Table Info

Table 3.

Self-replicating RNA viruses and examples of preclinical studies on cancer

Delivery method	Cancer	Outcome	Reference
Recombinant particles
SFV-endostatin	GBM	Tumor regression, superior to RV delivery	[100]
SFV-IL-18 + rec IL-12	GBM	Th1-biased response, anti-tumor immunity	[101]
VSVΔ-CHIKV Env	GBM	Selective infection, prolonged survival in mice	[102]
SFV4-miRT124	Glioma	Tumor growth inhibition, prolonged survival	[104]
SFV-1L-12 + LVR01	Breast	Inhibition of metastases, long-term survival	[105]
MV-HPV-16 L1	Cervical	Humoral immune response, neutralizing Abs	[106]
MV-HPV-16 L1	Cervical	Robust immune responses in primates	[107]
VSV-CRPV-E1/E2/E6/E7	Cervical	96.6% of papilloma volume, tumor eradication	[108]
VSV-HPV-16 E7	Cervical	T-cell responses, tumor volume reduction	[109]
VEE-HPV-16 E7	Cervical	T-cell responses, protection against tumors	[110]
SFVenh-HPV E6E7	Cervical	Complete tumor eradication in mice	[111]
KUN-GM-CSF	Colon	Tumor regression, cure of 50% of mice	[112]
SFV-VEGFR-2	Colon	Inhibition of tumor growth and metastases	[113]
SFV-VEGFR-2 + SFV-IL-4	Colon	Enhanced effect of co-administration	[113]
MV-GM-CSF	Colon	Complete remission in one third of mice	[114]
SFV-EGFP	Lung	Complete tumor regression of 3 out 7 mice	[115]
SIN-LacZ	Lung	Complete tumor remission, long-term survival	[116]
VSV-IFNβ	Lung	Tumor regression, cure of 30% of mice	[117]
KUN-GM-CSF	Melanoma	Tumor regression, cure of > 50% of mice	[112]
VEE-TRP-2	Melanoma	Anti-tumor activity, prolonged survival	[118]
VEE-TRP-2 + CTLA-4	Melanoma	Tumor regression in 50% of mice	[119]
VEE-TRP-2 + GITR	Melanoma	Complete tumor regression in 90% of mice	[119]
SIN-Luc	Hematologic	Tumor targeting, prolonged survival in mice	[120]
SIN + α4-1BB mAb	Lymphoma	Complete tumor eradication in mice	[121]
SFV-A20 mAb	Lymphoma	Antitumor protection, prolonged survival in mice	[122]
MV-αFR	Ovarian	Reduced tumor volume, improved survival	[123]
MV-CEA/MV-NIS	Ovarian	Superior tumor growth inhibition	[124]
SIN-IL-12 + irinotecan	Ovarian	Combination superior for prolonged survival	[125]
SFV-OVA + VV-OVA	Ovarian	Enhanced anti-tumor activity	[126]
MV-SLAMBlind	Pancreatic	Significant suppression of tumor growth	[127]
MV-CEA	Prostate	Delay in tumor growth, prolonged survival	[128]
VEE-PSMA	Prostate	PSMA-specific immune response	[129]
VEE-STEAP	Prostate	T-cell responses, prolonged survival	[130]
VEE-PSCA	Prostate	Long-term survival in 90% of mice	[131]
Oncolytic viruses
MV-GFP/CEA/NIS	Glioma	Cytotoxicity in GSCs, prolonged survival in mice	[132]
SFV VA-EGFP	Glioma	Long-term survival in 16 out 17 mice	[133]
M1 + doxorubicin	Breast	100-fold oncolytic activity with doxorubicin	[99]
MV-SLAMBlind	Breast	Strong oncolytic activity in mice	[134]
SFV VA-EGFP	Lung	Superior to Ad-based delivery	[135]
MV Hu-191	Lung	Tumor growth inhibition, prolonged survival	[136]
MV Schwarz	Lung	Prevention of uncontrolled tumor growth	[137]
MV-CEA Edmonston	Lung	Tumor regression in mice	[138]
YFV-OVA	Melanoma	Protection against tumor challenges in mice	[139]
MV-L-16	Melanoma	Tumor cell killing, prevention of tumor growth	[140]
VSV-LCMV-G	Melanoma	Tumor and metastases regression	[141]
VSV-LCMV-G + Rux	Ovarian	Tumor cell killing, enhanced tumor regression	[142]
VSVΔM51	Pancreatic	Superior tumor regression to Sendai virus & RSV	[143]
VSVΔM51-GFP + Gem	Pancreatic	Superior tumor regression with Gem	[144]
MV + MuV	Prostate	Superior oncolytic activity with combination	[145]
VSVΔM51-GFP	Prostate	Eradication of tumors, prolonged survival	[146]
VSV-LCMV-G	Prostate	Long-term remission of tumors and metastases	[147]
RNA replicons
SFV-LacZ	Colon	Tumor protection, regression. > survival	[148]
KUN-Mpt	Melanoma	CD8⁺ T-cell responses, protection against B16	[149]
Plasmid DNA replicons
SIN-gp100-IL-18	GBM	Protective and therapeutic effects, survival	[150]
SIN-HER2/neu	Breast	Tumor inhibition, superior with Ad-HER2/neu	[151]
SIN-HER2/neu	Breast	80% less DNA used compared to plasmid DNA	[152]
SFV-HPV E6-E7	Cervical	Eradication of 85% of tumors	[153]
SFV-VEGFR-2/IL-12 + SFV-survivin/β-hCG Ag	Melanoma	Superior tumor growth inhibition, prolonged survival after co-administration	[154]

CEA: carcinoembryonic antigen; CRPV: cottontail rabbit papillomavirus; CTLA-4: anti- cytotoxic T lymphocyte antigen-4; EGFP: enhanced green fluorescent protein; GBM: glioblastoma; Gem: gemcitabine; GFP: green fluorescent protein; GITR: anti-glucocorticoid-induced TNF family-related gene; GM-CSF: granulocyte-macrophage colony-stimulating factor; GSCs: glioma stem cells; HER2: human epidermal growth factor receptor 2; HPV: human papillomavirus; IL: interleukin; L-16: Leningrad-16; LCMV: lymphocytic choriomeningitis virus; Luc: luciferase: mAb: monoclonal Ab; Mpt: murine polyepitope; MuV: mumps virus; OVA: ovalbumin; PSCA: prostate stem cell antigen; PSMA: prostate-specific membrane antigen; Rux: ruxolitinib; SLAM: signaling lymphocyte activation molecule; STEAP: six-transmembrane epithelial antigen of the prostate; TRP-2: tyrosine-related protein-2; VEGFR-2: vascular epithelial growth factor receptor-2; αFR: alpha-folate receptor; β-hCG: beta-human chorionic gonadotropin

Declarations

Author contributions

The author contributed solely to the work.

