Pemra Nesil1, Züleyha Pestil2, Oytun Erbaş1

1ERBAS Institute of Experimental Medicine, Illinois, USA & Gebze, Turkey
2Pendik Veterinary Control Institute, İstanbul, Turkey

Keywords: Cancer immunotherapy, engineered viruses, oncolytic virus, tumor receptors, virotherapy

Abstract

Oncolytic viruses (OVs) are effective in curing cancer as they selectively infect and kill malignant tissues while causing no harm to healthy tissues. Every virus has a unique cellular tropism that dictates which tissues are preferentially infected and what disease is caused. Numerous naturally occurring viruses have a preferred, but not exclusive, affinity for tumors and tumor cells. This likely has more to do with tumor biology than virus biology since most tumors have evolved to resist apoptosis and translational suppression, which are essential responses used by normal cells to limit a virus infection. This means that tumor biology rather than virus biology is more likely to be at play here. Infected cancer cells can be eliminated by OVs in a variety of ways, from direct virus-mediated cytotoxicity to diverse cytotoxic immune effector pathways. Viruses typically infect a small number of host species, and productive infection beyond the native host range only rarely occurs. A novel host species' infection may present as a unique disease. In this context, using nonhuman viruses in clinical treatment can raise some red flags. It may give the viruses a chance to adapt to the new host and spread to the recipient's family members, healthcare providers, or even the typical host species. Clearly, such environmental damage is not desired, particularly in light of the coronavirus disease 2019 pandemic. This review primarily attempts to evaluate the impact of the most prevalent OVs and their action mechanism and explore potential future consequences of non-human viruses on human cancer therapy.

Cancer immunotherapy is an approach that has been more popular in preclinical research and clinical application during the past decade.[1] In addition to surgery, radiation, chemotherapy, and targeted therapy, cancer immunotherapy is now considered to be the fifth cornerstone of cancer treatment.[2-4]

Traditional oncolytic therapy appears to immediately eliminate or destroy cancer cells, but it has a high probability of recurrent or seriously negative side effects.[5] To focus treatment with targeted therapy, it is necessary to identify known oncogenic sites. Immunotherapy, on the other hand, fights cancer by using certain parts of the body’s immune system.[6,7] It aims to improve the host immune system’s capacity to eliminate cancer cells and aid in tumor regression, the development of anti-tumor immunological memory, and eventually persistent responses.[8]

Immunotherapy has great potential to cure cancer with very low side effects and high tumor elimination expectations. It includes adaptive cell therapy, immune checkpoint blockade, cytokine therapy, cancer vaccines, and oncolytic virotherapy as one the most encouraging therapies.[9,10] Now it’s supplied in the treatment of multiple cancers. The aim of the paper is to provide a conceptual theoretical framework based on the most popular oncolytic viruses (OVs) and non-human viruses’ considerable position in this content.

VIRAL ONCOLYSIS: HISTORICAL PERSPECTIVE

There has long been interesting in developing an approach by which tumor cells can be selectively and specifically targeted and destroyed. Surprisingly OVs viral strains can infect and kill malignant cells without harming normal cells while simultaneously stimülate the immune system and creating a system anti-tumor immunıty. Although viruses have been utilized as therapeutic agents in the form of vaccines since the late 1700s.[11] Their potential application as a cancer therapy was not explored until a series of earliest clinical reference reports dating back to the early 1900s. The first case was in 1904 in which a 42 years old woman with chronic myelogenous leukemia experienced a marked reduction in white blood cells during a flu-like illness.[12] Later, a range of other tumor types and viruses were involved in tentative oncolytic therapies, but because of the dreadful side effects, interest in OVs declined from the 1970s through the 1980s until the 1990s. In clinical studies, 22 patients with Hodgkin’s disease were treated with a total of 35 sera or tissue extracts containing “the hepatitis virus.”. These individuals had either infectious hepatitis, a self-limited picornavirus infection, or serum hepatitis, most likely caused by hepatitis B.[13] Flavivirus infections such as West Nile, Uganda, dengue, and yellow fever were highly common in the United States and elsewhere in 1952 and hence were among the first to be employed for OVs. Most patients had viremia and intra-tumoral viral multiplication, although tumor responses were uncommon. Immunocompromised individuals with leukemia or lymphoma were more likely to respond to medication, but they were also at a greater risk of fatal neurotoxicity. So, out of eight leukemia or lymphoma patients, five had severe encephalitis.[14,15]

Adenoidal-pharyngeal-conjunctival (APC, now known as an adenovirus) virus was discovered to be an antitumor agent in preclinical models in the 1950s. It quickly advanced to the point of care and was found to have fairly symptoms: most who received APC infrequently experienced pharyngeal or eye inflammation, were able of encephalitis, and, better yet, were quite alive after inoculation.[16] The development of genetic engineering in the 1990s made it possible to author viral genomes, and viral therapy has achieved a leap from laboratory to clinical.[17]

