Oncolytic Virotherapy in Glioma Tumors
Abstract
:1. Introduction
2. DNA Viruses Proposed as Glioma Oncolytic Agents
2.1. Herpes Simplex Virus Type I
2.1.1. Herpes Simplex Virus-1 Pre-Clinical Research
2.1.2. Herpes Simplex Virus-1 Clinical Studies
2.2. Adenovirus
2.2.1. Adenovirus Pre-Clinical Research
2.2.2. Adenovirus Clinical Studies
2.3. Vaccinia Virus (VV)
2.3.1. Vaccinia Virus Pre-Clinical Research
2.3.2. VV Clinical Studies
2.4. Myxoma
Myxoma Virus Pre-Clinical Research
2.5. Parvovirus
2.5.1. Parvoviridae Pre-Clinical Research
2.5.2. Parvoviridae Clinical Studies
3. RNA Viruses Proposed as Glioma Oncolytic Agents
3.1. Reovirus
3.1.1. Reovirus Pre-Clinical Research
3.1.2. Reovirus Clinical Studies
3.2. Measles
3.2.1. Measles Pre-Clinical Research
3.2.2. Measles Clinical Studies
3.3. Vesicular Stomatitis
Vesicular Stomatitis Virus Pre-Clinical Research
3.4. Newcastle Disease Virus (NDV)
3.4.1. Newcastle Disease Virus Pre-Clinical Research
3.4.2. Newcastle Disease Virus Clinical Studies
3.5. Seneca Valley
Seneca Valley Virus Pre-Clinical Research
3.6. Poliovirus
3.6.1. Poliovirus Pre-Clinical Research
3.6.2. Poliovirus Clinical Studies
3.7. Sindbis
Sindbis Pre-Clinical Research
3.8. Rift Valley Fever Virus (RVFV)
4. Current OV Challenges for Malignant Glioma
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
WHO | World Health Organization |
TMZ | Temozolomide |
DNA | Deoxyribonucleic acid |
RNA | Ribonucleic acid |
GBM | Glioblastoma |
OV | Oncolytic virotherapy |
CNS | Central nervous system |
DAMPs | Danger-Associated molecular patterns |
OS | Overall survival |
ICD | Immunogenic cell death |
PRRs | Pattern recognition receptors |
HSV-1 | Herpes simplex virus type 1 |
LAMR | Laminin receptor |
VV | Vaccinia virus |
MYXV | Myxoma virus |
NDV | Newcastle disease virus |
TVEC | Talimogene laherparepvec |
TTFields | Tumor treating fields |
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Virus | Modifications | Cell Lines | In Vivo Models | Results |
---|---|---|---|---|
Herpes | dlsptk: TK deletion. | Human: U87 and T98G [22] | U87 i.c. and s.c. nude mice | Tumor cell infection and death. In vivo tumor reduction and increased surveillance. |
HSV-1716: γ134.5 loci partial deletion. | Human: U87, T98G, SB18, U373 and U251 [24] | - | Tumor cell infection and death. | |
G207: γ134.5 loci deletion. ICP6 truncation. | Human: U87, U373, U138 and T98G [26] | U87 i.c. and s.c. nude mice, i.c. owl monkeys | Elimination of tumor cells, necrosis and no toxicity. | |
rQNestin34.5: ICP6 deletion. γ134.5 expression under Nestin promoter. | Human: U251, U87dEGFR, T98G, Gli36d5, U138, and MGH238 [28] | U87dEGFR i.c. and s.c. nude mice | Increase of oncolytic activity at in vitro and in vivo models | |
NG34: γ134.5 loci deletion. ICP6 deletion. GADD34 expression under Nestin promoter. | Human: U251, U87ΔEGFR and primary glioma cells Murine: GL261 [30] | U87ΔEGRF-RliFluc and G35 i.c. nude mice, BALB/c mice | Similar oncolytic activity as rQNestin34.5 with lower neurotoxicity. | |
NG34scFvPD-1: γ134.5 loci deletion. ICP6 deletion. GADD34 expression under Nestin promoter. scFvPD-1 expression under CMV’s IE promoter. | Human: U87ΔEGFR and U251 Murine: GL261N4 and CT2A [31] | GL261N4 and CT2A i.c. C57Bl/6J mice, GL261N4 and U87ΔEGFR i.c. nude mice | Increased oncolytic activity in comparison to NG34 in immunocompetent mice. Development of specific immunity and memory. | |
G47Δ: γ134.5 loci deletion. ICP6 truncation. α47 deletion. US11 expression under α47 promoter. | Human: U87 and U373 [34] | U87 s.c. in nude mice | Increased survival, higher number of cured mice than G207. | |