Conflicts of interest

The author declares that he has no conflicts of interest.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publication

Not applicable.

Availability of data and materials

Not applicable.

Funding

Not applicable.

Copyright

References

Patil S, Gao YG, Lin X, Li Y, Dang K, Tian Y, et al. The development of functional non-viral vectors for gene delivery. Int J Mol Sci. 2019;20:5491. [DOI] [PubMed] [PMC]

Chen YH, Keiser MS, Davidson BL. Viral vectors for gene transfer. Curr Protoc Mouse Biol. 2018;8:e58. [DOI] [PubMed]

Lundstrom K. Viral vectors in gene therapy. Diseases. 2018;6:42. [DOI] [PubMed] [PMC]

Lundstrom K. Self-replicating RNA viruses for vaccine development against infectious diseases and cancer. Vaccines (Basel). 2021;9:1187. [DOI] [PubMed] [PMC]

Frolov I, Hoffman TA, Prágai BM, Dryga SA, Huang HV, Schlesinger S, et al. Alphavirus-based expression vectors: strategies and applications. Proc Natl Acad Sci U S A. 1996;93:11371–7. [DOI] [PubMed] [PMC]

Strauss JH, Strauss EG. The alphaviruses: gene expression, replication and evolution. Microbiol Rev. 1994;58:491–562. [DOI] [PubMed] [PMC]

Liljeström P, Garoff H. A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (N Y). 1991;9:1356–61. [DOI] [PubMed]

Xiong C, Levis R, Shen P, Schlesinger S, Rice CM, Huang HV. Sindbis virus: an efficient, broad host range vector for gene expression in animal cells. Science. 1989;243:1188–91. [DOI] [PubMed]

Davis NL, Willis LV, Smith JF, Johnston RF. In vitro synthesis of infectious venezuelan equine encephalitis virus RNA from a cDNA clone: analysis of a viable deletion mutant. Virology. 1989;171:189–204. [DOI] [PubMed]

10.

DiCiommo PD, Bremner R. Rapid, high level protein production using DNA-based Semliki Forest virus vectors. J Biol Chem. 1998;273:18060–6. [DOI] [PubMed]

11.

Raouane M, Desmaële D, Urbinati G, Massaad-Massade L, Couvreur P. Lipid conjugated oligonucleotides: a useful strategy for delivery. Bioconjug Chem. 2012;23:1091–104. [DOI] [PubMed]

12.

Geall AJ, Verma A, Otten GR, Shaw CA, Hekele A, Banerjee K, et al. Nonviral delivery of self-amplifying RNA vaccines. Proc Natl Acad Sci U S A. 2012;109:14604–9. [DOI] [PubMed] [PMC]

13.

Blakney AK, Ip S, Geall AJ. An update on self-amplifying mRNA vaccine development. Vaccines (Basel). 2021;9:97. [DOI] [PubMed] [PMC]

14.

Pijlman GP, Suhrbier A, Khromykh AA. Kunjin virus replicons: an RNA-based non-cytopathic viral vector system for protein production, vaccine and gene therapy applications. Expert Opin Biol Ther. 2006;6:134–45. [DOI] [PubMed]

15.

Shi PY, Tilgner M, Lo MK. Construction and characterization of subgenomic replicons of New York strain of West Nile virus. Virology. 2002;296:219–33. [DOI] [PubMed]

16.

Molenkamp R, Kooi EA, Lucassen MA, Greve S, Thijssen JC, Spaan WJ, et al. Yellow fever virus replicons as an expression system for hepatitis C virus structural proteins. J Virol. 2003;77:1644–8. [DOI] [PubMed] [PMC]

17.

Jones M, Davidson A, Hibbert L, Gruenwald P, Schlaak J, Ball S, et al. Dengue virus inhibits alpha interferon signaling by reducing STAT2 expression. J Virol. 2005;79:5414–20. [DOI] [PubMed] [PMC]

18.

Gherke R, Ecker M, Aberle SW, Allison SL, Heinz FX, Mandi CW. Incorporation of tick-borne encephalitis virus replicons into virus-like particles by a packaging cell line. J Virol. 2003;77:8924–33. [DOI] [PubMed] [PMC]

19.

Fan ZC, Dennis JC, Bird RC. Bovine viral diarrhea virus is a suitable viral vector for stable expression of heterologous gene when inserted between N^pro and C genes. Virus Res. 2008;138:97–104. [DOI] [PubMed]

20.

Stetter P, Devos R, Moser C, Tratschin JD, Hofmann MA. Establishment and application of bicistronic classical swine fever virus genomes for foreign gene expression and complementation of E2 deletion mutants. Virus Res. 2002;85:173–85. [DOI] [PubMed]

21.

de Felipe P. Skipping the co-expression problem: the new 2A “CHYSEL” technology. Genet Vaccines Ther. 2004;2:13. [DOI] [PubMed] [PMC]

22.

Khromykh AA, Varnavski AN, Westaway EG. Encapsidation of the flavivirus kunjin replicon RNA by using a complementation system providing Kunjin virus structural proteins in trans. J Virol. 1998;72:5967–77. [DOI] [PubMed] [PMC]

23.

Mühlebach MD, Hutzler S. Development of recombinant measles virus-based vaccines. Methods Mol Biol. 2017;1581:151–68. [DOI] [PubMed] [PMC]

24.

Mühlebach MD. Vaccine platform recombinant measles virus. Virus Genes. 2017;53:733–40. [DOI] [PubMed] [PMC]

25.

Radecke F, Spielhofer P, Schneider H, Kaelin K, Huber M, Dötsch C, et al. Rescue of measles viruses from cloned DNA. EMBO J. 1995;14:5773–84. [DOI] [PubMed] [PMC]

26.

Schneider H, Spielhofer P, Kaelin K, Dötsch C, Radecke F, Sutter G, et al. Rescue of measles virus using a replication-deficient vaccinia-T7 vector. J Virol Methods. 1997;64:57–64. [DOI] [PubMed]

27.

Martin A, Staeheli P, Schneider U. RNA polymerase II-controlled expression of antigenomic RNA enhances the rescue efficacies of two different members of the Mononegavirales independently of the site of viral genome replication. J Virol. 2006;80:5708–15. [DOI] [PubMed] [PMC]

28.

