IFN-dependent and -independent reduction in West Nile virus infectivity in human dermal fibroblasts

Viruses

Volumn 6, Issue 3, 2014, Pages 1424-1441

  Hoover, Lisa I ^a   Fredericksen, Brenda L ^a  

^a University of Maryland   (United States)

Author keywords

Antiviral response; Human dermal fibroblast; Interferon; Intracellular innate immunity; West Nile virus

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; HUMAN INTERFERON;

ARTICLE; COLONY FORMING UNIT; FLAVIVIRUS INFECTION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LIMIT OF DETECTION; NONHUMAN; PLAQUE FORMING CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SKIN FIBROBLAST; VESICULAR STOMATITIS VIRUS; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

CELLS, CULTURED; FIBROBLASTS; HUMANS; INTERFERONS; VIRAL TROPISM; VIRUS REPLICATION; WEST NILE VIRUS;

EID: 84897142031     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6031424     Document Type: Article

References (61)

1. CDC. Available online: http://www. cdc. gov/westnile/index. html/(accessed on 1 November 2013).
2. Bondre, V. P.; Jadi, R. S.; Mishra, A. C.; Yergolkar, P. N.; Arankalle, V. A. West Nile virus isolates from India: Evidence for a distinct genetic lineage. J. Gen. Virol. 2007, 88, 875-884.
3. Lanciotti, R. S.; Ebel, G. D.; Deubel, V.; Kerst, A. J.; Murri, S.; Meyer, R.; Bowen, M.; McKinney, N.; Morrill, W. E.; Crabtree, M. B.; et al. Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 2002, 298, 96-105.
4. Bakonyi, T.; Ferenczi, E.; Erdélyi, K.; Kutasi, O.; Csörgo{double acute}, T.; Seidel, B.; Weissenböck, H.; Brugger, K.; Bán, E.; Nowotny, N. Explosive spread of a neuroinvasive lineage 2 West Nile virus in Central Europe, 2008/2009. Vet. Microbiol. 2013, 165, 61-70.
5. Sirbu, A.; Ceianu, C. S.; Panculescu-Gatej, R. I.; Vazquez, A.; Tenorio, A.; Rebreanu, R.; Niedrig, M.; Nicolescu, G.; Pistol, A. Outbreak of West Nile virus infection in humans, Romania, July to October 2010. Eurosurveillance 2011, 16, pii: 19762.
6. Danis, K.; Papa, A.; Theocharopoulos, G.; Dougas, G.; Athanasiou, M.; Detsis, M.; Baka, A.; Lytras, T.; Mellou, K. Outbreak of West Nile virus infection in Greece, 2010. Emerg. Infect. Dis. 2011, 17, 1868-1872.
7. Platonov, A. E.; Karan, L. S.; Shopenskaia, T. A.; Fedorova, M. V.; Koliasnikova, N. M.; Rusakova, N. M.; Shishkina, L. V.; Arshba, T. E.; Zhuravlev, V. I.; Govorukhina, M. V.; et al. Genotyping of West Nile fever virus strains circulating in Southern Russia as an epidemiological investigation method: Principles and results. Zh Mikrobiol. Epidemiol. Immunobiol. 2011, Mar-Apr, 29-37.
8. Frost, M. J.; Zhang, J.; Edmonds, J. H.; Prow, N. A.; Gu, X.; Davis, R.; Hornitzky, C.; Arzey, K. E.; Finlaison, D.; Hick, P.; et al. Characterization of virulent West Nile virus kunjin strain, Australia, 2011. Emerg. Infect. Dis. 2012, 18, 792-800.
9. Venter, M.; Human, S.; Zaayman, D.; Gerdes, G. H.; Williams, J.; Steyl, J.; Leman, P. A.; Paweska, J. T.; Setzkorn, H.; Rous, G.; et al. Lineage 2 West Nile virus as cause of fatal neurologic disease in horses, South Africa. Emerg. Infect. Dis. 2009, 15, 877-884.
10. Venter, M.; Swanepoel, R. West Nile virus lineage 2 as a cause of zoonotic neurological disease in humans and horses in Southern Africa. Vector Borne Zoonotic Dis. 2010, 10, 659-664.
11. Kutasi, O.; Bakonyi, T.; Lecollinet, S.; Biksi, I.; Ferenczi, E.; Bahuon, C.; Sardi, S.; Zientara, S.; Szenci, O. Equine encephalomyelitis outbreak caused by a genetic lineage 2 West Nile virus in Hungary. J. Vet. Intern. Med. 2011, 25, 586-591.
12. Magurano, F.; Remoli, M. E.; Baggieri, M.; Fortuna, C.; Marchi, A.; Fiorentini, C.; Bucci, P.; Benedetti, E.; Ciufolini, M. G.; Rizzo, C.; et al. Circulation of West Nile virus lineage 1 and 2 during an outbreak in Italy. Clin. Microbiol. Infect. 2012, 18, E545-E547.
13. Brault, A. C.; Langevin, S. A.; Bowen, R. A.; Panella, N. A.; Biggerstaff, B. J.; Miller, B. R.; Komar, N. Differential virulence of West Nile strains for American crows. Emerg. Infect. Dis. 2004, 10, 2161-2168.
