Role of innate signalling pathways in the immunogenicity of alphaviral replicon-based vaccines

Virology Journal

Volumn 8, Issue , 2011, Pages

  Näslund, Tanja I ^a   Kostic, Linda ^b   Nordström, Eva K L ^b,c   Chen, Margaret ^a,b   Liljeström, Peter ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c BioArctic Neuroscience   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA VIRAL REPLICON VECTOR; CYTOKINE; INTERFERON; INTERFERON REGULATORY FACTOR 3; MYELOID DIFFERENTIATION FACTOR 88; OVALBUMIN; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS VECTOR; DRUG CARRIER; VIRUS VACCINE;

ALPHA VIRUS; ANIMAL CELL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; IMMUNOGENICITY; INNATE IMMUNITY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIMARY IMMUNE RESPONSE; REPLICON; SIGNAL TRANSDUCTION; VIRUS PARTICLE; ANIMAL; GENE VECTOR; GENETICS; IMMUNOLOGY; MOUSE MUTANT;

MUS;

ALPHAVIRUS; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DRUG CARRIERS; FEMALE; GENETIC VECTORS; IMMUNITY, INNATE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; VIRAL VACCINES;

EID: 78751644761     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-8-36     Document Type: Article

References (69)

1. Driver DA, Latham EM, Polo JM, Belli BA, Banks TA, Chada S, Brumm D, Chang SM, Mento SJ, Jolly DJ, et al: Layered amplification of gene expression with a DNA gene delivery system. Ann N Y Acad Sci 1995, 772:261-264. (Pubitemid 26078788)
2. Herweijer H, Latendresse JS, Williams P, Zhang G, Danko I, Schlesinger S, Wolff JA: A plasmid-based self-amplifying Sindbis virus vector. Hum Gene Ther 1995, 6:1161-1167.
3. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, Alexopoulou L, Azuma YT, Flavell RA, Liljestrom P, Reis e Sousa C: Toll-like receptor 3 promotes cross-priming to virus-infected cells. Nature 2005, 433:887-892. (Pubitemid 40314900)
4. Atkins GJ, Fleeton MN, Sheahan BJ: Therapeutic and prophylactic applications of alphavirus vectors. Expert Rev Mol Med 2008, 10:e33.
5. Zhou X, Berglund P, Zhao H, Liljeström P, Jondal M: Generation of cytotoxic and humoral immune responses by nonreplicative recombinant Semliki Forest virus. Proc Natl Acad Sci USA 1995, 92:3009-3013.
6. Berglund P, Fleeton MN, Smerdou C, Liljeström P: Immunization with recombinant Semliki Forest virus induces protection against influenza challenge in mice. Vaccine 1999, 17:497-507. (Pubitemid 29064008)
7. Fleeton MN, Chen M, Berglund P, Rhodes G, Parker SE, Murphy M, Atkins GJ, Liljeström P: Self-replicative RNA vaccines elicit protection against influenza A virus, respiratory syncytial virus, and a tickborne encephalitis virus. J Infect Dis 2001, 183:1395-1398. (Pubitemid 32337123)
8. Chen M, Hu KF, Rozell B, Orvell C, Morein B, Liljeström P: Vaccination with recombinant alphavirus or immune-stimulating complex antigen against respiratory syncytial virus. J Immunol 2002, 169:3208-3216. (Pubitemid 35013167)
9. Hanke T, Barnfield C, Wee EG, Agren L, Samuel RV, Larke N, Liljeström P: Construction and immunogenicity in a prime-boost regimen of a Semliki Forest virus-vectored experimental HIV clade A vaccine. J Gen Virol 2003, 84:361-368. (Pubitemid 36175710)
10. Sundbäck M, Douagi I, Dayaraj C, Forsell MN, Nordstrom EK, McInerney GM, Spångberg K, Tjäder L, Bonin E, Sundström M, et al: Efficient expansion of HIV-1-specific T cell responses by homologous immunization with recombinant Semliki Forest virus particles. Virology 2005, 341:190-202. (Pubitemid 41416729)
11. Querec TD, Pulendran B: Understanding the role of innate immunity in the mechanism of action of the live attenuated Yellow Fever Vaccine 17D. Adv Exp Med Biol 2007, 590:43-53.
12. Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, et al: Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 2009, 10:116-25.
13. Pichlmair A, Reis e Sousa C: Innate recognition of viruses. Immunity 2007, 27:370-383. (Pubitemid 47418682)
14. Zhou S, Kurt-Jones EA, Mandell L, Cerny A, Chan M, Golenbock DT, Finberg RW: MyD88 is critical for the development of innate and adaptive immunity during acute lymphocytic choriomeningitis virus infection. Eur J Immunol 2005, 35:822-830. (Pubitemid 40425538)
15. Chen M, Barnfield C, Näslund TI, Fleeton MN, Liljeström P: MyD88 expression is required for efficient cross-presentation of viral antigens from infected cells. J Virol 2005, 79:2964-2972. (Pubitemid 40270575)
16. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T: IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434:772-777. (Pubitemid 44739521)
17. Hidmark AS, Nordström EK, Dosenovic P, Forsell MN, Liljeström P, Karlsson Hedestam GB: Humoral responses against coimmunized protein antigen but not against alphavirus-encoded antigens require alpha/beta interferon signaling. J Virol 2006, 80:7100-7110. (Pubitemid 44025206)
18. Le Bon A, Etchart N, Rossmann C, Ashton M, Hou S, Gewert D, Borrow P, Tough DF: Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat Immunol 2003, 4:1009-1015. (Pubitemid 37265922)
19. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF: Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 2001, 14:461-470. (Pubitemid 32441598)
20. Le Bon A, Durand V, Kamphuis E, Thompson C, Bulfone-Paus S, Rossmann C, Kalinke U, Tough DF: Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during cross-priming. J Immunol 2006, 176:4682-4689.
21. Le Bon A, Thompson C, Kamphuis E, Durand V, Rossmann C, Kalinke U, Tough DF: Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J Immunol 2006, 176:2074-2078. (Pubitemid 43201653)
22. Hidmark AS, McInerney GM, Nordström EK, Douagi I, Werner KM, Liljeström P, Karlsson Hedestam GB: Early alpha/beta interferon production by myeloid dendritic cells in response to UV-inactivated virus requires viral entry and interferon regulatory factor 3 but not MyD88. J Virol 2005, 79:10376-10385. (Pubitemid 41098578)
23. Sandström E, Nilsson C, Hejdeman B, Bråve A, Bratt G, Robb M, Cox J, Vancott T, Marovich M, Stout R, et al: Broad immunogenicity of a multigene, multiclade HIV-1 DNA vaccine boosted with heterologous HIV-1 recombinant modified vaccinia virus Ankara. J Infect Dis 2008, 198:1482-1490.
24. Lu S, Wang S, Grimes-Serrano JM: Current progress of DNA vaccine studies in humans. Expert Rev Vaccines 2008, 7:175-191. (Pubitemid 351357954)
25. Harari A, Bart PA, Stohr W, Tapia G, Garcia M, Medjitna-Rais E, Burnet S, Cellerai C, Erlwein O, Barber T, et al: An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J Exp Med 2008, 205:63-77. (Pubitemid 351185716)
26. Takaoka A, Taniguchi T: Cytosolic DNA recognition for triggering innate immune responses. Adv Drug Deliv Rev 2008, 60:847-857.
27. Kumagai Y, Takeuchi O, Akira S: TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliv Rev 2008, 60:795-804.
28. Sasaki S, Amara RR, Oran AE, Smith JM, Robinson HL: Apoptosis-mediated enhancement of DNA-raised immune responses by mutant caspases. Nat Biotechnol 2001, 19:543-547. (Pubitemid 32521185)
29. Chattergoon MA, Kim JJ, Yang JS, Robinson TM, Lee DJ, Dentchev T, Wilson DM, Ayyavoo V, Weiner DB: Targeted antigen delivery to antigen-presenting cells including dendritic cells by engineered Fas-mediated apoptosis. Nat Biotechnol 2000, 18:974-979. (Pubitemid 32977379)
30. Chattergoon MA, Muthumani K, Tamura Y, Ramanathan M, Shames JP, Saulino V, Robinson TM, Montaner LJ, Weiner DB: DR5 Activation of Caspase-8 Induces DC Maturation and Immune Enhancement In Vivo. Mol Ther 2008, 16:419-426. (Pubitemid 351168052)