Four OVs have been authorized internationally till now. Professor Aina Muceniece led a team of Institute of Microbiology and Virology researchers to discover that human intestinal viruses may eliminate tumors in the 1960s in Latvia. To conduct the research Muceniece founded the Cancer Virotherapy Laboratory in 1965. Upon the analysis of 60 intestinal viruses, five were deemed the most effective in fighting cancer cells. One of them is the Riga virus (Rigvir). Extensive studies were carried out and permission was granted to use the virus in clinical practice but the process was delayed due to the shifting political climate. Rigvir is the first OV to be filed and approved. It was formally registered in Latvia in 2004. Rigvir is an OV of the Picornaviridae family, Enterovirus genus, enteric cytopathic human orphan (ECHO) virus group, type-7, which is not genetically changed but has been chosen and optimized for melanoma however it was never broadly adopted.[18] Encouragingly the adenovirus mutant H101 became the world’s first OV drug approved for cancer treatment in 2005 in China to treat head and neck cancer.[19] An engineered herpes simplex virus (HSV)-1, named Talimogene laherparepvec (T-VEC) became the first OV approved by the Food and Drug Administration (FDA) in October 2015 for the intralesional treatment of melanoma.[20] At last, a modified herpes simplex virus was approved in Japan in 2021 for brain malignancies including glioblastoma.[21] Now the technologies of other forms of immunotherapy gaining ground and cancer despite all advances remains a major cause of mortality.

CHARACTERISTICS OF ONCOLYTIC VIRUSES AND CLINICAL TRIALS

Herpes Simplex Virus

Herpes simplex virus type 1 belongs to the alpha herpesvirus family, which also involves the varicella species. It is a DNA virus that includes a wide genome (152 kilobase/kb), 30 kb of which transmit genomes that are not obligated for the disease process. Upregulation of many receptors in cancer cells, like nectin-1 and the tumor necrosis factor (TNF) superfamily member herpesvirus entry mediator (HVEM), is necessary for oncolytic HSV infection of cancer cells.[22] HSV-1 replication materialized in the nucleus, but it is not mutagenic to its host.[23] The neurotoxicity of HSV can be significantly reduced by gene editing techniques that delete out or modify the HSV gene RL1, decreasing the production of the neurotoxic protein ICP34.5 (infected cell protein 34.5).[24] These characteristics make HSV-1 a promising option for the formation of OVs. HSV has quite a wide and adaptable genome. To enhance the anti-tumor impact, several foreign genes may be inserted, and the glycoprotein on the surface of HSV is either modified.[25] The essential to utilizing HSV for oncolytic therapy is genetically modified techniques, which involve removing the primary genes that enter normal cells, multiply and flourish in healthy cells, and infect tumors selectively.

Table 1 lists a number of the mutant HSV strains that are currently in use as OVs.

1) The first type 1 HSV mutant, dlsptk, has a mutation in its UL23 gene that inhibits it from making the protein thymidine kinase, which can stop mouse gliomas from spreading.[26] Direct injection of dlsptk into developing human gliomas in the brains of athymic mice resulted in dose-dependent tumor cell killing, improved animal survival, and in some cases, total cure for cancer.[27] Increasing the dosage will have major side effects, including encephalitis.[28]

2) The R3616 strain of HSV-1(F) greatly increases its anti-tumor efficacy by knocking out two genes that express ICP34.5.[29] Technical studies have demonstrated that R3616 can enter tumor antigenspecific lymphocytes, destroy the original tumor, and limit distant metastasis and recurrence.[30] Clinical trials showed that R3616 reduced tumor size in immunodeficient mice implanted with glioma cells.[31]

3) HSV1716, a strain generated from the HSV-1 (17+) strain, double-deletes the neurotoxicity-determining gene RL1. Protein kinase R (PKR) phosphorylates eukaryotic initiation factor 2a (eIF2a), which prevents translation and triggers apoptosis in tumor cells as well as virus mortality.[32] HSV1716 can be employed in cancer cells with unregulated protein production because the ICP34.5-mediated dephosphorylation of eIF2a can enhance protein translation and prevent cell death.[33] An OV clinical study using HSV1716 for malignant pleural mesothelioma revealed that it was well-tolerated and has anticancer activity. In seven of 12 patients’ tumor lesions, HSV proliferation and existence were consistently found. Within week eight, the patient’s stable disease (SD) was reported by half of them.[34]

4) G207 was the first HSV to be tested in medical trials on cancer. The virus can now integrate only in cancerous cells thanks to the lacZ gene that was placed into the removed ICP34.5 locus. Via PKR, the knockdown mutant ICP34.5 causes the suppression of late viral genes, such as US11. G207 stimulates cytotoxic T cells and causes the patient to develop systemic anti-tumor immunity.[35] Human glioma cells were killed by G207 treatment in monolayer cultures, while nude mice with subcutaneous or intracerebral U-87MG gliomas were treated intratumorally to slow tumor development and/or extend life. Additionally, intracerebral injection of mice and HSV-sensitive non-human primates with G207 revealed that it was avirulent.[36] Intracranial gliomas implanted in mice were subjected to cellular effects of oncolytic G207 treatment, which demonstrated broad regions of viral infection and replication (plaques), lower growth indices, and increased apoptotic frequencies in infected parts of the lesions. This study discovered a considerable reduction in the size of blood vessels in the lesions in addition to the direct death of tumor cells, indicating that G207 had both tumoricidal and antiangiogenic effects.[37] Based on phase I/II study data recently published at Tokyo University Hospital and Tokyo University Institute of Medical Sciences (data cutoff date, November 27, 2014; survival confirmed to March 1, 2022); After a 2-year monitoring period following the last G47 treatment, 10 out of 13 patients had died. One patient who demonstrated partial remission (PR) endured G47 treatment for more than 11 years (as of March 1, 2022). This patient lives without experiencing any more recurrences and does not have any long-term unfavorable effects from G47, such as an autoimmune disease in the central nervous system, which was one of the apparently predicted side effects.[38]

