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Frontiers of Medicine

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Front. Med.    2020, Vol. 14 Issue (2) : 160-184    https://doi.org/10.1007/s11684-020-0750-4
REVIEW
Development of oncolytic virotherapy: from genetic modification to combination therapy
Qiaoshuai Lan1, Shuai Xia1, Qian Wang1, Wei Xu1, Haiyan Huang2, Shibo Jiang1,3(), Lu Lu1()
1. Key Laboratory of Medical Molecular Virology (MOE/NHC/CAMS), School of Basic Medical Sciences and Shanghai Public Health Clinical Center, Fudan University, Shanghai 200032, China
2. Yantai Yuhuangding Hospital, Qingdao University, Yantai 264000, China
3. Lindsley F. Kimball Research Institute, New York Blood Center, New York, NY 10065, USA
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Abstract

Oncolytic virotherapy (OVT) is a novel form of immunotherapy using natural or genetically modified viruses to selectively replicate in and kill malignant cells. Many genetically modified oncolytic viruses (OVs) with enhanced tumor targeting, antitumor efficacy, and safety have been generated, and some of which have been assessed in clinical trials. Combining OVT with other immunotherapies can remarkably enhance the antitumor efficacy. In this work, we review the use of wild-type viruses in OVT and the strategies for OV genetic modification. We also review and discuss the combinations of OVT with other immunotherapies.
Keywords immunotherapy      oncolytic virus      genetic modification      immune checkpoint blockade      chimeric antigen receptor T cell     
Corresponding Author(s): Shibo Jiang,Lu Lu   
Just Accepted Date: 11 February 2020   Online First Date: 09 March 2020    Issue Date: 09 May 2020
 Cite this article:   
Qiaoshuai Lan,Shuai Xia,Qian Wang, et al. Development of oncolytic virotherapy: from genetic modification to combination therapy[J]. Front. Med., 2020, 14(2): 160-184.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-020-0750-4
https://academic.hep.com.cn/fmd/EN/Y2020/V14/I2/160
Fig.1  Schematic of some oncolytic viruses for cancer treatment. Many viruses, including double-stranded DNA viruses, such as AdV, herpes simplex virus (HSV), and VACV; single-stranded DNA viruses, such as parvovirus; negative-sense single-stranded RNA viruses, such as Newcastle disease virus (NDV), measles virus (MV), and vesicular stomatitis virus (VSV); positive-sense single-stranded RNA viruses, such as poliovirus and coxsackievirus; and double-stranded RNA viruses, such as reovirus, have been used in cancer treatment. The terms naked/enveloped are used to describe types of virus; high/moderate/low describes the genomic capacities of OVs.
Virus type Virus Family Natural host Receptor Replication site Common used virus strain or type References
DNA virus Adenovirus Adenoviridae Human CAR, integrin Nucleus, cytoplasm Ad5 [22]
Vaccinia virus Poxviridae Human Unknown Cytoplasm Lister, Wyeth, WR [23]
Herpesvirus Herpesviridae Human HVEM, nectin Nucleus, cytoplasm HSV-1 [24]
Parvovirus Parvoviridae Rat SARs Nucleus, cytoplasm H1-PV [25]
RNA virus Measles virus Paramyxoviridae Human CD46, SLAM Cytoplasm Edmonston vaccine strain [26]
Newcastle disease virus Paramyxoviridae Chicken Unknown Cytoplasm HUJ, MTH-68/H [27]
Vesicular stomatitis virus Rhabdoviridae Pigs, cattle, horses LDLR Cytoplasm Recombinant Indiana strain [28]
Poliovirus Picornaviridae Human CD155 Cytoplasm Sabin vaccine strain [29]
Coxsackievirus Picornaviridae Human ICAM-1, DAF Cytoplasm CVA21, CVB3 [30]
Reovirus Reoviridae Human Unknown Cytoplasm Reovirus-serotype 3 [31]
Tab.1  Characteristics of DNA virus- and RNA virus-derived OVs
Fig.2  Genetic modifications of OVs. (A) Genetic modifications for improving tumor targeting of OVs. Entry targeting: serotype switching and insertion of a tumor-targeting peptide, glycoproteins from other viruses, and single-chain antibodies (scAb) targeting tumor-associated antigens can allow OVs to target tumor surface molecules and enter tumor cells. Post-entry targeting: insertion of tumor-specific promotors can promote virus replication in tumor cells, while insertion of miRNA target sequences can restrict virus replication in normal cells. (B) Genetic modifications that enhance OV safety. Deletion of virulence genes can reduce the risk of OV infections of normal cells and enhance safety. (C) Genetic modifications to augment the antitumor efficacy of OVs. Antitumor efficacy can be augmented by inserting foreign genes, such as genes encoding immunostimulatory molecules/cytokines, suicide genes (pro-apoptotic proteins and prodrug-activating enzymes), extracellular matrix (ECM)-degrading enzymes, and anti-vasculature molecules. (D) Genetic modifications to monitor OV replication. Reporter genes, such as green fluorescent protein (GFP), Renilla luciferase (Rluc), sodium–iodide symporter (NIS), and human norepinephrine transporter (NET), can be inserted to monitor OV replication.