C134: γ134.5 loci deletion. HCMV’s IRS1 protein expression. | Human: D54, U87 and U251 Murine: N2A [32] | U87 i.c. in SCID mice | Reduced tumor volume and increased surveillance. | |
Human and murine: 12 established GBM [33] | N2A orthotopic in A/J and BALB/c mice | Improved replication and longer survival in vivo | ||
HSV-1 R-LM113: insertion of scFvHER2 in gD protein. | Murine: established GBM [35] | PDGFB/DsRed-induced gliomas in nude mice | No toxicity in nude mice and oncolytic effect in HER2 overexpressing and established tumors in vivo. | |
RAMBO: γ134.5 loci deletion. ICP6 truncation. Vstat120 expression under IE4/5 HSV promoter. | Human: U343, U87, U87ΔEGFR, LN229, Gli36ΔEGFR-H2B-RFP, U251-T2, U87ΔEGFR-Luc [36] | U87ΔEGFR-Luc and Gli36ΔEGFR-H2B-RFP i.c. and U87ΔEGFR-Luc s.c. nude mice | Increased survival in vivo and inhibition of tumor vascularization. | |
M002: γ134.5 loci deletion. IL-12 expression. | Murine: 4C8 [37] | 4C8 i.c. gliomas in B6D2F1 mice | Increase mice survival, infiltration of CD4+, CD8+ and NK cells. Longer viral persistence in tumors | |
HSV-IL4: γ134.5 loci deletion. IL-4 expression. | Human: U251 and D54 [21] | GL-261 i.c. in C57BL/6 | Infiltration of macrophages, CD4+ and CD8+. Longer survival. | |
Adenovirus | ONIX-15: E1B-55kD deletion. | Human: 4 primary GBM [49] | S.c. xenograft in nude mice | Tumor regression. |
Delta-24-RGD: E1A partial deletion. RGD tripeptide incorporation. | Human: U251, U373, U87 and D54 [53] | D54 s.c. in nude mice | Cell death with low doses, single injection inhibits tumor growth, several injections resulted in 36% of animals with tumor regression. | |
ICOVIR-5: E1A expression under E2F-1 promoter. E1A partial deletion. RGD tripeptide incorporation. | Human: U251 and U87 [54] | U87 i.c. xenograft in nude mice | Tumor cytotoxic effect in vitro high tumor selectivity and increase of survival in vivo. | |
Adenovirus | ICOVIR-17: E1A expression under a promoter including four palindromic E2F-1 sites and a Sp-1-binding site. E1A partial deletion. RGD tripeptide incorporation. PH20 expression under MLP promoter. | Human: U87, U138, LN308, Gli36, U373, LN229 and 6 primary GBM [60] | U87 and CSCs i.c. in nude mice | Better distribution in HA tumors. Longer mice survival. |
VCN-01: E1A expression under a promoter including four palindromic E2F-1 sites and a Sp-1-binding site. E1A partial deletion. RGD relocated in fiver shaft protein. PH20 expression under MLP promoter. | Human: U87, A172, T98G, U251, U373, SNB19 and 2 GBM CSC [61] | U87 and GBM CSC i.c. xenografts in nude mice | Control of tumor growth One single injection improves survival in aggressive infiltrative tumor. | |
Delta-24-RGDOX: E1A partial deletion. RGD tripeptide incorporation. OX40L expression. | Human: U87 Murine: GL261 [62] | GL261 i.c. in C57BL/6 mice | Proliferation of tumor specific T cells. Sinergy with anti PD-L1. | |
Delta-24-GREAT: E1A partial deletion. RGD tripeptide incorporation. GITRL expression. | Human: U87 and U251 Murine: GL261 [63] | GL261 i.c. in C57BL/6 mice | Extended survival and development of antiviral and antitumor specific response and memory. | |
Ad-RTS-IL-12: No replicative. Expression of IL-12 under RTS® system with veledimex as a co-treatment. | Murine: GL261 [64] | GL261 i.c. in C57BL/6 mice | Tumor infiltration with CD8, extended survival and immune memory development. | |
Vaccinia | rVV-p53: p53 expression. | Rat: C6 [69] | C6 s.c. in nude mice | Moderate cell apoptosis. Tumor growth control. |
