  Various Lytic Viruses Top


Herpes simplex virus

HSV is a double-stranded DNA virus that encodes 84 polypeptides and has a 152-kb long genome with a large viral gene that can easily be genetically engineered to become a tumorolytic virus. It can infect most tumor cells and its viral particles can produce a toxin effect on tumor cells.[13] HSV has been reported to be a promising tool for the development of OVs therapies,[14] and HSV tumor lysis can both directly lyse tumor cells and enhance the immune response of the tumor microenvironment. Viral entry into tumor cells requires the involvement of membrane receptors, and once the tumor cells are lysed, TAA are subsequently released to induce a systemic or local antitumor response.[15] The two main serotypes currently used for OV therapy are HSV-1 and HSV-2.[16] Among them, HSV-1 has a wide range of hosts, can carry much exogenous genetic information, and has various advantages such as easy modification and neurophilicity. Most of the oncolytic HSV (oHSV) currently in clinical trials were obtained by modifying HSV-1.[17] After research, there are clinical trials of the first generation of oHSV, such as HSV1716, which lacks the RL1 gene, which encodes the ICP34.5 protein that is neurotoxic. HSV1716 can proliferate in GBM cells cultured in vitro but not in normal tissues, and animal tests have confirmed this idea. Harrow et al. had intratumoral injections of HSV1716 in nine patients with no significant adverse effects during treatment, and four patients survived 14–24 months, with a slightly longer median survival than the standard treatment regimen. Subsequently, in 2004, 12 patients with glioma were collected and the lack of neurotoxicity of HSV1716 was confirmed by intratumoral injection of HSV1716 into the resected tumor cavity and reported survival of 15, 18, and 22 months in three patients injected with HSV1716, further confirming the efficacy and safety of HSV1716.[18]

A more typical second-generation oHSV is talimogene laherparepvec (T-VEC), which is missing two gene fragments, namely, deletion of γ134.5 and α45, and insertion of a human granulocyte-macrophage colony-stimulating factor at the γ134.5 locus. T-VEC has now become the first lysing virus approved by the US Food and Drug Administration that can be used in any advanced malignancy.[19] The third-generation oHSV is G47 Δ, which is a viral mutant created by knocking out the α47 gene in G207. Phase I clinical trials have been completed, and the results of the trials have not been reported. It has been reported that Fusheng Liu's team has developed a novel oncolytic virus, ON-01, and the results of animal experiments show that lysovirus ON-01 has good efficacy in treating malignant glioma and is currently in the clinical patient recruitment stage.

Adenovirus

Adenoviruses are the first envelope-free, linear double-stranded DNA viruses derived from human glands, approximately 70–90 nm in size, that usually cause symptoms of upper respiratory tract infections. Adenoviruses can be divided into six subtypes and 57 serotypes depending on their surface particles. The genetic information of human adenovirus types 2 and 5 has been well studied and is commonly used in the preparation of tumor-lysing viruses.[20] The adenovirus can bind to the Coxsackie and adenovirus receptor on the surface of tumor cells to enter the tumor cells.[21] The E1 gene is divided into the E1A and E1B genes, and the E1A gene encodes the E1A protein, which is synthesized early after infection with tumor cells and is a protein required for viral replication. Recombinant human type 5 adenovirus is to knock out E1B-55kD and E3 partial gene fragments in the human type 5 adenovirus gene. This recombinant human type 5 adenovirus can selectively replicate in P53-mutated tumor cells and has a cytotoxic effect. It can have a killing effect on P53-mutated tumors within an effective concentration without damaging normal cells. The recombinant human type 5 adenovirus with E1B-55kD knockdown cannot bind to P53 protein in normal cells, thus making it impossible to prevent the clearance of adenovirus by normal cells and therefore does not damage normal cells. In contrast, in tumor cells with P53 mutation, the loss of the P53 gene cannot encode P53 protein, making the tumor cells unable to clear the adenovirus and the virus can replicate and lyse the tumor cells in large numbers within the tumor cells. This released a large number of daughter viruses reinfect the surrounding tumor cells and gradually kill the tumor cells.[22],[23]

The first lysing adenovirus was Onyx-015, and a 2004 trial of Onyx-015 injected intraoperatively into the luminal cavity of a surgically resected tumor for recurrent malignant glioma showed no clear antitumor response. DNX-2401 (Delta-24-RGD, or tasadenoturev) is a highly effective adenovirus for the treatment of glioma, with a strong tumor lysis effect, high replication capacity, and high safety profile. 2401 can effectively infect tumor cells expressing Coxsackie and adenovirus receptors.[24] Lang et al.[25] reported a phase I clinical trial on DNX-2401, which included 37 patients with malignant glioma, the results of the preoperative injection followed by re-injection into the tumor cavity at the time of surgery showed that five of the patients survived more than 3 years and two of the patients survived more than 2 years. This genetically engineered DNX-2401 effectively improves the lysis effect and brings new hope for OV therapy. There are also trials on DNX-2401 synergistic with TMZ chemotherapy and interferon-gamma combined with OVs for antitumor therapy.