Virus Name of OVs Genetic modification Conditions Phase NCT Number Status References
HSV T-VEC ICP34.5 and ICP47 deletion; GM-CSF insertion Advanced melanoma Phase 1 NCT03747744 Recruiting [170–172]
Breast cancer Phase 1/2 NCT02779855 Recruiting
Melanoma Phase 2 NCT00289016 Completed
Melanoma Phase 3 NCT01368276 Completed
Melanoma Phase 3 NCT00769704 Completed; DRR: 36.1% (T-VEC-treated patients) versus 3.8% (GM-CSF treated patients)
HSV-1716 ICP34.5 deletion Glioma Phase 1 NCT02031965 Terminated
Rhabdomyosarcoma
Osteosarcoma		 Phase 1 NCT00931931 Completed
G207 ICP34.5 deletion; UL39 disruption Glioma Phase 1/2 NCT00028158 Completed
Brain tumors Phase 1 NCT03911388 Not yet recruiting
Malignant glioma Phase 1 NCT02457845 Recruiting
M032 ICP34.5 deletion; IL12 insertion Glioblastoma multiforme Phase 1 NCT02062827 Recruiting
HF10 HSV-HF strain Melanoma Phase 2 NCT03259425 Active, not recruiting [173]
Solid tumors with superficial lesions Phase 1 NCT02428036 Completed
Pancreatic cancer Phase 1 NCT03252808 Active, not recruiting
Melanoma Phase 2 NCT03153085 Completed
AdV LOAd703 CD40L and 4-1BBL insertion; ?24 in E1A Pancreatic adenocarcinoma Phase 1/2 NCT03225989 Recruiting [11,156,174]
Pancreatic cancer Phase 1/2 NCT02705196 Recruiting
VCN-01 Hyaluronidase and RGD insertion; ?24 in E1A Metastatic solid tumor Phase 1 NCT02045602 Active, not recruiting
Pancreatic adenocarcinoma Phase 1 NCT02045589 Completed
Retinoblastoma Phase 1 NCT03284268 Recruiting
DNX-2401
(Delta-24-RGD)		 RGD insertion; ?24 in E1A Glioblastoma Phase 1 NCT03896568 Recruiting
Brain stem glioma Phase 1 NCT03178032 Recruiting
Brain cancer Phase 1 NCT00805376 Completed; 20% of patients survived>3 years
CG0070 GM-CSF insertion; E3 deletion Bladder cancer Phase 2 NCT02143804 Withdrawn
Bladder cancer Phase 2 NCT02365818 Completed; overall 47% CR rate at 6 months for all patients and 50% for patients with CIS
ONCOS-102 (CGTG-102) Type 3 knob and GM-CSF insertion; ?24 in E1A Malignant solid tumor Phase 1 NCT01598129 Completed
Advanced or unresectable melanoma progressing after PD1 blockade Phase 1 NCT03003676 Recruiting
OBP-301 hTERT promoter insertion Hepatocellular carcinoma Phase 1 NCT02293850 Recruiting [175]
Melanoma Phase 2 NCT03190824 Active, not recruiting
Esophagogastric adenocarcinoma Phase 2 NCT03921021 Recruiting
Esophageal cancer Phase 1 NCT03213054 Recruiting
VACV JX-594
(Pexa-Vec)		 TK deletion; GM-CSF insertion Melanoma Phase 1/2 NCT00429312 Completed [111,148,176,177]
Ovarian cancer Phase 2 NCT02017678 Withdrawn
Melanoma Phase 1 NCT00625456 Completed
Renal cell carcinoma Phase 1 NCT03294083 Recruiting
Colorectal cancer Phase 1/2 NCT03206073 Recruiting
Hepatocellular carcinoma Phase 2 NCT00554372 Completed; intrahepatic mRECIST
Disease control rate at week 8 was 46% overall
GL-ONC1 Ruc-GFP, b-glucuronidase, and b-galactosidase insertion
TK and haemagglutinin disruption		 Solid organ cancers Phase 1 NCT02714374 Active, not recruiting
Peritoneal carcinomatosis Phase 1/2 NCT01443260 Completed; efficient intraperitoneal infection in eight patients (8/9)
Cancer of head and neck Phase 1 NCT01584284 Completed; combinations of GL-ONC1 with radiotherapy and chemotherapy: 1-year (2-year) PFS and OS were 74.4% (64.1%) and 84.6% (69.2%), respectively