Schnell MJ, Buonocore L, Kretzschmar E, Johnson E, Rose JK. Foreign glycoproteins expressed from recombinant vesicular stomatitis viruses are incorporated efficiently into virus particles. Proc Natl Acad Sci U S A. 1996;93:11359–65. [DOI] [PubMed] [PMC]

29.

Lyles DS, Rupprecht CE. Rhabdoviridiae. 5th ed. In: Knipe DM, Howley PM, editors. Fields’ virology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2007. pp. 1364–408.

30.

Hastie E, Grdzelishvili VZ. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J Gen Virol. 2012;93:2529–45. [DOI] [PubMed] [PMC]

31.

Ito N, Takayama-Ito M, Yamada K, Hosokawa J, Sugiyama M, Minamoto N. Improved recovery of rabies virus from cloned cDNA using a vaccinia virus-free reverse genetics system. Microbiol Immunol. 2003;47:613–7. [DOI] [PubMed]

32.

Harty RN, Brown ME, Hayes FP, Wright NT, Schnell MJ. Vaccinia virus-free recovery of vesicular stomatitis virus. J Mol Microbiol Biotechnol. 2001;3:513–7. [PubMed]

33.

Tani H, Morikawa S, Matsuura Y. Development and applications of VSV vectors based on cell tropism. Front Microbiol. 2012;2:272. [DOI] [PubMed] [PMC]

34.

Pol JG, Zhang L, Bridle BW, Stephenson KB, Rességuier J, Hanson S, et al. Maraba virus as a potent oncolytic vaccine vector. Mol Ther. 2014;22:420–9. [DOI] [PubMed] [PMC]

35.

Osakada F, Callaway EM. Design and generation of recombinant rabies virus vectors. Nat Protoc. 2013;8:1583–601. [DOI] [PubMed] [PMC]

36.

Ohara S, Inoue K, Yamada M, Yamawaki T, Koganezawa N, Tsuttsui K, et al. Dual transneural tracing in the rat entorhoinal-hippocampal circuit by intracerebral injection of recombinant rabies virus vectors. Front Neuroanat. 2009;3:1. [DOI] [PubMed] [PMC]

37.

Thomas JM, Moen ST, Gnade BT, Vargas-Inchaustegui DA, Foitz SM, Suarez G, et al. Recombinant Sindbis virus vectors designed to express protective antigen of Bacillus anthracis protect animals from anthrax and display synergy with ciprofloxacin. Clin Vaccine Immunol. 2009;16:1696–9. [DOI] [PubMed] [PMC]

38.

Cabrera A, Sáez D, Céspedes S, Andrews E, Oñate A. Vaccination with recombinant Semliki Forest virus particles expressing translation initiation factor 3 of Brucella abortus induces protective immunity in BALB/c mice. Immunobiology. 2009;214:467–74. [DOI] [PubMed]

39.

Andersson C, Vasconcelos NM, Sievertzon M, Haddad D, Liljeqvist S, Berglund P, et al. Comparative immunization study using RNA and DNA constructs encoding a part of the Plasmodium falciparum antigen Pf332. Scand J Immunol. 2001;54:117–24. [DOI] [PubMed]

40.

Tsuji M, Bergmann CC, Takita-Sonoda Y, Murata K, Rodrigues EG, Nussenzweig RS, et al. Recombinant Sindbis viruses expressing a cytotoxic T-lymphocyte epitope of a malaria parasite or of influenza virus elicit protection against the corresponding pathogen in mice. J Virol. 1998;72:6907–10. [DOI] [PubMed] [PMC]

41.

Ljungberg K, Liljeström P. Self-replicating alphavirus RNA vaccines. Expert Rev Vaccines. 2015;14:177–94. [DOI] [PubMed]

42.

Chattopadhyay A, Aquilar PV, Bopp NE, Yarovinsky TO, Weaver SC, Rose JK. A recombinant virus vaccine that protects against both Chikungunya and Zika virus infections. Vaccine. 2018;36:3894–900. [DOI] [PubMed]

43.

Reed DS, Glass PJ, Bakken RR, Barth JF, Lind CM, da Silva L, et al. Combined alphavirus replicon particle vaccine induces durable and cross-protective immune responses against equine encephalitis viruses. J Virol. 2014;88:12077–86. [DOI] [PubMed] [PMC]

44.

Rossi SL, Comer JE, Wang E, Azar SR, Lawrence WS, Plante JA, et al. Immunogenicity and efficacy of a measles virus-vectored chikungunya vaccine in nonhuman primates. J Infect Dis. 2019;220:735–42. [DOI] [PubMed] [PMC]

45.

Safronetz D, Mire C, Rosenke K, Feldmann F, Haddock E, Geissbert T, et al. A recombinant vesicular stomatitis virus-based Lassa fever vaccine protects guinea pigs and macaques against challenge with geographically and genetically distinct Lassa viruses. PLoS Negl Trop Dis. 2015;9:e0003736. [DOI] [PubMed] [PMC]

46.

Mateo M, Reynard S, Carnec X, Journeaux A, Baillet N, Schaeffer J, et al. Vaccines inducing immunity to Lassa fever glycoprotein and nucleoprotein protect macaques after a single shot. Sci Transl Med. 2019;11:eaaw3163. [DOI] [PubMed]

47.

Bredenbeek PJ, Molenkamp R, Spaan WJM, Deubel V, Marianneu P, Salvato MS, et al. A recombinant yellow fever 17D expressing Lassa virus glycoproteins. Virology. 2006;345:299–304. [DOI] [PubMed] [PMC]

48.

Lukashevich IS, Pushko P. Vaccine platforms to control Lassa fever. Expert Rev Vaccines. 2016;15:1135–50. [DOI] [PubMed]

49.

Pushko P, Geisbert J, Parker M, Jahrling P, Smith J. Individual and bivalent vaccines based on alphavirus replicons protect guinea pigs against infection with Lassa and Ebola virus. J Virol. 2001;75:11677–85. [DOI] [PubMed] [PMC]

50.

Thompson JM, Whitmore AC, Staats HF, Johnston RE. Alphavirus replicon particles acting as adjuvants promote CD8⁺ T cell responses to co-delivered antigen. Vaccine. 2008;26:4267–75. [DOI] [PubMed] [PMC]

51.

Pyankov OV, Bodnev SA, Pyankova OG, Solodkyi VV, Pyankov SA, Setoh YX, et al. A kunjin replicon virus-like vaccine provides protection against Ebola virus infection in nonhuman primates. J Infect Dis. 2015;212 Suppl 2:S368–71. [DOI] [PubMed] [PMC]

52.

Marzi A, Robertson SJ, Haddock E, Feldmann F, Hanley PW, Scott DP, et al. Ebola vaccine. VSV-EBOV rapidly protects macaques against infection with the 2014/2015 Ebola virus outbreak strain. Science. 2015;349:739–42. [DOI] [PubMed]

53.