rVV-mIL12/mIL2: IL12 expression. IL2 expression. | Rat: C6 [71] | C6 s.c. in nude mice | Cytokine toxicity at high dose Antitumor NK dependent effect. | |
rVV-p53 and rVV-mL12: p53 expression. IL12 expression. | Rat: C6 [74] | C6 s.c. in nude mice | Better tumor growth control. Higher NK and macrophage infiltration. | |
vvDD: TK deletion. VGF deletion. | Human: A172, U87MG and U118 Rat: RG2, F98 and C6 [73] | U87, U118 and C6 s.c. and RG2, F98 i.c. in nude mice | Control of tumor growth. Sinergy with rapamycin or cyclophosphamide. | |
Rhesus macaques [75] | No adverse effects. | |||
vvDD-IL15Rα: TK deletion. VGF deletion. IL15Rα expression. | Murine: GL261 [75] | GL261 i.c. in C57BL/6J | Increase of NK and CD8+ in tumor. Prolonged survival. | |
TG6002: TK deletion. ribonucleotide reductase genes deletion. FCU1 expression. | Human: U87 and patient derived GBM [76] | U87 i.c. and s.c. in nude mice | Prolonged survival in s.c. and i.c. Synergic effect with 5FC in i.c. model. | |
Myxoma | MYXV WT | Human: U87, U251, U373, U343, A172 and U118 Rat: RG2 and 9L [79] | U87 and U251 i.c. in nude mice | Regression and longer survival in both models. |
Human: U87, U251, and U118 [80] | U87 orthotopic in CB-17 SCID mice | Inhibition of MHC-I tumor expression and promotes NK mediated death. | ||
Human: U118 and 3 patient samples Murine: GL261 Rat: T9 [81] | - | SOC co-treatment increases results of MYXV. | ||
MYXV WT: administered in ADSCs | Human: U87 and U251 [82] | U87 orthotopic in nude mice | Increase the tumor infection rate | |
MYXV-M011L-KO: M11L deletion | Human: Brain tumor initiating cells (BTIC) [80] | mBITCs i.c. in C57Bl/6J mice | Prolonged survival. TMZ increases oncolysis | |
Parvovirus | Human: U87 Rat: RG-2 [89] | U87 i-deficient rats and RG-2 i-competent | Complete remission of the tumors | |
H-1PV WT | Human: U373, U138 and 5 CSCs [87] Human: U87 Rat: RG-2 [89] | RGD orthotopic ratsU87 i-deficient rats and RG-2 i-competent | Cathepsin B activation induces cell death in H-1PVComplete remission of the tumors | |
Human: U87, U373, U118, MO59J and A172 Murine: GL261 [90] Human: U373, U138 and 5 CSCs [87] | U87 and U373 s.c. U87 orthotopic CB17-SCID miceRGD orthotopic rats | Selective infection, no toxicity, reduce tumor volume in vivo Cathepsin B activation induces cell death in H-1PV | ||
MVMp WT | Human: U373, U87, SW1088, SK-N-SH Rat: C6 [91] Human: U87, U373, U118, MO59J and A172 Murine: GL261 [90] | -U87 and U373 s.c. U87 orthotopic CB17-SCID mice | MVM p strain cytotoxic only in U373 and C6 (MVM) selective infection, no toxicity, reduce tumor volume in vivo | |
Human: U87 and MO59J [92] Human: U373, U87, SW1088, SK-N-SH Rat: C6 [91] | - | Selective infection MVM p strain cytotoxic only in U373 and C6 (MVM) | ||
Murine: Fibroblast L929 and A9. Astrocytoma MT539MG [93], Human: U87 and MO59J [92] | - | Safe for microglia (MVMp) selective GBM infection (MVM) | ||
Murine: Fibroblast L929 and A9. Astrocytoma MT539MG [93], | - | Safe for microglia (MVMp) |
Virus | Modifications | Cell Lines | In Vivo Models | Results |
---|---|---|---|---|
Reovirus | Reovirus | Human: 24 GBM cell lines [99] | U87 and U251 intracranial and subcutaneous in SCID mice | Death in 20 out of 24 GBM lines Regression in both in vivo models Toxicity in nude mice. |
Human: U87 and 2 patient-derived lines [100] | GL261 intracranial in C57/BL6 | i.v. administration reaches brain tumors. T cell tumor recruitment and cytotoxicity. Synergy with anti PD-L1. | ||
Measles | MV-CEA: CEA expression. | Human: U87, U251, and U118 [105] | U87 intracranial and subcutaneous in nude mice | Regression in s.c. tumor after intravenous and intratumor administration. Regression in intracranial tumor after intratumor administration. |