5) The G47∆ strain of HSV, which was confined from the G207 strain, has genetic changes in the RL1 and ICP47 genes as well as an addition of the lacZ gene fragment into its ICP6 gene. This decrease in the large subunit of the ribonucleic acid reductase gene that it encodes causes the oncolytic HSV to be more actively replicated in cancer cells.[39] G47 was given intratumorally and repeatedly for up to six dosages. The main objective was 1-year survival rate following G47 start, which was 84.2% (95% confidence interval/CI), 60.4-96.6; 16 of 19). The experiment was discontinued early since the predetermined endpoint was fulfilled. In terms of secondary endpoints, the median overall survival after G47 commencement was 20.2 (16.8-23.6) months and 28.8 (20.1-37.5) months after the original operation. Fever (17 of 19) was the most prevalent G47-related adverse event, followed by vomiting, nausea, lymphocytopenia, and leukopenia.[40]

6) The virus HF10 underwent spontaneous mutation without the addition of any foreign genes. The linear double-stranded DNA (dsDNA) HF10 genome contains 6,127 kb of naturally occurring deletion, 6,027 base pair (bp) of insertions, and frame-shift mutations at various nucleotide locations. The UL43, UL49.5, UL55, UL56, and latency-associated transcript (LAT) gene activity was lost as a result of these deletions and insertions, while UL53 and UL54 were overexpressed.[41] In the phase I clinical investigation, HF10 was inoculated intratumorally into cutaneous or subcutaneous spreading nodules of recurrent breast tumors to assess its safety and effectiveness at the Nagoya University Graduate School of Medicine, in Japan. No significant side effects were experienced by any of the patients despite good treatment compliance. Histologically, tumor mortality of 30 to 100% was seen along with tumor cell distortion. Unexpectedly, after the elimination of tumor cells, a wide spectrum of melting-like fibrosis was seen.[42.43] In Japan, after intratumoral injection of HF10 [1x105 plaque forming units/milliliter (pfu/mL) or 0.5 mL for 3 days], adverse effects, viral replication, and immune response were assessed. With considerable infiltration of the cluster of differentiation 4 (CD4+) or CD8+ cells in both patients, HF10 replicated efficiently and caused apoptosis of tumor cells. After receiving the injection, individuals had a cold temperature, but no other overt side effects.[44] From 2005 through 2009, eight male patients with aggressive pancreatic ductal carcinoma underwent a phase I clinical study at Nagoya University’s School of Medicine in Japan. Without after-treatment side effects being noticed, all patients tolerated the therapy properly. The tumor marker carbohydrate antigen 19-9 (CA19-9) decreased in three cases. Three patients had complete remission as their therapy response, one patient had a limited response, and four individuals had advancing illnesses. With an average of 180 days, the survival period varied from 98 to 318 days.[45,46] Twenty-six patients with melanoma and other resistant and superficial cancers were involved in a phase I study to evaluate the safety of intratumoral (IT) delivered HF10. Eighteen of the 24 patients who got therapy experienced adverse events, six that were attributable to HF10. Chills (two patients), redness, edema, and discomfort at the injection site (one patient), lethargy (one patient), pruritus (one patient), and hypotension (one patient). After a single injection, one patient experienced ulceration of tumor sites at both injected and non-injected lesions, but healthy tissue did not show any ulcers.[47]

7) M032 is a c134.5 deleted HSV-1 virus that expresses human interleukin (IL)-12. The experimental effectiveness and safety of M002 were shown, however, if this virus was used in human clinical trials, there was a risk of an unfavorable immunological reaction to the murine IL-12 protein.[41] Scientists constructed the c134.5-deleted oncolytic HSV M032, which has the same structure as M002 but expresses the human IL-12, p35, and p40 subunits. A clinical study of M032 in patients with malignant gliomas is still being tested. Nonhuman primate (NHP) models were assessed following intracerebral injections of saline, 1106 pfu, or 1108 pfu of M032.[48]