Geisbert TW, Feldmann H. Recombinant vesicular stomatitis virus-based vaccines against Ebola and Marburg infections. J Infect Dis. 2011;204 Suppl 3:S1075–81. [DOI] [PubMed] [PMC]

54.

Khalil SM, Tonkin DR, Mattocks MD, Snead AT, Johnston RE, White LJ. A tetravalent alphavirus-vector based dengue vaccine provides effective immunity in an early life mouse model. Vaccine. 2014;32:4068–74. [DOI] [PubMed] [PMC]

55.

Hu HM, Chen HW, Hsiao YJ, Wu SH, Chung HH, Hsieh CH, et al. The successful induction of T-cell and antibody responses by a recombinant measles virus-vectored tetravalent dengue vaccine provides partial protection against dengue-2 infection. Hum Vaccines Immunother. 2016;12:1678–89. [DOI] [PubMed] [PMC]

56.

Kurup D, Wirblich C, Lambert R, Diba LZ, Leiby BE, Schnell MJ. Measles-based Zika vaccine induces long-term immunity and requires NS1 antibodies to protect the female reproductive tract. NPJ Vaccines. 2022;7:43. [DOI] [PubMed] [PMC]

57.

Lorin C, Mollet L, Delebecque F, Combredet C, Hurtrel B, Charneau P, et al. A single injection of recombinant measles virus vaccine expressing human immunodeficiency virus (HIV) type 1 clade B envelope glycoproteins induces neutralizing antibodies and cellular immune responses to HIV. J Virol. 2004;78:146–57. [DOI] [PubMed] [PMC]

58.

Brand D, Lemiale F, Turbica I, Buzelay L, Brunet S, Barin F. Comparative analysis of humoral immune responses to HIV type 1 envelope glycoproteins in mice immunized with a DNA vaccine, recombinant Semliki Forest virus RNA, or recombinant Semliki Forest virus particles. AIDS Res Hum Retroviruses. 1998;14:1369–77. [DOI] [PubMed]

59.

Ajbani SP, Velhal SM, Kadam RB, Patel VV, Lundstrom K, Bandivdekar AH. Immunogenicity of virus-like Semliki Forest virus replicon particles expressing Indian HIV-1C gag, env and polRT genes. Immunol Lett. 2017;190:221–32. [DOI] [PubMed]

60.

Ito T, Kumagai T, Yamaji Y, Sawada A, Nakayama T. Recombinant measles AIK-C vaccine strain expressing influenza HA protein. Vaccines (Basel). 2020;8:149. [DOI] [PubMed] [PMC]

61.

Ryder AB, Buonocore L, Vogel L, Nachbagauer R, Krammer F, Rose JK. A viable recombinant rhabdovirus lacking its glycoprotein gene and expressing influenza virus hemagglutinin and neuraminidase is a potent influenza vaccine. J Virol. 2015;89:2820–30. [DOI] [PubMed] [PMC]

62.

Furuyama W, Reynolds P, Haddock E, Meade-White K, Quynh Le M, Kawaoka Y, et al. A single dose of a vesicular stomatitis virus-based influenza vaccine confers rapid protection against H5 viruses from different clades. NPJ Vaccines. 2020;5:4. [DOI] [PubMed] [PMC]

63.

Schultz-Cherry S, Dybing JK, Davis NL, Williamson C, Suarez DL, Johnston R, et al. Influenza virus (A/HK/156/97) hemagglutinin expressed by an alphavirus replicon system protects against lethal infection with Hong Kong-origin H5N1 viruses. Virology. 2000;278:55–9. [DOI] [PubMed]

64.

Krishnavajhala HR, Willimas J, Heidner H. An influenza A virus vaccine based on an M2e-modified alphavirus. Arch Virol. 2018;163:483–8. [DOI] [PubMed]

65.

Démoulins T, Ruggli N, Gerber M, Thomann-Harwood LJ, Ebensen T, Schulze K, et al. Self-amplifying pestivirus replicon RNA encoding influenza virus nucleoprotein and hemagglutinin promote humoral and cellular immune responses in pigs. Front Immunol. 2021;11:622385. [DOI] [PubMed] [PMC]

66.

Lundstrom K. Viral vector-based vaccines against SARS-CoV-2. Explor Immunol. 2021;1:295–308. [DOI]

67.

Sheahan T, Whitmore A, Long K, Ferris M, Rockx B, Funkhouser W, et al. Successful vaccination strategies that protect aged mice from lethal challenge from influenza virus and heterologous severe acute respiratory syndrome coronavirus. J Virol. 2011;85:217–30. [DOI] [PubMed] [PMC]

68.

Liu R, Wang J, Shao Y, Wang X, Zhang H, Shuai L, et al. A recombinant VSV-vectored MERS-CoV vaccine induces neutralizing antibody and T cell responses in rhesus monkeys after single dose immunization. Antiviral Res. 2018;150:30–8. [DOI] [PubMed] [PMC]

69.

Hörner C, Schürmann C, Auste A, Ebenig A, Muraleedharan S, Dinnon KH 3rd, et al. A highly immunogenic and effective measles virus-based Th1-biased COVID-19 vaccine. Proc Natl Acad Sci U S A. 2020;117:32657–66. [DOI] [PubMed] [PMC]

70.

Case JB, Rothlauf PW, Chen RE, Kafai NM, Fox JM, Smith BK, et al. Replication-competent vesicular stomatitis virus vaccine vector protects against SARS-CoV-2-mediated pathogenesis in mice. Cell Host Microbe. 2020;28:465–74.e4. [DOI] [PubMed] [PMC]

71.

Yahalom-Ronen Y, Tamir H, Melamed S, Politi B, Shifman O, Achdout H, et al. A single dose of recombinant VSV-ΔG-spike provides protection against SARS-CoV-2 challenge. Nat Commun. 2020;11:6402. [DOI] [PubMed] [PMC]

72.

Scaglione A, Opp S, Hurtado A, Lin Z, Pampeno C, Noval MG, et al. Combination of a Sindbis-SARS-CoV-2 spike vaccine and aOX40 antibody elicits protective immunity against SARS-CoV-2 induced disease and potentiates long-term SARS-CoV-2-specific humoral and T-cell immunity. Front Immunol. 2021;12:719077. [DOI] [PubMed] [PMC]

73.

Tao J, Li B, Shi Y, Chen J, Zhu G, Shen X, et al. Attenuated porcine-derived type 2 bovine viral diarrhea virus as vector stably expressing viral gene. J Virol Methods. 2020;279:113842. [DOI] [PubMed]

74.