Echovirus (reavirus)

Enterovirus is an envelope-free, double-stranded RNA virus with a genome consisting of 10 dsRNAs that encode eight structural and four nonstructural proteins.[26] It can infect the respiratory and intestinal tracts but does not cause significant symptoms, and no serious diseases caused by this virus have been identified.[27] Echovirus has a robust genome, and its replication process is still not clearly defined, which makes it difficult to modify it by genetic engineering. However, many mutated wild-type eutherian viruses exist in nature, which have a strong tumorolytic effect. Its unique double-stranded RNA encodes protein kinase R, which prevents protein synthesis and thus promotes apoptosis. Most tumor cells activate the Ras system through mutations in the gene encoding the epidermal growth factor receptor, allowing Escherichia coli to specifically recognize tumor cells and promote apoptosis. Samson et al.[28] completed a phase Ib trial in 2018, enrolling nine cases of high-grade gliomas and brain metastases that were given intravenous reavirus before surgery. The study showed a median survival of 15 months with preoperative administration of intravenous Reolysin, and analysis of resected tumor tissue confirmed that the eutherian virus crosses the blood–brain barrier to reach the tumor site and is restricted to replicate at the tumor site. The clinical trials that have been conducted so far have confirmed that Echovirus alone is not effective in the treatment of glioma, and its possible combination with other antitumor chemotherapeutic agents may have better results and is worth further exploration.

Measles virus

MeV is a single-stranded negative-stranded RNA virus belonging to the paramyxovirus family, which is a relatively common and highly infectious human pathogen that usually causes a distinctive red rash. MeV enters tumor cells through receptors such as CD 150/SLAM, nectin-4, and the complement regulator CD 46.[29] In glioblastoma, the regulation of nectin-4 levels by miR-31 and miR-128 is associated with an increase in nectin-4 receptor levels, promoting viral entry into tumor cells.[30] The mechanism of MeV tumor lysis is not clear, and early studies found that MeV-infected cells have increased apoptotic markers that elevate immunogenicity and promote the production of pro-immune cell migration factors ccl3, ccl4, ccl5, and ccl10 expression in the tumor microenvironment, thereby increasing the expression of immune cells such as T-cells in the tumor microenvironment. Allen et al.[31] conducted an in vitro trial of MeV lysis in 2013, which demonstrated the effectiveness of MeV in glioma lysis. Meanwhile, related trials demonstrated that tumorolytic MeV could treat relapsed refractory myeloma and patients could effectively relieve the clinical symptoms associated with myeloma, indicating that MeV has a powerful tumorolytic effect.[32],[33] Related studies have observed a synergistic effect of MeV with radiotherapy on GBM in in vitro trials[34] and a synergistic antitumor effect with chemotherapeutic agents.[35] Current clinical trials of MeV for glioma include monotherapy and combined TMZ chemotherapy and combined radiotherapy, and these clinical trials have yielded relatively promising results.

Newcastle disease virus

Newcastle disease virus (NDV) is an enveloped, single-stranded, negative-stranded RNA virus that also belongs to the paramyxovirus family and is primarily an avian pathogen that causes only mild symptoms in population species. The weaker strains of nipah virus tend to be tumorigenic and promote viral entry into tumor cells mainly through the binding of their encoded hemagglutinin-neuraminic acid protein to the sialic acid receptor on the surface of tumor cells. The entry of neoplastic viruses into tumor cells induces tumor cells to secrete Bcl-2 family proteins, resulting in mitochondrial damage and loss of membrane potential. Two types of NDVs, MTH-68/H, and NDV-HUJ (HUJ virus strain of Newcastle disease virus) have been used in clinical trials for the treatment of malignant gliomas, and MTH-68/H was mainly administered intravenously to treat patients with recurrent GBM and mesenchymal astrocytoma.[36] Csatary et al.[37] conducted a clinical trial on MTH-68/H for the treatment of malignant gliomas. No adverse events were reported with MTH-68/H during the trial. Meanwhile, Freeman et al.[38] conducted a phase I/II clinical trial, in which 1 of 14 patients with NDV-HUJ had a complete remission, and this trial initially confirmed the safety and reliability of NDV treatment for glioma. At present, the treatment of malignant glioma with NDV is still in the exploratory stage, and there is still a lot of unknown information that needs to be studied by our department.