8) Talimogene laherparepvec remove ICP34.5 area factor genes were merged with HSV genes encoding ICP34.5 and ICP47, as well as a number of cytokines, including granulocyte-macrophage colony-stimulating factor (GM-CSF), IL-12, interferon alpha (IFN-α), TNF-alpha, and others. As a result, oncolytic HSV’s anti-tumor immune function is improved, antigen-specific T lymphocytes’ immunostimulatory capacity is increased, CD4+ T cell’s negative immune regulation is decreased, and CD8+ T cells exhibit a particular anti-tumor impact.[49,50] The first OV authorized by the FDA for the treatment of melanoma was T-VEC, an HSV-1 virus that encodes GM-CSF.[51] T-VEC was utilized as an adjuvant medication following melanoma surgery in phase II clinical research. With or without T-VEC postoperatively, 150 postoperative patients with stage IIIB-IVM1a melanoma were split equally into two groups for the purpose of assessing the surgical risk of melanoma recurrence. After three years of monitoring, 17.1% of patients who received T-VEC treatment post-surgery experienced pathological complete remission (pCR) and elevated CD8+ in tumor lesions. Postoperative adjuvant therapy decreased total melanoma recurrence by 25% in the T-VEC arm when opposed to the surgery solo group.[52]

Adenoviruses

Adenovirus is an icosahedral capsid with a virion width ranging from 70 to 90 nanometers (nm). It is a naked (non-enveloped), double-stranded DNA virus with a linear genome of around 35 kb. Its enormous genome allows for the incorporation of lengthy DNA sequences, enabling several engineered changes. Both animals and humans are frequently infected with adenoviruses, which can spread by aerosols and making contact. Therefore, the vast majority of people are seropositive for adenovirus exposure. Adenoviral infections can cause diseases in infants and vulnerable people even when they are asymptomatic in immunocompetent hosts.[53] The coxsackie-adenovirus receptor (CAR) allows adenovirus to get into the cell. When an adenovirus enters a cell, it travels to the nucleus and expresses adenovirus early genes (encoding E1A and E1B), which are required for viral replication. To enhance cell cycle entrance, E1A and E1B intentionally target the tumor suppressors p53 (a tumor suppressor gene that produces a protein that controls cell growth and proliferation) and retinoblastoma-associated protein (pRb). In normal cells, however, adenoviral E1A and E1B protein binding of host cell cycle regulators p53 and pRb culminate in death and virus elimination.[54,55] Adenovirus is an appealing vector for clinical testing due to its capacity to effectively decrease viral pathogenicity and encode big foreign transgenes. Human serotype 5 adenoviruses, a frequently used oncolytic adenovirus vector, is ineffective in infecting tumor cells because most tumor cells have poor or no CAR expression on their membrane.[56] As a result, some experiments insert RGD (a short peptide made up of the amino acids arginine) glycine, and aspartic acid, into the viral capsid fibers.[57] Antitumor adenovirus vectors with RGD are more able to actively target tumor cells because they can bind the highly expressed integrin αvβ3 receptors in cancerous tissue.[58] Adenovirus can be altered with usable targeting groups in addition to RGD. Examples include targeting CD46, which is elevated in colorectal and breast cancer[59], or desmoglein, which is highly expressed in a range of malignant epithelial tumors.[60] After showing that adenovirus can successfully reproduce in huge numbers in tumor cells, the researchers included a variety of foreign genes, such as TNF-related apoptosis-inducing ligand (TRAIL)[61] or adenoviral death protein (ADP)[62], into the genome of the oncolytic adenovirus vector. Another type of gene that has been used is the prodrug activator, whose expression encourages the transformation of nontoxic prodrugs into toxic compounds in the limited region of the tumor and also delivers these toxic substances to nearby non-infected tumor cells through gap junctions between tumor cells, improving the tumor suppressor effect.[63] For instance, viruses that can encode the herpes simplex virus type 1 thymidine kinase (HSV-tk)[64] or bacterial cytosine deaminase (CD).[65] These encoded proteins can help cancer areas convert prodrugs like acyclovir or 5-fluorocytosine into hazardous compounds, greatly increasing the anticancer effect of adenovirus.[66] Adenoviruses are able to immediately destroy tumor cells, but they can also create a lasting, particular anti-tumor immunological memory in the body, which is crucial for the body’s long-term prognosis. However, adenovirus replication must continue in order to maintain this immunological response.[67] When adenoviruses in tumor cells are eliminated, the total viral population decreases, reducing the long-term therapeutic effect. Over the last ten years, research on oncolytic adenoviruses has shifted from optimizing the rapid destruction of cancer cells to increasing the immune response induced by viral oncolysis. This concept leads to the addition of additional immunomodulatory adenoviral vectors to oncolytic adenoviral vectors, such as GM-CSF, CD40 ligands, or IFN-1.[68]

Adenoviruses have two stages to their cell replication. Accordingly, early (E1-E4) and late (L1-L5) transcription units are organized into the adenoviral genome. The two primary isoforms, 12S and 13S, which are encoded by the early region 1A (E1A) and are necessary for early replication, are five distinct proteins.[69,70] While E1A 12S missing CR3, the E1A 13S protein has 289 amino acids and four conserved domains (CR1-CR4), allowing it to transactivate the other early transcription units E1B, E2, E3, and E4.[71] Adenoviruses with the E1 gene removed are thought to be replication-deficient and are employed in gene therapy or immunization as transport vectors. In oncolytic adenovirus treatment, replication-competent adenoviruses that are only capable of reproducing in cancer cells are known as conditionally replicating adenoviruses (CRAds).[72]

Table 2 lists several mutant adenovirus strains that have been identified and exploited as OVs.