31. Sasaki S, Amara RR, Yeow WS, Pitha PM, Robinson HL: Regulation of DNA-raised immune responses by cotransfected interferon regulatory factors. J Virol 2002, 76:6652-6659. (Pubitemid 34633531)
32. Berglund P, Smerdou C, Fleeton MN, Tubulekas I, Liljeström P: Enhancing immune responses using suicidal DNA vaccines. Nat Biotechnol 1998, 16:562-565. (Pubitemid 28269815)
33. Nordström EK, Forsell MN, Barnfield C, Bonin E, Hanke T, Sundström M, Karlsson GB, Liljeström P: Enhanced immunogenicity using an alphavirus replicon DNA vaccine against human immunodeficiency virus type 1. J Gen Virol 2005, 86:349-354.
34. Hariharan MJ, Driver DA, Townsend K, Brumm D, Polo JM, Belli BA, Catton DJ, Hsu D, Mittelstaedt D, McCormack JE, et al: DNA immunization against herpes simplex virus: enhanced efficacy using a Sindbis virusbased vector. J Virol 1998, 72:950-958. (Pubitemid 28116872)
35. Leitner WW, Ying H, Driver DA, Dubensky TW, Restifo NP: Enhancement of tumor-specific immune response with plasmid DNA replicon vectors. Cancer Res 2000, 60:51-55. (Pubitemid 30058729)
36. Ljungberg K, Whitmore AC, Fluet ME, Moran TP, Shabman RS, Collier ML, Kraus AA, Thompson JM, Montefiori DC, Beard C, Johnston RE: Increased immunogenicity of a DNA-launched Venezuelan equine encephalitis virus-based replicon DNA vaccine. J Virol 2007, 81:13412-13423. (Pubitemid 350247838)
37. Lundstrom K: Alphavirus-based vaccines. Curr Opin Mol Ther 2002, 4:28-34.
38. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S: Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998, 9:143-150. (Pubitemid 28361303)
39. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T: Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13:539-548.
40. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M: Functional role of type I and type II interferons in antiviral defense. Science 1994, 264:1918-1921. (Pubitemid 24245635)
41. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of doublestranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413:732-738. (Pubitemid 33009951)
42. Smerdou C, Liljeström P: Two-helper RNA system for production of recombinant Semliki forest virus particles. J Virol 1999, 73:1092-1098. (Pubitemid 29036760)
43. Leitner WW, Hwang LN, deVeer MJ, Zhou A, Silverman RH, Williams BR, Dubensky TW, Ying H, Restifo NP: Alphavirus-based DNA vaccine breaks immunological tolerance by activating innate antiviral pathways. Nat Med 2003, 9:33-39. (Pubitemid 36098257)
44. Pichlmair A, Schulz O, Tan CP, Rehwinkel J, Kato H, Takeuchi O, Akira S, Way M, Schiavo G, Reis e Sousa C: Activation of MDA5 requires higher-order RNA structures generated during virus infection. J Virol 2009, 83:10761-10769.
45. Bracci L, La Sorsa V, Belardelli F, Proietti E: Type I interferons as vaccine adjuvants against infectious diseases and cancer. Expert Rev Vaccines 2008, 7:373-381. (Pubitemid 351520025)
46. Bramson JL, Dayball K, Hall JR, Millar JB, Miller M, Wan YH, Lin R, Hiscott J: Super-activated interferon-regulatory factors can enhance plasmid immunization. Vaccine 2003, 21:1363-1370. (Pubitemid 36263177)
47. Kwissa M, Amara RR, Robinson HL, Moss B, Alkan S, Jabbar A, Villinger F, Pulendran B: Adjuvanting a DNA vaccine with a TLR9 ligand plus Flt3 ligand results in enhanced cellular immunity against the simian immunodeficiency virus. J Exp Med 2007, 204:2733-2746. (Pubitemid 350044795)
48. Zhang X, Sun S, Hwang I, Tough DF, Sprent J: Potent and selective stimulation of memory-phenotype CD8+ T cells in vivo by IL-15. Immunity 1998, 8:591-599. (Pubitemid 28264750)
49. Marrack P, Kappler J, Mitchell T: Type I interferons keep activated T cells alive. J Exp Med 1999, 189:521-530.
