Acute infection with Venezuelan equine encephalitis virus replicon particles catalyzes a systemic antiviral state and protects from lethal virus challenge

Journal of Virology

Volumn 83, Issue 23, 2009, Pages 12432-12442

  Konopka, Jennifer L ^a,b   Thompson, Joseph M ^a,b,c   Whitmore, Alan C ^b   Webb, Drue L ^a,b   Johnston, Robert E ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON RECEPTOR; INTERFERON REGULATORY FACTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS REPLICON PARTICLE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; BRAIN; BRAIN INFECTION; CONTROLLED STUDY; FEMALE; FOOT PAD; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNITY; INFLUENZA VIRUS; INNATE IMMUNITY; LIVER; LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON; SIGNAL TRANSDUCTION; SURVIVAL TIME; TISSUE DISTRIBUTION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VESICULAR STOMATITIS VIRUS; VIREMIA; VIRUS ACTIVATION; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TITRATION;

ANIMALS; BRAIN; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; ENCEPHALOMYELITIS, VENEZUELAN EQUINE; FEMALE; GENE EXPRESSION PROFILING; IMMUNITY, INNATE; INTERFERONS; LIVER; LYMPH NODES; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; RHABDOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS;

ANIMALIA; MURINAE; MUS; ORTHOMYXOVIRIDAE; VENEZUELAN EQUINE ENCEPHALITIS VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 70450187302     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00564-09     Document Type: Article

References (74)

1. Alsharifi, M., M. Regner, R. Blanden, M. Lobigs, E. Lee, A. Koskinen, and A. Mullbacher. 2006. Exhaustion of type I interferon response following an acute viral infection. J. Immunol. 177:3235-3241. (Pubitemid 44277842)
2. Anishchenko, M., S. Paessler, I. P. Greene, P. V. Aguilar, A.-S. Carrara, and S. C. Weaver. 2004. Generation and characterization of closely related epizootic and enzootic infectious cDNA clones for studying interferon sensitivity and emergence mechanisms of Venezuelan equine encephalitis virus. J. Virol. 78:1-8. (Pubitemid 37549714)
3. Aronson, J. F., F. B. Grieder, N. L. Davis, P. C. Charles, T. Knott, K. Brown, and R. E. Johnston. 2000. A single-site mutant and revertants arising in vivo define early steps in the pathogenesis of Venezuelan equine encephalitis virus. Virology 270:111-123.
4. Barna, M., T. Komatsu, Z. Bi, and C. S. Reiss. 1996. Sex differences in susceptibility to viral infection of the central nervous system. J. Neuroimmunol. 67:31-39. (Pubitemid 26245701)
5. Bennett, A. M., S. J. Elvin, A. J. Wright, S. M. Jones, and R. J. Phillpotts. 2000. An immunological profile of Balb/c mice protected from airborne challenge following vaccination with a live attenuated Venezuelan equine encephalitis virus vaccine. Vaccine 19:337-347.
6. Bernard, K. A., W. B. Klimstra, and R. E. Johnston. 2000. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93-103.
7. Bi, Z., M. Barna, T. Komatsu, and C. S. Reiss. 1995. Vesicular stomatitis virus infection of the central nervous system activates both innate and acquired immunity. J. Virol. 69:6466-6472.
8. Bradish, C. J., and D. Titmuss. 1981. The effects of interferon and double-stranded RNA upon the virus-host interaction: studies with togavirus strains in mice. J. Gen. Virol. 53:21-30.
9. Brave, A., K. Ljungberg, B. Wahren, and M. A. Liu. 2007. Vaccine delivery methods using viral vectors. Mol. Pharm. 4:18-32.
10. Casals, J., S. M. Buckley, and D. W. Barry. 1973. Resistance to arbovirus challenge in mice immediately after vaccination. Appl. Microbiol. 25:755-762.
11. Charles, P. C., K. W. Brown, N. L. Davis, M. K. Hart, and R. E. Johnston. 1997. Mucosal immunity induced by parenteral immunization with a live attenuated Venezuelan equine encephalitis virus vaccine candidate. Virology 228:153-160.