1) Tumor-specific promoters are distinguished by their capacity to increase the expression of particular genes that are essential for a malignant phenotype. Replication is limited to the proper cells when E1A-mediated viral proliferation is controlled by a tumor- or tissue-specific promoter.[73] Therefore, the E1A regulatory region of exogenous promoters is often inserted without any or with minor deletions, leaving the E1A enhancer/encapsidation intact as in CRAd-Survivin-pk7.[74] CRAd-Survivin-pk7 has a high affinity for heparan sulfate proteoglycans seen in tumors because a polylysine modification with a binding domain for heparan sulfate was integrated into the fiber protein (pk7).[74] It was also successful to limit adenoviral replication to particular tissues and tumor types. It was decided to employ the alpha-fetoprotein (AFP) promoter for hepatocellular carcinoma (HCC)[75] and the probasin promoter for prostate tissue in order to drive E1A and E1B, respectively.[76]

2) Ad2xTyr, an oncolytic adenovirus with replacements for the E1A gene promoter and the E4 promoter, was created using a synthetic fusion construct of the core promoter and enhancers of the human tyrosinase. Instead of normal fibroblasts and keratinocytes, Ad2xTyr demonstrated tumor selectivity towards melanoma cells.[77]

3) Telomelysin (OBP-301) is an oncolytic adenovirus in which the human telomerase reverse transcriptase (hTERT) promoter controls both E1A and E1B, which are connected by the internal ribosome entry site (IRES).[78] A single intratumoral injection resulted in a partial response in 56.7% of patients in an early phase I dosage progression study of 16 patients with solid tumors. Only adverse effects of grade 1/2 were found.[79] A phase I clinical research of locoregional administration of OBP-301 as monotherapy in patients with advanced malignancies, such as head and neck cancer or metastatic melanoma, was conducted in the United States to assess the safety of OBP301 in the treatment of cancer.[79] OBP-301 and radiotherapy are believed to work synergistically in both directions, according to a therapeutic strategy used at Okayama University Hospital.[80]

4) pRB interacts with members of the E2F transcription factor family in non-replicating cells to operate as a negative regulator and govern cell cycle progression.[81] An alteration to the adenovirus E1A CR2 in Delta-24 results in a loss of 24 base pairs, which precludes E1A from binding to pRB.[82] Due to its inability to proliferate, this virus cannot release E2F in healthy cells. E2F is no longer negatively controlled by pRB in tumor cells with mutant or dysregulated pRB, and this enables viral gene transcription and hence replication.[83] DNX-2401 (Delta-24-RGD) is the first AdDelta-24 derivative that has undergone clinical testing. has already finished four phases I studies, mostly for the treatment of gliomas. Progressionfree survival of three years was achieved in three of the 25 patients, five of whom lived longer than three years following therapy and three of whom had tumors that shrank dramatically.[84] Forty-nine patients with recurrent glioblastoma participated in a phase II study of DNX-2401 combined with the anti-PD-1 antibody pembrolizumab. The outcomes with the oncolytic adenovirus were positive, with median overall survival of 12.5 months and survival at 18 months of 20.2% compared to the median overall survival of 7.2 months with monotherapies of temozolomide.[85] In a phase I study, ICOVIR-5 (Ad5-E2F-Delta-24-RGD) was given systemically intravenously to patients with melanoma, and it was well tolerated. Twelve individuals did not have tumor shrinkage, but four of them had metastatic skin or liver lesions, demonstrating that ICOVIR-5, when given intravenously, can target and identify metastatic cancer cells.[86]

5) VCN-01 (Ad5-E2F-Delta-24-RGD-PH20) produces hyaluronidase (PH20), which promotes viral intratumoral dissemination.[87] It is now being evaluated in many clinical studies for advanced pancreatic cancer and head and neck squamous cell carcinoma in conjunction with chemotherapy or immune checkpoint inhibitors. Administration of VCN-01 was well tolerated in a retinoblastoma study and showed an anti-tumor effect in retinoblastoma vitreous seeds.[88]

6) The first oncolytic adenovirus used in clinical studies to treat head and neck cancer was ONYX-015 (dl1520).[89] A stop codon and an E1B55K (the viral E1B55K product, which binds and introduces ubiquitination substrates.[90]) deletion characterize ONYX-015, a chimeric adenovirus (Ad5/2) that prevents the translation of the protein. Tumor destruction at the injection site was seen in 5 out of 22 patients, despite the fact that there was no objective response seen. The Oncorine (also named H101, a genetically modified adenovirus) phase I clinical studies were started in China in 2000. Three out of fifteen patients experienced impressive tumor reduction in addition to an acceptable safety profile. In patients with squamous cell carcinoma of the head and neck (SCCHN), Oncorine had a higher positive response rate (79%) when combined with chemotherapy than when chemotherapy was used alone (40%). The State Food and Drug Administration (SFDA) of China authorized it as the first commercially available oncolytic in 2005 on the basis of this research.[91]