MV-NIS: NIS expression. | Human: U87, U251 and 6 patient derived GBM [106] | U251 subcutaneous and GBM intracranial in nude mice | Synergic effect of virotherapy and radiotherapy. | |
MV-GFP-HAA-scEGFR: H protein partial deletion. scEGFR insertion in H protein. | Human: 5 patient derived GBM [107] | GBM intracranial in nude mice Mouse model Ifnarko CD46 Ge | Tumor regression after intratumor administration. No toxicity in CNS. | |
MV-141.4: scFvCD133 insertion in H. | Human: primary GBM [111] | GBM intracranial in NOD/SCID | Better survival rate in comparison with MV-Edm. | |
VSV | VSV WT | - | C6 subcutaneous nude mice [112] | Inhibition of tumor growth. |
VSV-ΔG: G protein deletion. | Human: U87 Rat: C6 [111] | - | Infection of cell lines. Rapid lysis. | |
VSVΔM51: M51 single nucleotide deletion. | Human: 14 glioma cell lines and 15 primary gliomas [115] | U87 and U118 subcutaneous in nude mice | Infection and elimination of all cell lines. Tumor regression and prolonged survival. | |
VSV-rp30: unknown viral glioma adaptation | Human: U87, U118, U373 and A172 [92] | U87 subcutaneous in nude mice | Increased selectivity and lytic capacity in glioblastoma cells. Tumor selectivity and cytopathic effect. | |
Human: U87 and U118 [116] | U87 orthotopic in nude mice | Infection and lysis of brain and peripheral tumors. | ||
VSV-CT1/CT2: G protein partial deletion | Human: U87, U118, U373 and A172 [114] | U87 orthotopic in nude mice | Elimination of tumor cells. Normal cell toxicity can be eliminated with IFN co-treatment VSV-1p-GFP: infection and potent apoptosis over tumor. | |
VSV-1p-GFP: GFP at the first position in the genome. VSV-CT9-M51: G protein partial deletion. M51 single nucleotide deletion. | Human: U87, U118, U373 and A172 Rat: 9L [119] | U87 orthotopic in CB17-SCID mice | VSV-CT1 and VSV-CT9-M51 have less toxicity than wt VSV. VSV-CT9-M51 is able to infect and kill tumors in brain. | |
VSV-CT9-M51: G protein partial deletion. M51 single nucleotide deletion. | Human: primary GBM [122] | Orthotopic CB17 SCID | Coinfection with AAV-mIFN-β or with ribavirin enhances oncolytic properties. | |
Seneca Valley | SVV-001 WT | Human: primary GBM [138] | 4 orthotopic models in nude mice | Partial response against glioma cells Effectivity in 2 of 4 in vivo tumors |
Human: GBM CSCs [139] | 6 GBM CSC orthotopic nude mice | 4 of 6 prolonged survival, tumor infection and cell lysis. Susceptibility dependent of sialic acid presence. | ||
NDV | NDV WT | Human: 6 GBM CSCs [129] | Orthotopic nude mice | NDV replication is dependent on IFN deletion. |
Human: U87 and DBTRG.05MG [130] | Subcutaneous nude mice | Induce apoptosis. Decrease tumor volume. | ||
Human: A172 and U87 and 2 CSCs [131] | - | Induce apoptosis. | ||
Murine: GL261 [132] | GL261 orthotopic mice | NDV induces ICD. | ||
Human: T98G, LN18, U251, U87. Rat: C6 [133] | C6 in rats | Synergistic effects with TMZ. Decrease tumor volumes and increase OS. | ||
Poliovirus | PVS-RIPO: IRES replaced with HRV2 | Human: U87 [142] | - | Reduce viability. |
Human: CSCs and established cell lines [145] | HTB14 orthotopic and HTB15 flanks | Tumor regression. | ||
Human: 6 CSCs [143] | - | Cytolysis. | ||
Human: U87, HTB14 and HTB15 [144] | HTB15 in athymic Balb/c mice | Tumor regression. | ||
Sindbis | Sindbis WT | Human: U87, U-118, U373, M059J, A172 [92] | U87 in flanks CB17-SCID mice | Effective replication and selective kill U87. |
Sindbis Gal.fu | Human: U87 [150] | U87 orthotopic in nude mice | Cytopathic activity. | |