12. Charles, P. C., J. Trgovcich, N. L. Davis, and R. E. Johnston. 2001. Immunopathogenesis and immune modulation of Venezuelan equine encephalitis virus-induced disease in the mouse. Virology 284:190-202.
13. Charles, P. C., E. Walters, F. Margolis, and R. E. Johnston. 1995. Mechanism of neuroinvasion of Venezuelan equine encephalitis virus in the mouse. Virology 208:662-671.
14. Davis, N. L., F. B. Grieder, J. F. Smith, G. F. Greenwald, M. L. Valenski, D. C. Sellon, P. C. Charles, and R. E. Johnston. 1994. A molecular genetic approach to the study of Venezuelan equine encephalitis virus pathogenesis. Arch. Virol. Suppl. 9:99-109.
15. Davis, N. L., N. Powell, G. F. Greenwald, L. V. Willis, B. J. Johnson, J. F. Smith, and R. E. Johnston. 1991. Attenuating mutations in the E2 glycoprotein gene of Venezuelan equine encephalitis virus: construction of single and multiple mutants in a full-length cDNA clone. Virology 183:20-31.
16. Davis, N. L., A. West, E. Reap, G. MacDonald, M. Collier, S. Dryga, M. Maughan, M. Connell, C. Walker, K. McGrath, C. Cecil, L. H. Ping, J. Frelinger, R. Olmsted, P. Keith, R. Swanstrom, C. Williamson, P. Johnson, D. Montefiori, and R. E. Johnston. 2002. Alphavirus replicon particles as candidate HIV vaccines. IUBMB Life 53:209-211.
17. Davis, N. L., L. V. Willis, J. F. Smith, and R. E. Johnston. 1989. In vitro synthesis of infectious Venezuelan equine encephalitis virus RNA from a cDNA clone: analysis of a viable deletion mutant. Virology 171:189-204.
18. Durbin, J. E., A. Fernandez-Sesma, C.-K. Lee, T. D. Rao, A. B. Frey, T. M. Moran, S. Vukmanovic, A. Garcia-Sastre, and D. E. Levy. 2000. Type I IFN modulates innate and specific antiviral immunity. J. Immunol. 164:4220-4228.
19. Durbin, R. K., S. E. Mertz, A. E. Koromilas, and J. E. Durbin. 2002. PKR protection against intranasal vesicular stomatitis virus infection is mouse strain dependent. Viral Immunol. 15:41-51.
20. d system. J. Virol. 65:4950-4958.
21. Garcia-Sastre, A., R. K. Durbin, H. Zheng, P. Palese, R. Gertner, D. E. Levy, and J. E. Durbin. 1998. The role of interferon in influenza virus tissue tropism. J. Virol. 72:8550-8558. (Pubitemid 28471792)
22. Gleiser, C. A., W. S. Gochenour, Jr., T. O. Berge, and W. D. Tigertt. 1962. The comparative pathology of experimental Venezuelan equine encephalomyelitis infection in different animal hosts. J. Infect. Dis. 110:80-97.
23. Greene, I. P., S. Paessler, L. Austgen, M. Anishchenko, A. C. Brault, R. A. Bowen, and S. C. Weaver. 2005. Envelope glycoprotein mutations mediate equine amplification and virulence of epizootic Venezuelan equine encephalitis virus. J. Virol. 79:9128-9133. (Pubitemid 40934824)
24. Greenway, T. E., J. H. Eldridge, G. Ludwig, J. K. Staas, J. F. Smith, R. M. Gilley, and S. M. Michalek. 1998. Induction of protective immune responses against Venezuelan equine encephalitis (VEE) virus aerosol challenge with microencapsulated VEE virus vaccine. Vaccine 16:1314-1323.
25. Gresser, I. 1984. Role of interferon in resistance to viral infection in vivo, p. 221-247. In J. Vilcek and E. De Maeyer (ed.), Interferon: interferons and the immune system, vol.2. Elsevier Science, Amsterdam, The Netherlands.