7) The first OV produced by this unique approach was enadenotucirev (Colo-Ad1), a complex Ad3/Ad11p hybrid virus.[92] Colo-Ad1, a new adenoviral vector that was specifically chosen to replicate solely in colon cancer cells, was developed by controlled evolution from a pool of several serotypes of species B to F.[93] There was three phases I trials. One of them compared the effectiveness of intratumoral vs intravenous administration on 17 patients with solid tumors. Eleven out of 12 patients who received intravenous infusions and two out of five patients who had intratumoral injections had viral DNA found in tumor samples. No significant adverse effects associated with the therapy were recorded, and both approaches were well tolerated. Patients with rectal cancer who will receive enadenotucirev in combination with radiotherapy and chemotherapy are being sought for two other phases I trial with enadenotucirev that are currently recruiting individuals with colon cancer, head, and neck cancer, or other epithelial tumors for combination therapy with enadenotucirev and nivolumab (PD-1 inhibitor) or individuals with these conditions (capecitabine).[94] NG-350A, which expresses the CD40 antibody, and NG-641, which expresses the bispecific T-cell engager (BiTE), fibroblast activation protein (FAP)/CD3 chemokine ligands nine and 10 (CXCL9 and CXCL10), as well as IFN-α, are two variants of enadenotucirev that are currently being studied in phase I clinical.[73]

Reovirus

The Reoviridae family of viruses, including the nonenveloped, double-stranded RNA virus known as reovirus (RV), has identified hosts in a variety of organisms, including fungi, plants, fish, reptiles, birds, and mammalians.[94,95] The double-stranded RNA is classified into three sizes: large (L1-3), medium (M1-3), and small (S1-3).[96] The filamentous attachment protein, known as σ1, is used by reoviruses to bind to target tissues. All reovirus serotypes sigma 1 protein (σ1) -the reovirus cell attachment protein- interacts with junctional adhesion molecule (JAM)-A, a crucial element of intercellular tight junctions. The kind of carbohydrate that the σ1 protein attaches to on the surface of cells varies by serotype.[97] Reovirus internalization is mediated by beta 1 integrin after binding to JAM-A and carbohydrates, most likely via clathrin-dependent endocytosis. The discharge of viral progeny and RV replication both depend on the Ras (term derived from the “rat sarcoma virus,” which acts as an on/off switch for chemicals that indicate cell proliferation.) signaling system, according to data.[98] Reovirus also activates the Ras/RalGEF (Ras-like (Ral) small GTPases)/p38 pathway, which causes cell death.[99] As a result, Ras-overexpressing tumor cells are the focus of RV exclusively. Reovirus serotypes type one Lang, type two Jones, and type three Abney and Dearing have all been discovered.[100] The most effective oncolytic RNA virus for treating cancer is Reolysin (also known as Pelareorep), serotype 3 RV, which has successfully completed a number of clinical trials as a mono or in combination with other treatments.[101]

Vaccinia virus

The vaccinia virus (VV) is an enclosed virus with double-stranded DNA that belongs to the family Poxviridae’s Orthopoxvirus genus.[102] The 190 kb-long VV genome, which has a diameter of 70 to 100 nm, enables the insertion and strong expression of big foreign genes.[103,104] One of the most popular strategies to improve the selective replication and lytic capabilities of VV is the deletion of viral thymidine kinase (TK), vaccinia type I IFN-α binding protein (B18R), or vaccinia growth factor (VGF).[105] Vaccinia virus demonstrated natural tumor selectivity as an oncolytic drug and the potential for systemic delivery.[106] A Wyeth strain VV-derived OV called JX-594 is equipped with GM-CSF and beta-galactosidase but lacks the TK gene.[107] The selectivity of vaccinia to tumors was markedly improved by the deletion of the viral TK gene.[108]

The prototype poxvirus vaccinia virus, which may cause transitory macropinocytosis, endocytic internalization, and infection, all vitally depend on the presence of exposed phosphatidylserine in the viral membrane, suggesting that vaccinia virus mimics apoptosis to penetrate the host cells.[109]

Studies have shown that JX-594 delivered through intravenous injection constantly promotes infection inside tumors but does not affect healthy tissue.[110,111]. The JX-594 was demonstrated to be well tolerated following intravenous infusion in phase I/II clinical studies and to cause no dose-limiting toxicities; the maximum tolerated dosage was not attained.[110-113] However, a phase III trial involving patients with advanced HCC who had not had prior systemic treatment and JX-594 failed to demonstrate a survival advantage.[114] There are still numerous problems that need to be resolved before JX-594 may be used, such as in conjunction with other immunotherapies.