Ravel G, Mantel N, Silvano J, Rogue A, Guy B, Jackson N, et al. Biodistribution and safety of a live and attenuated tetravalent dengue vaccine in the cynomolgus monkey. Vaccine. 2017;35:5918–23. [DOI] [PubMed]

75.

Abeyratne E, Tharmarajah K, Freitas JR, Mostafavi H, Mahalingam S, Zaid A, et al. Liposomal delivery of the RNA genome of a live-attenuated Chikungunya virus vaccine candidate provides local, but not systemic protection after one dose. Front Immunol. 2020;11:304. [DOI] [PubMed] [PMC]

76.

Zhang YN, Chen C, Deng CL, Zhang CG, Li N, Wang Z, et al. A novel rabies vaccine based on propagating particles derived from hybrid VEEV-Rabies replicon. EBIOMedicine. 2020;56:102819. [DOI] [PubMed] [PMC]

77.

Pardi N, Hogan MJ, Porter FW, Weissman D. mRNA vaccines—a new era in vaccinology. Nat Rev Drug Discov. 2018;17:261–79. [DOI] [PubMed] [PMC]

78.

Erasmus JH, Khandhar AP, Guderian J, Granger B, Archer J, Archer M, et al. A nanostructured lipid carrier for delivery of a replicating viral RNA provides single, low-dose protection against Zika. Mol Ther. 2018;26:2507–22. [DOI] [PubMed] [PMC]

79.

Giraud A, Ataman-Onal Y, Battail N, Piga N, Brand D, Mandrand B, et al. Generation of monoclonal antibodies to native human immunodeficiency virus type 1 envelope glycoprotein by immunization of mice with naked RNA. J Virol Methods. 1999;79:75–84. [DOI] [PubMed]

80.

Melo M, Porter E, Zhang Y, Silva M, Li N, Dobosh B, et al. Immunogenicity of RNA replicons encoding HIV env immunogens designed for self-assembly into nanoparticles. Mol Ther. 2019;27:2080–90. [DOI] [PubMed] [PMC]

81.

Bogers WM, Oostermeijer H, Mooij P, Koopman G, Verschoor EJ, Davis D, et al. Potent immune responses in rhesus macaques induced by nonviral delivery of self-amplifying RNA vaccine expressing HIV type 1 envelope with a cationic nanoemulsion. J Infect Dis. 2015;211:947–55. [DOI] [PubMed] [PMC]

82.

Fleeton MN, Chen M, Berglund P, Rhodes G, Parker SE, Murphy M, et al. Self-replicative RNA vaccines elicit protection against influenza A virus, respiratory syncytial virus, and a tickborne encephalitis virus. J Infect Dis. 2001;183:1395–8. [DOI] [PubMed]

83.

Vogel AB, Lambert L, Kinnear E, Busse D, Erbar S, Reufer KC, et al. Self-amplifying RNA vaccines give equivalent protection against influenza to mRNA vaccines but at much lower doses. Mol Ther. 2018;26:446–55. [DOI] [PubMed] [PMC]

84.

McKay PF, Hu K, Blakney AK, Samnuan K, Brown JC, Penn R, et al. Self-amplifying RNA SARS-CoV-2 lipid nanoparticle vaccine candidate induces high neutralizing antibody titers in mice. Nat Commun. 2020;11:3523. [DOI] [PubMed] [PMC]

85.

de Alwis R, Gan ES, Chen S, Leong YS, Tan HC, Zhang SL, et al. A single dose of self-transcribing and replicating RNA-based SARS-CoV-2 vaccine produces protective adaptive immunity in mice. Mol Ther. 2021;29:1970–83. [DOI] [PubMed] [PMC]

86.

Tretyakova I, Tibbens A, Jokinen JD, Johnson DM, Lukashevich JS, Pushko P. Novel DNA-launched Venezuelan equine encephalitis virus vaccine with rearranged genome. Vaccine. 2019;37:3317–25. [DOI] [PubMed]

87.

Tretyakova I, Plante KS, Rossi SL, Lawrence WS, Peel JE, Gudjohnsen S, et al. Venezuelan equine encephalitis vaccine with rearranged genome resists reversion and protects non-human primates from viremia after aerosol challenge. Vaccine. 2020;38:3378–86. [DOI] [PubMed]

88.

Knudsen ML, Ljungberg K, Tatoud R, Weber J, Esteban M, Liljeström P. Alphavirus replicon DNA expressing HIV antigens is an excellent prime for boosting with recombinant modified vaccinia Ankara (MVA) or with HIV gp140 protein antigen. PLoS One. 2015;10:e0117042. [DOI] [PubMed] [PMC]

89.

Henao-Restrepo AM, Longini IM, Egger M, Dean NE, Edmunds WJ, Camacho A, et al. Efficacy and effectiveness of an rVSV-vectored vaccine expressing Ebola surface glycoprotein: interim results from the Guinea ring vaccination cluster-randomised trial. Lancet. 2015;386:857–66. [DOI] [PubMed]

90.

Henao-Restrepo AM, Camacho A, Longini IM, Watson CH, Edmunds WJ, Egger M, et al. Efficacy and effectiveness of an rVSV-vectored vaccine in preventing Ebola virus disease: final results from the Guinea ring vaccination, open-label, cluster-randomised trial (Ebola Ça Suffit!). Lancet. 2017;389:505–18. Erratum in: Lancet. 2017;389:504. [DOI]

91.

Nature [Internet]. Berlin: Springer Nature Limited; c2022 [cited 2022 Mar 14]. Available from: https://www.nature.com/articles/nature.2017.22024

92.

Torresi J, Ebert G, Pellegrini M. Vaccines licensed and in clinical trials for the prevention of dengue. Hum Vaccin Immunother. 2017;13:1059–72. [DOI] [PubMed] [PMC]

93.

Godói IP, Lemos LL, de Araújo VE, Bonoto BC, Godman B, Guerra Júnior AA. CYD-TDV dengue vaccine: systematic review and meta-analysis of efficacy, immunogenicity and safety. J Comp Eff Res. 2017;6:165–80. [DOI] [PubMed]

94.

Wecker M, Gilbert P, Russell N, Hural J, Allen M, Pensiero M, et al. Phase I safety and immunogenicity evaluations of an alphavirus replicon HIV-1 subtype C gag vaccine in healthy HIV-1-uninfected adults. Clin Vaccine Immunol. 2012;19:1651–60. [DOI] [PubMed] [PMC]

95.