26. Grieder, F. B., B. K. Davis, X. D. Zhou, S. J. Chen, F. D. Finkelman, and W. C. Gause. 1997. Kinetics of cytokine expression and regulation of host protection following infection with molecularly cloned Venezuelan equine encephalitis virus. Virology 233:302-312.
27. Grieder, F. B., N. L. Davis, J. F. Aronson, P. C. Charles, D. C. Sellon, K. Suzuki, and R. E. Johnston. 1995. Specific restrictions in the progression of Venezuelan equine encephalitis virus-induced disease resulting from single amino acid changes in the glycoproteins. Virology 206:994-1006.
28. Grieder, F. B., and S. N. Vogel. 1999. Role of interferon and interferon regulatory factors in early protection against Venezuelan equine encephalitis virus infection. Virology 257:106-118.
29. Hart, M. K., W. Pratt, F. Panelo, R. Tammariello, and M. Dertzbaugh. 1997. Venezuelan equine encephalitis virus vaccines induce mucosal IgA responses and protection from airborne infection in BALB/c, but not C3H/HeN mice. Vaccine 15:363-369.
30. Hui, D. J., F. Terenzi, W. C. Merrick, and G. C. Sen. 2005. Mouse p56 blocks a distinct function of eukaryotic initiation factor 3 in translation initiation. J. Biol. Chem. 280:3433-3440.
31. Huneycutt, B. S., Z. Bi, C. J. Aoki, and C. S. Reiss. 1993. Central neuropathogenesis of vesicular stomatitis virus infection of immunodeficient mice. J. Virol. 67:6698-6706.
32. Huneycutt, B. S., I. V. Plakhov, Z. Shusterman, S. M. Bartido, A. Huang, C. S. Reiss, and C. Aoki. 1994. Distribution of vesicular stomatitis virus proteins in the brains of BALB/c mice following intranasal inoculation: an immunohistochemical analysis. Brain Res. 635:81-95.
33. Huprikar, J., M. C. Dal Canto, and S. G. Rabinowitz. 1990. Protection against lethal Venezuelan equine encephalitis (VEE) virus infection by cell-free supernatant obtained from immune spleen cells. J. Neurol. Sci. 97:143-153.
34. Jahrling, P. B., E. Navarro, and W. F. Scherer. 1976. Interferon induction and sensitivity as correlates to virulence of Venezuelan encephalitis viruses for hamsters. Arch. Virol. 51:23-35.
35. Johnson, B. J., R. M. Kinney, C. L. Kost, and D. W. Trent. 1986. Molecular determinants of alphavirus neurovirulence: nucleotide and deduced protein sequence changes during attenuation of Venezuelan equine encephalitis virus. J. Gen. Virol. 67:1951-1960.
36. Johnston, L. J., G. M. Halliday, and N. J. C. King. 2000. Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus. J. Investig. Dermatol. 114:560-568.
37. Jordan, G. W. 1973. Interferon sensitivity of Venezuelan equine encephalomyelitis virus. Infect. Immun. 7:911-917.
38. Katze, M. G., Y. He, and M. Gale, Jr. 2002. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2:675-687.
39. Konopka, J. L., L. O. Penalva, J. M. Thompson, L. J. White, C. W. Beard, J. D. Keene, and R. E. Johnston. 2007. A two-phase innate host response to alphavirus infection identified by mRNP-tagging in vivo. PLoS Pathog. 3:e199.
40. Laust, A. K., B. W. Sur, K. Wang, B. Hubby, J. F. Smith, and E. L. Nelson. 2007. VRP immunotherapy targeting neu: treatment efficacy and evidence for immunoediting in a stringent rat mammary tumor model. Breast Cancer Res. Treat. 106:371-382.