Advanced cancers (solid tumors) Phase 1 NCT00794131 Completed
TG6002 FCU1 insertion; J2R and I4L deletion Glioblastoma Phase 1/2 NCT03294486 Recruiting
Colon cancer Phase 1/2 NCT03724071 Recruiting
MV MV-NIS NIS insertion Multiple myeloma Phase 2 NCT02192775 Recruiting [169]
Malignant ovarian tumor Phase 2 NCT02364713 Recruiting
MV-CEA CEA insertion Glioblastoma Phase 1 NCT00390299 Active, not recruiting
Ovarian epithelial cancer or primary peritoneal cancer Phase 1 NCT00408590 Completed
VSV VSV-IFNb-NIS IFNb and NIS insertion Malignant solid tumor Phase 1 NCT02923466 Recruiting [178]
Hepatocellular carcinoma Phase 1 NCT03647163 Recruiting
Poliovirus PVSRIPO Replace IRES of poliovirus with IRES from HRV2 Malignant glioma Phase 1 NCT03043391 Recruiting [179,180]
Glioblastoma Phase 1 NCT01491893 Active, not recruiting; OS among the patients who received PVSRIPO reached a plateau of 21% (95% confidence interval, 11 to 33) at 24 months
Malignant glioma Phase 2 NCT02986178 Recruiting
Melanoma Phase 1 NCT03712358 Recruiting
Maraba virus MG1- MAGEA3 MAGEA3 insertion Metastatic melanoma Phase 1 NCT03773744 Not yet recruiting [181]
Non-small cell lung cancer Phase 1/2 NCT02879760 Active, not recruiting
MG1-E6E7 E6, E7 antigens insertion HPV-associated cancers Phase 1 NCT03618953 Active, not recruiting
Coxsackievirus CAVATAK® None (wild type) Uveal melanoma with liver metastases Phase 1 NCT03408587 Completed [30]
Malignant melanoma Phase 2 NCT01227551 Completed
Reovirus Pelareorep (Reolysin®) None (Wild type) Malignant glioma Phase 1 NCT00528684 Completed [182]
Osteosarcoma Phase 2 NCT00503295 Completed
Bladder carcinoma Phase 1 NCT02723838 Withdrawn
Pancreatic adenocarcinoma Phase 1 NCT02620423 Completed
Pancreatic adenocarcinoma Phase 2 NCT01280058 Completed; PFS: 4.9 months (paclitaxel/carboplatin+ pelareorep) versus 5.2 months (paclitaxel/carboplatin)
Head and neck cancers Phase 3 NCT01166542 Completed
Parvovirus H-1 ParvOryx None (Wild type) Glioblastoma multiforme Phase 1/2 NCT01301430 Completed; H-1PV treatment was safe and can extend median survival [183,184]
Pancreatic cancer Phase 1/2 NCT02653313 Completed
NDV NDV None (Wild type) Glioblastoma Phase 1/2 NCT01174537 Withdrawn [20,185]
Metastatic cancer Phase 2 NCT00348842 Withdrawn
Tab.2  Oncolytic viruses in clinical trials
Fig.3  Combinations of oncolytic viruses with immune checkpoint inhibitors and CAR-T cell therapy. (A) Mechanisms of OVs combined with ICIs targeting the programmed cell death protein 1 (PD-1)/programmed cell death 1 ligand 1 (PD-L1) pathway. OVs can attract CD8 T cells and NK cells into the TME. The expression of PD-L1 on tumor cells is upregulated by OV infection. Anti-PD-1/PD-L1 antibodies block the PD-1/PD-L1 pathway and stop the immune inhibitory signal. (B) OVs in combination with CAR-T cells in the treatment of solid tumors. Modified OVs can express cytokines that attract CAR-T cells into the TME and enhance their antitumor activities; BiTE-armed OVs express BiTEs that bridge CAR-T cells with tumor cells to prevent the immune evasion of tumor cells; OVs armed with anti-PD1/PD-L1 mini-antibody (mini-body) express anti-PD-1/PD-L1 mini-body blocking the immune inhibitory signal and enhancing the antitumor efficacy of CAR-T cells.