Fukuhara H, Ino Y, Todo T. Oncolytic virus therapy: a new era of cancer treatment at dawn. Cancer Sci. 2016;107:1373–9. [DOI] [PubMed] [PMC]

96.

Zamarin D, Palese P. Oncolytic Newcastle disease virus for cancer therapy: old challenges and new directions. Future Microbiol. 2012;7:347–67. [DOI] [PubMed] [PMC]

97.

Aref S, Bailey K, Fielding A. Measles to the rescue: a review of oncolytic measles virus. Viruses. 2016;8:294. [DOI] [PubMed] [PMC]

98.

Ebert O, Shinozaki K, Huang TG, Savontaus MJ, Garcia-Sastre A, Woo SL. Oncolytic vesicular stomatitis virus for treatment of orthotopic hepatocellular carcinoma in immune-competent rats. Cancer Res. 2003;63:3605–11. [PubMed]

99.

Zhang J, Liu Y, Tan J, Zhang Y, Wong CW, Lin Z, et al. Necroptotic virotherapy of oncolytic alphavirus M1 cooperated with doxorubicin displays promising therapeutic efficacy in TNBC. Oncogene. 2021;40:4783–95. [DOI] [PubMed]

100.

Yamanaka R, Zullo SA, Ramsey J, Onodera M, Tanaka R, Blaese M. Induction of therapeutic antitumor anti-angiogenesis by intratumoral injection of genetically engineered endostatin-producing Semliki Forest virus. Cancer Gene Ther. 2001;8:796–802. [DOI] [PubMed]

101.

Yamanaka R, Tsuchiya N, Yajima N, Honma J, Hasegawa H, Tanaka R, et al. Induction of an antitumor immunological response by an intratumoral injection of dendritic cells pulsed with genetically engineered Semliki Forest virus to produce interleukin-18 combined with the systemic administration of interleukin-12. J Neurosurg. 2003;99:746–53. [DOI] [PubMed]

102.

Zhang X, Mao G, van den Pol AN. Chikungunya-vesicular stomatitis chimeric virus targets and eliminates brain tumors. Virology. 2018;522:244–59. [DOI] [PubMed] [PMC]

103.

Griffin D. Neurotropic alphaviruses. In: Reiss C, editor. Neurotropic viral infections. Cham, Switzerland: Springer International Publishing; 2016. pp. 175–204. [DOI]

104.

Martikainen M, Niittykoski M, von und zu Fraunberg M, Immonen A, Koponen S, van Geenen M, et al. MicroRNA-attenuated clone of virulent Semliki Forest virus overcomes antiviral type I interferon in resistant mouse CT-2A glioma. J Virol. 2015;89:10637–47. [DOI] [PubMed] [PMC]

105.

Kramer MG, Masner M, Casales E, Moreno M, Smerdou C, Chabalgoity JA. Neoadjuvant administration of Semliki Forest virus expressing interleukin-12 combined with attenuated Salmonella eradicates breast cancer metastasis and achieves long-term survival in immunocompetent mice. BMC Cancer. 2015;15:620. [DOI] [PubMed] [PMC]

106.

Cantarella G, Liniger M, Zuniga A, Schiller JT, Billeter M, Naim HY, et al. Recombinant measles virus-HPV vaccine candidates for prevention of cervical carcinoma. Vaccine. 2009;27:3385–90. [DOI] [PubMed] [PMC]

107.

Gupta G, Giannino V, Rishi N, Glueck R. Immunogenicity of next-generation HPV vaccines in non-human primates: measles-vectored HPV vaccine versus Pichia pastoris recombinant protein vaccine. Vaccine. 2016;34:4724–31. [DOI] [PubMed] [PMC]

108.

Brandsma JL, Shylankevich M, Su Y, Roberts A, Rose JK, Zelterman D, et al. Vesicular stomatitis virus-based therapeutic vaccination targeted to the E1, E2, E6, and E7 proteins of cottontail rabbit papillomavirus. J Virol. 2007;81:5749–58. [DOI] [PubMed] [PMC]

109.

Liao JB, Publicover J, Rose JK, DiMaio D. Single-dose, therapeutic vaccination of mice with vesicular stomatitis virus expressing human papillomavirus type 16 E7 protein. Clin Vaccine Immunol. 2008;15:817–24. [DOI] [PubMed] [PMC]

110.

Velders MP, McElhiney S, Cassetti MC, Eiben GL, Higgins T, Kovacs GR, et al. Eradication of established tumors by vaccination with Venezuelan equine encephalitis virus replicon particles delivering human papillomavirus 16 E7 RNA. Cancer Res. 2001;61:7861–7. [PubMed]

111.

Daemen T, Riezebos-Brilman A, Bungener L, Regts J, Dontje B, Wilschut J. Eradication of established HPV16-transformed tumours after immunisation with recombinant Semliki Forest virus expressing a fusion protein of E6 and E7. Vaccine. 2003;21:1082–8. [DOI] [PubMed]

112.

Hoang-Le D, Smeenk L, Anraku I, Pijlman GP, Wang XJ, de Vrij J, et al. A Kunjin replicon vector encoding granulocyte macrophage colony-stimulating factor for intra-tumoral gene therapy. Gene Ther. 2009;16:190–9. [DOI] [PubMed]

113.

Lyons JA, Sheahan BJ, Galbraith SE, Mehra R, Atkins GJ, Fleeton MN. Inhibition of angiogenesis by a Semliki Forest virus vector expressing VEGFR-2 reduces tumour growth and metastasis in mice. Gene Ther. 2007;14:503–13. [DOI] [PubMed]

114.

Grossardt C, Engeland CE, Bossow S, Halama N, Zaoui K, Leber MF, et al. Granulocyte-macrophage colony-stimulating factor-armed oncolytic measles virus is an effective therapeutic cancer vaccine. Hum Gene Ther. 2013;24:644–54. [DOI] [PubMed] [PMC]

115.

Murphy AM, Morris-Downes MM, Sheahan BJ, Atkins GJ. Inhibition of human lung carcinoma cell growth by apoptosis induction using Semliki Forest virus recombinant particles. Gene Ther. 2000;7:1477–82. [DOI] [PubMed]

116.

Granot T, Yamanashi Y, Meruelo D. Sindbis viral vectors transiently deliver tumor-associated antigens to lymph nodes and elicit diversified antitumor CD8⁺ T-cell immunity. Mol Ther. 2014;22:112–22. [DOI] [PubMed] [PMC]

117.

Patel MR, Jacobson BA, Ji Y, Drees J, Tang S, Xiong K, et al. Vesicular stomatitis virus expressing interferon-β is oncolytic and promotes antitumor immune responses in a syngeneic murine model of non-small cell lung cancer. Oncotarget. 2015;6:33165–77. [DOI] [PubMed] [PMC]

118.