41. Letchworth, G. J., L. L. Rodriguez, and J. Del cbarrera. 1999. Vesicular stomatitis. Vet. J. 157:239-260.
42. Lukaszewski, R. A., and T. J. G. Brooks. 2000. Pegylated alpha interferon is an effective treatment for virulent Venezuelan equine encephalitis virus and has profound effects on the host immune response to infection. J. Virol. 74:5006-5015.
43. Lundstrom, K. 2003. Alphavirus vectors for vaccine production and gene therapy. Expert Rev. Vaccines 2:447-459. (Pubitemid 36713370)
44. MacDonald, G. H., and R. E. Johnston. 2000. Role of dendritic cell targeting in Venezuelan equine encephalitis virus pathogenesis. J. Virol. 74:914-922.
45. Malmgaard, L. 2004. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24:439-454. (Pubitemid 39120592)
46. Marcus, P. I., L. L. Rodriguez, and M. J. Sekellick. 1998. Interferon induction as a quasispecies marker of vesicular stomatitis virus populations. J. Virol. 72:542-549.
47. Perry, A. K., G. Chen, D. Zheng, H. Tang, and G. Cheng. 2005. The host type I interferon response to viral and bacterial infections. Cell Res. 15:407-422.
48. Pinto, A. J., P. S. Morahan, and M. A. Brinton. 1988. Comparative study of various immunomodulators for macrophage and natural killer cell activation and antiviral efficacy against exotic RNA viruses. Int. J. Immunopharmacol. 10:197-209.
49. Pittman, P. R., R. S. Makuch, J. A. Mangiafico, T. L. Cannon, P. H. Gibbs, and C. J. Peters. 1996. Long-term duration of detectable neutralizing antibodies after administration of live-attenuated VEE vaccine and following booster vaccination with inactivated VEE vaccine. Vaccine 14:337-343.
50. Polo, J. M., J. P. Gardner, Y. Ji, B. A. Belli, D. A. Driver, S. Sherrill, S. Perri, M. A. Liu, and T. W. Dubensky, Jr. 2000. Alphavirus DNA and particle replicons for vaccines and gene therapy. Dev. Biol. (Basel) 104:181-185.
51. Pushko, P., M. Parker, G. V. Ludwig, N. L. Davis, R. E. Johnston, and J. F. Smith. 1997. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus: expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology 239:389-401. (Pubitemid 28105644)
52. Rayner, J. O., S. A. Dryga, and K. I. Kamrud. 2002. Alphavirus vectors and vaccination. Rev. Med. Virol. 12:279-296.
53. Reiss, C. S., I. V. Plakhov, and T. Komatsu. 1998. Viral replication in olfactory receptor neurons and entry into the olfactory bulb and brain. Ann. N. Y. Acad. Sci. 855:751-761.
54. Riezebos-Brilman, A., A. de Mare, L. Bungener, A. Huckriede, J. Wilschut, and T. Daemen. 2006. Recombinant alphaviruses as vectors for anti-tumour and anti-microbial immunotherapy. J. Clin. Virol. 35:233-243.
55. Rivas, F., L. A. Diaz, V. M. Cardenas, E. Daza, L. Bruzon, A. Alcala, O. De la Hoz, F. M. Caceres, G. Aristizabal, J. W. Martinez, D. Revelo, F. De la Hoz, J. Boshell, T. Camacho, L. Calderon, V. A. Olano, L. I. Villarreal, D. Roselli, G. Alvarez, G. Ludwig, and T. Tsai. 1997. Epidemic Venezuelan equine encephalitis in La Guajira, Colombia, 1995. J. Infect. Dis. 175:828-832.
56. Rose, J. K., and M. A. Whitt. 2001. Rhabdoviridae: the viruses and their replication, p. 1221-1244. In D. M. Knipe, B. N. Fields, and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
57. Ryman, K. D., L. J. White, R. E. Johnston, and W. B. Klimstra. 2002. Effects of PKR/RNase L-dependent and alternative antiviral pathways on alphavirus replication and pathogenesis. Viral Immunol. 15:53-76.