Newcastle Disease Virus

The Newcastle disease virus (NDV) belongs to the family Paramyxoviridae and is an enclosed virus containing negative-sense single-stranded RNA.[115] Its genome is about 15 kb long and expresses at least eight proteins: nucleocapsid (N), phosphoprotein (P), matrix protein (M), fusion protein (F), hemagglutinin-neuraminidase protein (HN), large polymerase protein (L), and two other proteins, V and W. Its diameter range from 100 to 500.[116]. The HN protein, which engages with sialic acid receptors located on the host cells to attach tumor cells, then fuses with the engaged F protein to join the virus to the host cell membrane. Consequently, the virus’ genome penetrates the cytoplasm of the host.[117,118] The insertion location of foreign genes between P/M is advised since the genomes have a considerable capacity (>5 kb) for gene transfer. Numerous clinical trials have shown that NDV, an OV, has a very excellent safety record for cancer patients and demonstrates considerable antitumor activity.[119]

Measles Virus

The measles virus (MeV) belongs to the genus Morbillivirus in the Paramyxoviridae family and is an enveloped virus containing negative-sense single-stranded RNA. Its genome is approximately 16 kb in length and has six genes that code for eight proteins, including two auxiliary proteins and six anti-genome configurations. Its results of various from 100 to 200 nm (V and C).[120] Three receptors, CD46, the signaling lymphocyte activation molecule (SLAM)/CD150, and poliovirus-receptor-like-4 (PVRL4), are used by MeV to connect with host cells.[121] Measles virus is inherently selective for infecting tumor cells since SLAM/CD150 is often overexpressed on many hematological malignancies whereas CD46 is constitutively overexpressed on many tumor cells.[122] However, CD46 is not a tumor-selective receptor because it is also expressed basally in normal cells.[121] MeV is a viable OV option due to its good potency, which includes the lack of dose-limiting toxicities and spontaneous oncotropism.[123]

EFFECTS OF ONCOLYTIC VIRUSES ON ANTITUMOR MECHANISMS

The oncolytic viruses that are now being used in therapy, as mentioned above and shown in Figure 1, naturally prefer cell surface proteins that are expressed abnormally in cancer cells. After connecting and infiltrating tumor cells (some viruses in order to promote virus entrance or infection, exposed phosphatidylserine on the viral surface interacts either wholly or partly with phosphatidylserine receptors,[124] OVs can use a variety of lytic mechanisms, some of which may or may not be connected to the actual level of viral replication inside the target cells, to destroy the infected cancer cells.

Figure 1. Cell surface receptors, which are typically overexpressed on cancer cells, are just one of the entry points that oncolytic viruses employ to infiltrate host cells. Some viruses enter cells by endocytosis, which is facilitated by cell fusion and syncytia forming. Through phosphatidylserine acquisition and incorporation into the viral membrane, a virus mimics apoptosis. (CAR; coxsackievirus-adenovirus receptor, HVEM; herpesvirus entry mediator, JAM-A; junctional adhesion molecule-A, PVRL4; poliovirus-receptor-like-4, SLAM; signaling lymphocytic activation molecule, AXL; phosphatidylserine receptor.)

The precise processes of viral oncolysis are still poorly known, vary greatly amongst viruses, and can even vary significantly among various target cancer cell types.[125] Multiple pathways are considered to be involved in how OVs mediate anticancer activity:

(a) specific viral replication inside cancer cells that results in primary cytolytic effects (a process also referred to as oncolysis)[126-128];

(b) indirect cell death (e.g., apoptosis-like vs. necrosis-like) impacts on both healthy and infected cancer cells, as well as related endothelial cells in the tumor-associated vasculature, which result in decreased angiogenesis[129];

(c) the infiltration of immune cells that have been triggered into the tumor microenvironment (TME).[130,131]

However, the way in which the OV, TME, and host immune system act overall, the form and kind of cancer cells and these processes vary greatly from virus to virus. The majority of viruses interfere with the mechanisms that the host activates to cause cell death after viral infection. Virus-encoded peptides are sometimes known to target various cell death processes as stimulants or inhibitors.[132,133]

Immunogenic cell death (ICD) is commonly used to characterize cancer cell death that can reveal cancer cell antigens to resident immune cells in the TME and is generally evaluated in cultured cells by extracellular release of normally intracellular signals or cell release of intracellular agents. Oncolytic viruses have the benefit of being able to activate multi-mechanistic cell death cascades inside the tumor site. Immunogenic cell death is thought to be important in promoting innate anti-tumor immunity.[134,135]

The discharge of tumor-associated antigens (TAAs), damage-associated molecular patterns (DAMPs) such as ATP, high mobility group box 1 protein (HMGB1), heat shock protein (HSP), ecto-calreticulin and proinflammatory cytokines, OV-derived pathogen-associated molecular patterns (PAMPs), and increased expression of numerous inflammatory cytokines occur when the copying of OVs in cancer cells provokes ICD. These events then activate both innate and adaptive immune reactions. These PAMPs and DAMPs are detected by pattern recognition receptors (PRRs) on immune cells, including stimulator of IFN genes (STING), toll-like receptor (TLR) adaptor molecule 1, and TLR3,[136,137] generating a proinflammatory milieu by promoting the expression of proinflammatory cytokines, such as type I IFNs, IL-1, IL-6, IL-12, TNF-α, GM-CSF, and chemokines, such as CCL2, CCL3, CCL5, and CXCL10, which causes immunologically “cool” tumors to turn into “hot” tumors.[138]

First, chemokines that are locally released, such as CCL3 also known as macrophage inflammatory protein 1-alpha (MIP-1α) and CXCL10, attract the first cell mediators, including neutrophils and macrophages, to the site of infection.[139] These cytokines are also implicated in the generation of efficient antitumor reactions.[140]

The effects of OVs on tumor cells are illustrated in Figure 2 below.