Avogadri F, Merghoub T, Maughan MF, Hirschhorn-Cymerman D, Morris J, Ritter E, et al. Alphavirus replicon particles expressing TRP-2 provide potent therapeutic effect on melanoma through activation of humoral and cellular immunity. PLoS One. 2010;5:e12670. [DOI] [PubMed] [PMC]

119.

Avogadri F, Zappasodi R, Yang A, Budhu S, Malandro N, Hirschhorn-Cymerman D, et al. Combination of alphavirus replicon particle-based vaccination with immunomodulatory antibodies: therapeutic activity in the B16 melanoma mouse model and immune correlates. Cancer Immunol Res. 2014;2:448–58. [DOI] [PubMed] [PMC]

120.

Suzme R, Tseng JC, Levin B, Ibrahim S, Meruelo D, Pellicer A. Sindbis viral vectors target hematopoietic malignant cells. Cancer Gene Ther. 2012;19:757–66. [DOI] [PubMed]

121.

Yu M, Scherwitzl I, Opp S, Tsirigos A, Meruelo D. Molecular and metabolic pathways mediating curative treatment of a non-Hodgkin B cell lymphoma by Sindbis viral vectors and anti-4-1BB monoclonal antibody. J Immunother Cancer. 2019;7:185. [DOI] [PubMed] [PMC]

122.

Casales E, Martisova E, Villanueva H, de Cerio ALD, Inoges S, Silva-Pilipich N, et al. Idiotype vaccines produced with a non-cytopathic alphavirus self-amplifying RNA vector induce antitumor responses in a murine model of B-cell lymphoma. Sci Rep. 2021;11:21427. [DOI] [PubMed] [PMC]

123.

Hasegawa K, Nakamura T, Harvey M, Ikeda Y, Oberg A, Figini M, et al. The use of a tropism-modified measles virus in folate receptor-targeted virotherapy of ovarian cancer. Clin Cancer Res. 2006;12:6170–8. [DOI] [PubMed]

124.

Hasegawa K, Pham L, O’Connor MK, Federspiel MJ, Russel SJ, Peng KW. Dual therapy of ovarian cancer using measles viruses expressing carcinoembryonic antigen and sodium iodide symporter. Clin Cancer Res. 2006;12:1868–75. [DOI] [PubMed]

125.

Granot T, Meruelo D. The role of natural killer cells in combinatorial anti-cancer therapy using Sindbis viral vectors and irinotecan. Cancer Gene Ther. 2012;19:588–91. [DOI] [PubMed]

126.

Zhang YQ, Tsai YC, Monie A, Wu TC, Hung CF. Enhancing the therapeutic effect against ovarian cancer through a combination of viral oncolysis and antigen-specific immunotherapy. Mol Ther. 2010;18:692–9. [DOI] [PubMed] [PMC]

127.

Awano M, Fuijyki T, Shoji K, Amagai Y, Murakami Y, Furukawa Y, et al. Measles virus selectively blind to signaling lymphocyte activity molecule has oncolytic efficacy against nectin-4-expressing pancreatic cancer cells. Cancer Sci. 2016;107:1647–52. [DOI] [PubMed] [PMC]

128.

Msaouel P, Iankov ID, Allen C, Morris JC, von Messling V, Cattaneo R, et al. Engineered measles virus as a novel oncolytic therapy against prostate cancer. Prostate. 2009;69:82–91. [DOI] [PubMed] [PMC]

129.

Durso RJ, Andjelic S, Gardner JP, Margitich DJ, Donovan GP, Arrigale RR, et al. A novel alphavirus vaccine encoding prostate-specific membrane antigen elicits potent cellular and humoral immune responses. Clin Cancer Res. 2007;13:3999–4008. [DOI] [PubMed]

130.

Garcia-Hernandez Mde L, Gray A, Hubby B, Kast WM. In vivo effects of vaccination with six-transmembrane epithelial antigen of the prostate: a candidate antigen for treating prostate cancer. Cancer Res. 2007;67:1344–51. [DOI] [PubMed]

131.

Garcia-Hernandez Mde L, Gray A, Hubby B, Klinger OJ, Kast WM. Prostate stem cell antigen vaccination induces a long-term protective immune response against prostate cancer in the absence of autoimmunity. Cancer Res. 2008;68:861–9. [DOI] [PubMed]

132.

Allen C, Opyrchal M, Aderca I, Schroeder MA, Sarkaria JN, Domingo E, et al. Oncolytic measles virus strains have a significant antitumor activity against glioma stem cells. Gene Ther. 2013;20:444–9. [DOI] [PubMed] [PMC]

133.

Heikkilä JE, Vähä-Koskela MJ, Ruotsalainen JJ, Martikainen MW, Stanford MM, McCart JA, et al. Intravenously administered alphavirus vector VA7 eradicates orthotopic human glioma xenografts in nude mice. PLoS One. 2010;5:e8603. [DOI] [PubMed] [PMC]

134.

Sugiyama T, Yoneda M, Kuraishi T, Hattori S, Inoue Y, Sato H, et al. Measles virus selectively blind to signaling lymphocyte activation molecule as a novel oncolytic virus for breast cancer treatment. Gene Ther. 2013;20:338–47. [DOI] [PubMed]

135.

Määttä AM, Mäkinen K, Ketola A, Liimatainen T, Yongabi FN, Vähä-Koskela M, et al. Replication competent Semliki Forest virus prolongs survival in experimental lung cancer. Int J Cancer. 2008;123:1704–11. [DOI] [PubMed]

136.

Zhao D, Chen P, Yang H, Wu Y, Zeng X, Zhao Y, et al. Live attenuated measles virus vaccine induces apoptosis and promotes tumor regression in lung cancer. Oncol Rep. 2013;29:199–204. [DOI] [PubMed]

137.

Boisgerault N, Guillerme JB, Pouliquen D, Mesel-Lemoine M, Achard C, Combredet C, et al. Natural oncolytic activity of live-attenuated measles virus against human lung and colorectal adenocarcinomas. Biomed Res Int. 2013;2013:387362. [DOI] [PubMed] [PMC]

138.

Patel MR, Jacobson BA, Belgum H, Raza A, Sadiq A, Drees J, et al. Measles vaccine strains for virotherapy of non-small-cell lung carcinoma. J Thorac Oncol. 2014;9:1101–10. [DOI] [PubMed] [PMC]

139.

McAllister A, Arbetman AE, Mandl S, Peña-Rossi C, Andino R. Recombinant yellow fever viruses are effective therapeutic vaccines for treatment of murine experimental solid tumors and pulmonary metastases. J Virol. 2000;74:9197–205. [DOI] [PubMed] [PMC]

140.