58. Sabin, A. B., and P. K. Olitsky. 1937. Influence of host factors on neuroinvasiveness of vesicular stomatitis virus. I. Effect of age on the invasion of the brain by virus instilled in the nose. J. Exp. Med. 66:15-34.
59. Samuel, C. E. 1991. Antiviral actions of interferon. Interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology 183:1-11.
60. Schoneboom, B. A., K. M. K. Catlin, A. M. Marty, and F. B. Grieder. 2000. Inflammation is a component of neurodegeneration in response to Venezuelan equine encephalitis virus infection in mice. J. Neuroimmunol. 109:132-146.
61. Schoneboom, B. A., J. S. Lee, and F. B. Grieder. 2000. Early expression of IFN-alpha/beta and iNOS in the brains of Venezuelan equine encephalitis virus-infected mice. J. Interferon Cytokine Res. 20:205-216.
62. Sen, G. C. 2001. Viruses and interferons. Annu. Rev. Microbiol. 55:255-281.
63. Shabman, R. S., T. E. Morrison, C. Moore, L. White, M. S. Suthar, L. Hueston, N. Rulli, B. Lidbury, J. P.-Y. Ting, S. Mahalingam, and M. T. Heise. 2007. Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J. Virol. 81:237-247.
64. Spotts, D. R., R. M. Reich, M. A. Kalkhan, R. M. Kinney, and J. T. Roehrig. 1998. Resistance to alpha/beta interferons correlates with the epizootic and virulence potential of Venezuelan equine encephalitis viruses and is determined by the 5′ noncoding region and glycoproteins. J. Virol. 72:10286-10291.
65. Steinhoff, U., U. Muller, A. Schertler, H. Hengartner, M. Aguet, and R. M. Zinkernagel. 1995. Antiviral protection by vesicular stomatitis virus-specific antibodies in alpha/beta interferon receptor-deficient mice. J. Virol. 69:2153-2158.
66. Stetson, D. B., and R. Medzhitov. 2006. Type I interferons in host defense. Immunity 25:373-381.
67. Terenzi, F., S. Pal, and G. C. Sen. 2005. Induction and mode of action of the viral stress-inducible murine proteins, P56 and P54. Virology 340:116-124. (Pubitemid 41191183)
68. Thompson, J. M., M. G. Nicholson, A. C. Whitmore, M. Zamora, A. West, A. Iwasaki, H. F. Staats, and R. E. Johnston. 2008. Nonmucosal alphavirus vaccination stimulates a mucosal inductive environment in the peripheral draining lymph node. J. Immunol. 181:574-585.
69. Thompson, J. M., A. C. Whitmore, J. L. Konopka, M. L. Collier, E. M. B. Richmond, N. L. Davis, H. F. Staats, and R. E. Johnston. 2006. Mucosal and systemic adjuvant activity of alphavirus replicon particles. Proc. Natl. Acad. Sci. USA 103:3722-3727.
70. Tsunoda, I., T. E. Lane, J. Blackett, and R. S. Fujinami. 2004. Distinct roles for IP-10/CXCL10 in three animal models, Theiler's virus infection, EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10. Mult. Scler. 10:26-34.
71. Wacher, C., M. Müller, M. J. Hofer, D. R. Getts, R. Zabaras, S. S. Ousman, F. Terenzi, G. C. Sen, N. J. C. King, and I. L. Campbell. 2007. Coordinated regulation and widespread cellular expression of interferon-stimulated genes (ISG) ISG-49, ISG-54, and ISG-56 in the central nervous system after infection with distinct viruses. J. Virol. 81:860-871. (Pubitemid 46067911)
72. Ward, A. C. 1997. Virulence of influenza A virus for mouse lung. Virus Genes 14:187-194.
73. White, L. J., J.-G. Wang, N. L. Davis, and R. E. Johnston. 2001. Role of alpha/beta interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5′ untranslated region. J. Virol. 75:3706-3718.
74. Wright, P. F., and R. G. Webster. 2001. Orthomyxoviruses, p. 1533-1579. In D. M. Knipe, B. N. Fields, and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.