RVFV | RVFV MP-12 and ZH548: attenuated strains | Rat: C6 [154] Human: U87 [155] | - | Infection occurs. |
Virus | Phase and Reference | n Patients | Results |
---|---|---|---|
Herpes | Phase I: HSV-1716 [38] | 9 | Two 24 moth survivors |
Phase Ib: HSV-1716 [39] | 12 | Evidence of tumor infection Three patients clinically stable for two years | |
Phase II: HSV-1716 NCT02031965 | 2 | No results available | |
Phase I: G207 [41] | 21 | No toxicities | |
Phase Ib: G207 [41] | 6 | No toxicity Evidence of tumor infection | |
Phase I: G207 [42] | 9 | No toxicities in combination with 5 Gy | |
Phase I: rQNestin34.5v2 NCT03152318 | 108 | Recruiting | |
Phase I: C134 NCT03657576 | 24 | Recruiting | |
Adenovirus | Phase I: ONYX-015 [66] | 24 | No toxicity One patient without progression and some with regression |
Phase I: Delta-24-RGD NCT03896568 | 36 | Recruiting | |
Phase I: Delta-24-RGD NCT03178032 | 12 | No results available | |
Phase II: Delta-24-RGD NCT02798406 | 49 | Active | |
Phase I: Delta-24-RGD NCT02197169 | 37 | No toxicities | |
Phase I: Delta-24-RGD NCT01956734 | 31 | No results available | |
Phase I and II: Delta-24-RGD NCT01582516 [156] | 20 | Virus spread in tumor, oncolytic effect and immunostimulation | |
Phase I: Delta-24-RGD NCT00805376 | 37 | 20% of >3 year survivors 12% of >95% tumor regression Evidence of immunostimulation | |
Phase II Delta-24-RGD (2016-001600-40) | - | Discontinued | |
Phase I: Delta-24-RGD NCT03714334 | 24 | Recruiting | |
Phase I: Delta-24-RGD NCT03072134 | 36 | No results available | |
Phase I: DNX-2440 NCT03714334 | 24 | Recruiting | |
Phase I/II: Ad-RTS-IL-12 NCT03330197 | 45 | Recruiting | |
Reovirus | Phase I: Reovirus [101] | 12 | No toxicities |
Phase I: Reovirus NCT00528684 [102] | 15 | One 2 year survivor One 3 year survivor | |
Phase Ib: Reovirus [100] | 9 | Evidence of T cell tumor infiltration and upregulation of IFN and PD-1/PD-L1 axis | |
Phase I: Reovirus/Sargramostim NCT02444546 | 6 | Active | |
Vaccinia | Phase I and II: TG6002 NCT03294486 | 78 | Recruiting |
Measles | Phase I: MV-CEA NCT00390299 | 23 | No toxicities |
NDV | Phase I/II: NDV-HUJ NCT01174537 [136] | 14 | No toxicities Complete regression in 1 patient |
Phase 0: MTH-68/H [134] | 4 | OS 5–9 years | |
VOL-DC vaccine [135] | 10 | Increased OS | |
Phase II: ATV-NDV vaccine [157] | 23 | PFS 40 weeks vs. 26 weeks | |
Parvovirus | H-1PV [94] | 18 | Enhanced immunogenicity |
Poliovirus | Phase I: NCT01491893 [147] | 61 | No neurovirulence and increased survival rate |
Phase II: NCT02986178 | 122 | Active | |
Phase Ib: NCT03043391 | 12 | Recruiting |
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Rius-Rocabert, S.; García-Romero, N.; García, A.; Ayuso-Sacido, A.; Nistal-Villan, E. Oncolytic Virotherapy in Glioma Tumors. Int. J. Mol. Sci. 2020, 21, 7604. https://doi.org/10.3390/ijms21207604
Rius-Rocabert S, García-Romero N, García A, Ayuso-Sacido A, Nistal-Villan E. Oncolytic Virotherapy in Glioma Tumors. International Journal of Molecular Sciences. 2020; 21(20):7604. https://doi.org/10.3390/ijms21207604
Chicago/Turabian StyleRius-Rocabert, Sergio, Noemí García-Romero, Antonia García, Angel Ayuso-Sacido, and Estanislao Nistal-Villan. 2020. "Oncolytic Virotherapy in Glioma Tumors" International Journal of Molecular Sciences 21, no. 20: 7604. https://doi.org/10.3390/ijms21207604
APA StyleRius-Rocabert, S., García-Romero, N., García, A., Ayuso-Sacido, A., & Nistal-Villan, E. (2020). Oncolytic Virotherapy in Glioma Tumors. International Journal of Molecular Sciences, 21(20), 7604. https://doi.org/10.3390/ijms21207604