Ammour Y, Ryabaya O, Shchetinina Y, Profokeva E, Gavrilova M, Khochenkov D, et al. The susceptibility of human melanoma cells to infection with the leningrad-16 vaccine strain of measles virus. Viruses. 2020;12:173. [DOI] [PubMed] [PMC]

141.

Kimpel J, Urbiola C, Koske I, Tober R, Banki Z, Wollmann G, et al. The oncolytic virus VSV-GP is effective against malignant melanoma. Viruses. 2018;10:108. [DOI] [PubMed] [PMC]

142.

Dold C, Rodriguez Urbiola C, Wollmann G, Egerer L, Muik A, Bellmann L, et al. Application of interferon modulators to overcome partial resistance to human ovarian cancers to VSV-GP oncolytic viral therapy. Mol Ther Oncolytics. 2016;3:16021. [DOI] [PubMed] [PMC]

143.

Murphy AM, Besmer DM, Moerdyk-Schauwecker M, Moestl N, Ornelles DA, Mukherjee P, et al. Vesicular stomatitis virus as an oncolytic agent against pancreatic ductal adenocarcinoma. J Virol. 2012;86:3073–87. Erratum in: J Virol. 2013;87:1923. [DOI] [PubMed] [PMC]

144.

Hastle E, Besmer DM, Shah NR, Murphy AM, Moredyk-Schauwecker M, Molestina C, et al. Oncolytic vesicular stomatitis virus in an immunocompetent model of MUC1-positive or MUC1-nulll pancreatic ductal adenocarcinoma. J Virol. 2013;87:10283–94. [DOI] [PubMed] [PMC]

145.

Son HA, Zhang L, Cuong BK, Van Tong H, Cuong LD, Hang NT, et al. Combination of vaccine-strain measles and mumps viruses enhances oncolytic activity against human solid malignancies. Cancer Invest. 2018;36:106–17. [DOI] [PubMed]

146.

Zhao X, Huang S, Luo H, Wan X, Gui Y, Li J, et al. Evaluation of vesicular stomatitis virus mutant as an oncolytic agent against prostate cancer. Int J Clin Exp Med. 2014;7:1204–13. [PubMed] [PMC]

147.

Urbiola C, Santer FR, Petersson M, van der Pluijm G, Horninger W, Erlmann P, et al. Oncolytic activity of the rhabdovirus VSV-GP against prostate cancer. Int J Cancer. 2018;143:1786–96. [DOI] [PubMed] [PMC]

148.

Ying H, Zaks TZ, Wang RF, Irvine KR, Kammula US, Marincola FM, et al. Cancer therapy using a self-replicating RNA vaccine. Nat Med. 1999;5:823–7. [DOI] [PubMed] [PMC]

149.

Anraku I, Harvey TJ, Linedale R, Gardner J, Harrich D, Suhrbier A, et al. Kunjin virus replicon vaccine vectors induce protective CD8⁺ T-cell immunity. J Virol. 2002;76:3791–9. [DOI] [PubMed] [PMC]

150.

Yamanaka R, Xanthopoulos KG. Induction of antigen-specific immune responses against malignant brain tumors by intramuscular injection of sindbis DNA encoding gp100 and IL-18. DNA Cell Biol. 2005;24:317–24. [DOI] [PubMed]

151.

Wang X, Wang JP, Rao XM, Price JE, Zhou HS, Lachman LB. Prime-boost vaccination with plasmid and adenovirus gene vaccines control HER2/neu⁺ metastatic breast cancer in mice. Breast Cancer Res. 2005;7:R580–8. [DOI] [PubMed] [PMC]

152.

Lachman LB, Rao XM, Kremer RH, Ozpolat B, Kirjakova G, Price JE. DNA vaccination against neu reduces breast cancer incidence and metastasis in mice. Cancer Gene Ther. 2001;8:259–68. [DOI] [PubMed]

153.

van de Wall S, Ljungberg K, Ip PP, Boerma A, Knudsen ML, Nijman HW, et al. Potent therapeutic efficacy of an alphavirus replicon DNA vaccine expressing human papilloma virus E6 and E7 antigens. Oncoimmunology. 2018;7:e1487913. [DOI] [PubMed] [PMC]

154.

Yin X, Wang W, Zhu X, Wang Y, Wu S, Wang Z, et al. Synergistic antitumor efficacy of combined DNA vaccines targeting tumor cells and angiogenesis. Biochem Biophys Res Commun. 2015;465:239–44. [DOI] [PubMed]

155.

Crosby EJ, Gwin W, Blackwell K, Marcom PK, Chang S, Maecker HT, et al. Vaccine-induced memory CD8⁺ T cells provide clinical benefit in HER2 expressing breast cancer: a mouse to human translational study. Clin Cancer Res. 2019;25:2725–36. [DOI] [PubMed] [PMC]

156.

Crosby EJ, Hobeika AC, Niedzweicki D, Rushing C, Hsu D, Berglund P, et al. Long-term survival of patients with stage III colon cancer treated with VRP-CEA(6D), an alphavirus vector that increases the CD8⁺ effector memory T cell to Treg ration. J Immunother Cancer. 2020;8:e001662. [DOI] [PubMed] [PMC]

157.

Komdeur FL, Singh A, van de Wall S, Meulenberg JJM, Boerma A, Hoogeboom BN, et al. First-in-human phase I clinical trial of an SFV-Based RNA replicon cancer vaccine against HPV-induced cancers. Mol Ther. 2021;29:611–25. [DOI] [PubMed] [PMC]

158.

Galanis E, Hartmann LC, Cliby WA, Long HJ, Peethambaram PP, Barrette BA, et al. Phase I trial of intraperitoneal administration of an oncolytic measles virus strain engineered to express carcinoembryonic antigen for recurrent ovarian cancer. Cancer Res. 2010;70:875–82. [DOI] [PubMed] [PMC]

159.

Morse MA, Hobelka AC, Osada T, Berglund P, Hubby B, Negri S, et al. An alphavirus vector overcomes the presence of neutralizing antibodies and elevated numbers of Tregs to induce immune responses in humans with advanced cancer. J Clin Invest. 2010;120:3234–41. [DOI] [PubMed] [PMC]

160.

Slovin SF, Kehoe M, Durso R, Fernandez C, Olson W, Gao JP, et al. A phase I dose escalation trial of vaccine replicon particles (VRP) expressing prostate-specific membrane antigen (PSMA) in subjects with prostate cancer. Vaccine. 2013;31:943–9. [DOI] [PubMed]