50. Diebold SS, Schulz O, Alexopoulou L, Leitner WW, Flavell RA, Reis ESC: Role of TLR3 in the immunogenicity of replicon plasmid-based vaccines. Gene Ther 2008.
51. Paun A, Pitha PM: The IRF family, revisited. Biochimie 2007, 89:744-753. (Pubitemid 47001634)
52. Tamura T, Yanai H, Savitsky D, Taniguchi T: The IRF family transcription factors in immunity and oncogenesis. Annu Rev Immunol 2008, 26:535-584. (Pubitemid 351600385)
53. White L, Sali T, Alvarado D, Gatti E, Pierre P, Streblow D, Defilippis VR: Chikungunya Virus Induces IPS-1-Dependent Innate Immune Activation and PKR-Independent Translational Shutoff. J Virol 2011, 85:606-20.
54. Rhee EG, Blattman JN, Kasturi SP, Kelley RP, Kaufman DR, Lynch DM, La Porte A, Simmons NL, Clark SL, Pulendran B, et al: Multiple Innate Immune Pathways Contribute to the Immunogenicity of Recombinant Adenoviral Vaccine Vectors. J Virol 2011, 85:315-23.
55. Pugachev KV, Guirakhoo F, Monath TP: New developments in flavivirus vaccines with special attention to yellow fever. Curr Opin Infect Dis 2005, 18:387-394. (Pubitemid 41345295)
56. Leitner WW, Bergmann-Leitner ES, Hwang LN, Restifo NP: Type I Interferons are essential for the efficacy of replicase-based DNA vaccines. Vaccine 2006, 24:5110-5118. (Pubitemid 43818199)
57. Gehring S, Gregory SH, Kuzushita N, Wands JR: Type 1 interferon augments DNA-based vaccination against hepatitis C virus core protein. J Med Virol 2005, 75:249-257. (Pubitemid 40053736)
58. Sellins K, Fradkin L, Liggitt D, Dow S: Type I interferons potently suppress gene expression following gene delivery using liposome(-)DNA complexes. Mol Ther 2005, 12:451-459. (Pubitemid 41150130)
59. Liljeström P, Garoff H: Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J Virol 1991, 65:147-154.
60. Liljeström P, Garoff H: A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (N Y) 1991, 9:1356-1361.
61. McInerney GM, Kedersha NL, Kaufman RJ, Anderson P, Liljestrom P: Importance of eIF2alpha phosphorylation and stress granule assembly in alphavirus translation regulation. Mol Biol Cell 2005, 16:3753-3763. (Pubitemid 41077084)
62. Breakwell L, Dosenovic P, Karlsson Hedestam GB, D'Amato M, Liljeström P, Fazakerley J, McInerney GM: Semliki Forest virus nonstructural protein 2 is involved in suppression of the type I interferon response. J Virol 2007, 81:8677-8684. (Pubitemid 47242841)
63. Fros JJ, Liu WJ, Prow NA, Geertsema C, Ligtenberg M, Vanlandingham DL, Schnettler E, Vlak JM, Suhrbier A, Khromykh AA, Pijlman GP: Chikungunya virus nonstructural protein 2 inhibits type I/II interferon-stimulated JAKSTAT signaling. J Virol 2010, 84:10877-10887.
64. Lemke G, Rothlin CV: Immunobiology of the TAM receptors. Nat Rev Immunol 2008, 8:327-336. (Pubitemid 351595219)
65. Tovey MG, Lallemand C, Thyphronitis G: Adjuvant activity of type I interferons. Biol Chem 2008, 389:541-545. (Pubitemid 351874185)
66. Ying H, Zaks TZ, Wang RF, Irvine KR, Kammula US, Marincola FM, Leitner WW, Restifo NP: Cancer therapy using a self-replicating RNA vaccine. Nat Med 1999, 5:823-827. (Pubitemid 29318618)
67. Leitner WW, Hwang LN, Bergmann-Leitner ES, Finkelstein SE, Frank S, Restifo NP: Apoptosis is essential for the increased efficacy of alphaviral replicase-based DNA vaccines. Vaccine 2004, 22:1537-1544. (Pubitemid 38446932)
68. Bergmann-Leitner ES, Leitner WW, Duncan EH, Savranskaya T, Angov E: Molecular adjuvants for malaria DNA vaccines based on the modulation of host-cell apoptosis. Vaccine 2009, 27:5700-5708.
69. Rhee EG, Kelley RP, Agarwal I, Lynch DM, La Porte A, Simmons NL, Clark SL, Barouch DH: TLR4 ligands augment antigen-specific CD8+ T lymphocyte responses elicited by a viral vaccine vector. J Virol 2010, 84:10413-10419.