Oncolytic virus Transgene ICB/ CAR-T cell Tumors/tumor cells Therapeutic outcomes References
Combinations with ICB in preclinical studies
vvDD-CXCL11 (VACV) CXCL11 Anti-PD-L1 MC38 colon and ID8 ovarian tumor models Combination therapy: more than 40% cures in models of colon and ovarian cancers [194]
HSV1716 (HSV-1) None Anti-PD-1 RMS model Combination therapy significantly prolongs survival of mice bearing M3-9-M tumors [195]
MV-EGFR, MV-NIS (MV) EGFR-scAb Anti-PD-1 GL261 glioma cell Combination therapy: 60% of mice remained alive for at least 120 days [196]
Reolysin® (Reovirus) None Anti-PD-1 Brain tumor
GL261 glioma cell		 Combination therapy improves survival [7]
VSV-mIFNb-NIS (VSV) mIFNb, NIS Anti-PD-L1 AML Combination therapy significantly improves the survival of mice with AML [197]
MG1 (Maraba virus) None Anti-PD-1 Human TNBC cell lines, murine mammary carcinoma Combination therapy significantly slows tumor growth in the 4T1 model [10]
NDV-Fluc (NDV) Fluc Anti-CTLA-4 MC38 colon carcinoma B16-F10 melanoma More than 80% protection against tumor re-challenge (combination therapy) vs. 40% (anti-CTLA-4 alone) [9]
G47?-mIL12 (HSV-1) IL-12 Anti-CTLA-4 and anti-PD-1 Glioma model (CT-2A, 005 GSCs) Median survival: 66.5 days (triple combination therapy) versus 20 days (mock-treated group) [198]
WR (VACV) None Anti-PD1 or anti-CTLA4 MCA205 tumor Combination therapy increased survival in MCA205 sarcoma model [199]
Combinations with ICB in clinical trials
T-VEC (HSV-1) GM-CSF Pembrolizumab Advanced melanoma Overall response rate 62%, complete response rate 33% [200]
T-VEC (HSV-1) GM-CSF Pembrolizumab, ipilimumab/nivolumab, or nivolumab Unresectable stage III–IV melanoma Overall response rate for on-target lesions: 90% (9/10) [201]
T-VEC (HSV-1) GM-CSF Ipilimumab Unresectable stage IIIB–IV melanoma Objective response rate: 50% [202]
T-VEC (HSV-1) GM-CSF Ipilimumab Advanced melanoma Objective response rate: 39% (combination therapy) versus 18% (ipilimumab alone) [203]
Combinations with CAR T cell therapies
OAd-BiTE (Adenovirus) EGFR-targeting-BiTE CAR-T cell targeting the FR-a Solid tumors (SKOV3, HCT116, and Panc-1 cell) Median survival: all animals survived until the experimental endpoint of 41 days (CAR-T cells and OAd-BiTE) versus 20 days (OAd-BiTE alone) or 38 days (CAR-T cells alone) [204]
OAd-TNFa-IL2 (Adenovirus) TNF-a and IL-2 Mesothelin-redirected CAR-T cell Pancreatic cancer (BxPC-3, Capan-2, and AsPC-1 cell line, AsPC-1 tumor xenograft model) Combination therapy efficiently inhibits tumor growth [205]
Ad5D24/Ad5D24.RANTES.IL15 (Adenovirus) RANTES and IL-15 GD2.CAR-T cell Neuroblastoma cell tumor model Survival rate: 73% (GD2.CAR-T cells and Ad5D24.RANTES.IL15) vs. 44% (GD2.CAR-T cells and Ad5D24) at day 45 [206]
CAd12_PDL1 (Adenovirus) PD-L1-antibody, IL-12p70 HER2.CAR-T cell HNSCC xenograft model Median survival: more than 100 days (CAd12_PDL-1+ CAR-T) vs. 21 or 24 days (control group) [207]
CAd-VECPDL1 (Adenovirus) PD-L1mini-body HER2.CAR-T cell Solid tumor cell lines (PC-3, A549, HepG2) Median survival: 110 days (twofold longer than mice treated with a single agent) [208]
Tab.3  Oncolytic viruses combined with immune checkpoint inhibitors and CAR-T cell therapies
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