Figure 2. The mechanism that oncolytic viruses function in cancer cells. When OVs infect normal, non-cancerous cells, they are unable to proliferate, leaving the cells undamaged. The viruses may successfully reproduce once they enter cancer cells, producing additional viral products and eventually inducing immunogenic cell death (ICD). After cell lysis, the tumor microenvironment is exposed to the viral products, pathogen-associated molecular patterns (PAMP), damage-associated molecular patterns (DAMP), heat shock protein (HSP), (adenosine triphosphate) ATP, and tumor-associated antigens (TAA), tumor microenvironment (TME). The virus transmission is continued by the discharged virus product, which further infects the functional tumor cells. Immune cells are drawn to the TME by immunogenic molecules delivered there.

OVERCOMING PATHOGENICITY: ANIMAL VIRUSES IN HUMAN THERAPY

It was once thought that a non-human animal virus would preserve oncolytic activity even in a host not typically sensitive to that specific virus in an effort to manage virulence and avoid the issue of fast virus elimination caused by or before antiviral immunity. Moore’s[141] early research using the human disease Russian Far East encephalitis virus, which showed efficacy against a mouse tumor, supported this notion. A panel of human cancer cell lines was used in early work to carry out a high-throughput search for non-human animal viruses with oncolytic activity. In this instance, adaptation through in vitro transmission was still seen to be favorable since the original strain was either non-pathogenic or non-infectious to people. Therefore, it was assumed that the viruses would not acquire any extra cell tropism in the lack of normal cells beyond that for which they were already equipped.[142]

Twenty-seven non-human virus species were identified that are in (pre) clinical development, mainly as oncolytic agents.[143] In a thorough examination of the six viruses, Yohn et al.[144] assessed the oncolytic potential by determining if the viruses could prevent the growth of heterotransplanted human cancers or cause the tumors that had already grown to necrose and return. Two of these herpes viruses-equine rhinopneumonitis and infectious bovine rhinotracheitis- which are not pathogenic to humans have been found to be oncolytic for one or perhaps more human cancers.

After the relatively underwhelming clinical results of a virus known as the “MP” virus (after the authors Molomut and Padnos), which is now known to be a strain of lymphocytic choriomeningitis virus, arenaviruses have not been widely used as oncolytic. The MP virus, as is typical for virotherapy, caused substantial tumor regressions in rat models and, in some cases, increased survival by more than 60% compared to controls[144]; however, it had a little therapeutic effect in human trials and failed to extend survival.[145]

A non-human virus may develop changes that might boost its pathogenicity in a host that is not typically vulnerable, but these adaptations have not received nearly as much notice as viral changes that are useful for targeting. Nowadays, with the effect of the coronavirus disease 2019 pandemic, it would be regarded as highly perilous to introduce wild-type viruses into a typically gullible host whose populations have not developed any viral resistance. In fact, the feline panleukopenia virus, which was employed in virotherapy, developed on its own to be transmissible to dogs, leading to the pandemic canine parvovirus that is thought to have infected more than 80% of wild and domestic dogs between 1978 and 1979 worldwide.[146]

In conclusion, cancer immunotherapy is a sort of cancer treatment that activates our own immune system to fight cancer. Oncolytic viral treatment is one of the most popular forms of cancer immunotherapy. The majority of cancer cells lack the typical antiviral defense systems, making them prone to viral infections. Cancer cells are modified healthy cells. A modified virus is administered to patients during oncolytic viral treatment, allowing the virus to infect cancer cells. These modified viruses move to the tumor side and create substances that draw nearby immune cells, and they are specifically instructed not to infect healthy cells since their capacity to infect cells has been reduced. The viruses can cause infected cancer cells to explode, releasing more of the previously hidden cancer antigens to the surrounding area and drawing additional immune cells to destroy the surviving cancer cells. The fact that humans lack the same protection as the viral reservoir host makes new infections so hazardous. And since there are so many, it’s presently impossible to forecast when or which particular viruses will spread, but we do know the circumstances under which it may happen. More information on how to stop the non-human virus from spreading conditions would help us to establish a greater degree of accuracy on this matter. Further work needs to be done to identify realistic methods that simplify application while obtaining tolerable risk levels, a list might be employed. To safeguard mankind against potential virus-induced pandemics, it will be required to establish such methods and identify solutions that support research that might provide oncolytic viral treatment.

Cite this article as: Nesil P, Pestil Z, Erbaş O. How Can a Virus Infection Treat Cancer? Relevance to Non-Human Viruses and the Use of Oncolytic Viruses. JEB Med Sci 2022;3(2):158-172.

Conflict of Interest

The authors declared no conflicts of interest with respect to the authorship and/or publication of this article.

Financial Disclosure

The authors received no financial support for the research and/or authorship of this article.

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