Other viruses

Poliovirus (PV), an envelope-free single-stranded RNA virus, is a natural neurological pathogen with neurotropic properties. PV can bind to the PV receptor CD155 on the surface of tumor cells and promote viral entry into tumor cells. In contrast, CD155 is highly expressed in glioma cells, which makes PV have strong antitumor properties.[39] The PV currently used for the treatment of malignant glioma is recombinant nonpathogenic PV-rhinovirus chimera, and its phase I clinical trial for the treatment of malignant glioma was reported in 2018, which treated 61 recurrent gliomas, with 21% of patients surviving long-term at 24 and 36 months.[40] Another study on parvoviruses (ParvOryx) showed that ParvOryx can cross the blood–brain barrier and have the potent antitumor potential,[41] offering new hope for OV therapies. Other OV therapeutic viruses are bovine pox virus and vesicular stomatitis virus in active animal testing, all of which have greater potential and further offer new hope for OV therapy.


  Challenges and Hopes of Oncolytic Viruses Therapy for Malignant Glioma Top


In the past 30 years, with the rapid development of genetic engineering, OVs therapies have developed rapidly, and through the modification of viral genes, OVs have better safety, targeting, and efficacy. Meanwhile, with the continuous understanding of microorganisms, more and more viruses are used to modify into lysing viruses, and even phase I, phase II, and even phase III clinical trials have been conducted, bringing the possibility of prolonging life and improving the quality of survival for glioma patients. The route and timing of viral administration are one of these challenges, and different time windows and routes of administration may have very different consequences. Postsurgical perineural injections of OVs have been shown to be effective in producing antitumor effects, and some OVs that can cross the blood–brain barrier have also been shown to reduce tumor size. Again, different time windows of administration bring different effects. The dose of the virus is also a big challenge; low doses do not achieve antitumor effects and high doses may bring about side effects of the virus. In addition, the safety of OVs remains to be studied, as the human body reacts differently to different OVs, and we need to study the possible consequences of OVs therapy thoroughly before conducting clinical trials. Despite the many uncertainties and limitations of OVs therapy, many clinical studies of OVs in combination with other therapies have been conducted. There are synergistic effects of OVs in combination with radiotherapy in multiple models, and one study showed that the synergistic effects were dependent on radiation-induced inhibition of the JNK signaling pathway.[42] There are precedents for OVs in combination with chemotherapy, such as adenovirus in combination with cisplatin, TMZ, and paclitaxel. Antitumor therapy with OVs combined with chemotherapy enhances the antitumor effect and may prolong patient survival.[9] OVs combined with immune checkpoint inhibitor therapy offers a new prospect for antitumor therapy, and studies have found synergistic effects of PD-1 and cytotoxic T lymphocyte antigen 4 (CTLA-4) immune checkpoint inhibitors with OVs therapy in initiating and enhancing immune responses.[43] There are also some studies suggesting that OVs combined with immune checkpoint inhibitors have more potent antitumor effects.

Limitations

This article has some limitations. It only summarizes the mechanistic effects of various OV reported in the database literature and fails to laboratory test replicate experiments to verify whether they are real and effective, with some information bias. Overview of the relevant viruses has limited access to information and does not provide a comprehensive overview of the characteristics of the viruses and their mechanisms in glioma treatment.


  Conclusion Top


OV therapy has a certain antitumor effect and certain safety for glioma. A large number of clinical trials have shown that different OVs have different tumor lysis mechanisms, and all of them can produce better tumor lysis effects. The safety, efficacy, and usefulness of OV therapy need to be further improved in the future. Despite the challenges of OVs therapy for glioma, many studies on OVs therapy have achieved satisfactory results, and it is believed that OVs therapy will bring good news to glioma patients in the near future.

Acknowledgments

We would like to thank Wei Ni's medical team for their support of this article, including Wei Ni for coordinating the process of the article and proposing the overall idea of the article, Xiangxiang Shao for collecting and organizing relevant data and writing the article, Yuanyuan Luo for viral characteristics data, and Xiaobin Xu for collecting clinical experimental data of lysosomal disease.

Financial support and sponsorship

This work was supported by the Medical Reserve Talent Training Program of Yunnan Provincial Health and Family Planning Commission (H-2017048).

Conflicts of interest

There are no conflicts of interest.



 
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