14. Langevin, S. A.; Brault, A. C.; Panella, N. A.; Bowen, R. A.; Komar, N. Variation in virulence of West Nile virus strains for house sparrows (Passer domesticus). Am. J. Trop. Med. Hyg. 2005, 72, 99-102.
15. Botha, E. M.; Markotter, W.; Wolfaardt, M.; Paweska, J. T.; Swanepoel, R.; Palacios, G.; Nel, L. H.; Venter, M. Genetic determinants of virulence in pathogenic lineage 2 West Nile virus strains. Emerg. Infect. Dis. 2008, 14, 222-230.
16. Beasley, D. W. C.; Li, L.; Suderman, M. T.; Barrett, A. D. T. Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 2002, 296, 17-23.
17. Beasley, D. W. C.; Davis, C. T.; Whiteman, M.; Granwehr, B.; Kinney, R. M.; Barrett, A. D. T. Molecular determinants of virulence of West Nile virus in North America. Arch. Virol. Suppl. 2004, 18, 35-41.
18. Colpitts, T. M.; Conway, M. J.; Montgomery, R. R.; Fikrig, E. West Nile virus: Biology, transmission, and human infection. Clin. Microbiol. Rev. 2012, 25, 635-648.
19. Machain-Williams, C.; Padilla-Paz, S. E.; Weber, M.; Cetina-Trejo, R.; Juarez-Ordaz, J. A.; Loroño-Pino, M. A.; Ulloa, A.; Wang, C.; Garcia-Rejon, J.; Blitvich, B. J. Antibodies to West Nile virus in wild and farmed crocodiles in Southeastern Mexico. J. Wildl. Dis. 2013, 49, 690-693.
20. Reagan, K. L.; Machain-Williams, C.; Wang, T.; Blair, C. D. Immunization of mice with recombinant mosquito salivary protein D7 enhances mortality from subsequent West Nile virus infection via mosquito bite. PLoS Negl. Trop. Dis. 2012, 6, e1935.
21. Styer, L. M.; Kent, K. A.; Albright, R. G.; Bennett, C. J.; Kramer, L. D.; Bernard, K. A. Mosquitoes inoculate high doses of West Nile virus as they probe and feed on live hosts. PLoS Pathog. 2007, 3, 1262-1270.
22. Styer, L. M.; Lim, P.-Y.; Louie, K. L.; Albright, R. G.; Kramer, L. D.; Bernard, K. A. Mosquito saliva causes enhancement of West Nile virus infection in mice. J. Virol. 2011, 85, 1517-1527.
23. Schneider, B. S.; McGee, C. E.; Jordan, J. M.; Stevenson, H. L.; Soong, L.; Higgs, S. Prior exposure to uninfected mosquitoes enhances mortality in naturally-transmitted West Nile virus infection. PLoS One 2007, 2, e1171.
24. Johnston, L. J.; Halliday, G. M.; King, N. J. Phenotypic changes in Langerhans' cells after infection with arboviruses: A role in the immune response to epidermally acquired viral infection? J. Virol. 1996, 70, 4761-4766.
25. Limon-Flores, A. Y.; Perez-Tapia, M.; Estrada-Garcia, I.; Vaughan, G.; Escobar-Gutierrez, A.; Calderon-Amador, J.; Herrera-Rodriguez, S. E.; Brizuela-Garcia, A.; Heras-Chavarria, M.; Flores-Langarica, A.; et al. Dengue virus inoculation to human skin explants: An effective approach to assess in situ the early infection and the effects on cutaneous dendritic cells. Int. J. Clin. Exp. Pathol. 2005, 86, 323-334.
26. Palmer, D. R.; Sun, P.; Celluzzi, C.; Pang, S.; Sun, W.; Marovich, M. A.; Burgess, T.; Bisbing, J. Differential effects of dengue virus on infected and bystander dendritic cells. J. Virol. 2005, 79, 2432-2439.
27. Wu, S. J.; Grouard-Vogel, G.; Sun, W.; Mascola, J. R.; Brachtel, E.; Putvatana, R.; Louder, M. K.; Filgueira, L.; Marovich, M. A.; Wong, H. K.; et al. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 2000, 6, 816-820.
28. Byrne, S. N.; Halliday, G. M.; Johnston, L. J.; King, N. J. Interleukin-1beta but not tumor necrosis factor is involved in West Nile virus-induced Langerhans cell migration from the skin in C57BL/6 mice. J. Investig. Dermatol. 2001, 117, 702-709.
29. Johnston, B. L.; Conly, J. M. West Nile virus-Where did it come from and where might it go? Can. J. Infect. Dis. Med. Microbiol. 2000, 11, 175-178.
30. Lim, P.-Y.; Behr, M. J.; Chadwick, C. M.; Shi, P.-Y.; Bernard, K. A. Keratinocytes are cell targets of West Nile virus in vivo. J. Virol. 2011, 85, 5197-5201.
31. Kurane, I.; Janus, J.; Ennis, F. A. Dengue virus infection of human skin fibroblasts in vitro production of IFN-beta, IL-6 and GM-CSF. Arch. Virol. 1992, 124, 21-30.
32. Shi, P. Y.; Tilgner, M.; Lo, M. K.; Kent, K. A.; Bernard, K. A. Infectious cDNA clone of the epidemic West Nile virus from New York City. J. Virol. 2002, 76, 5847-5856.
33. Lazear, H. M.; Pinto, A. K.; Vogt, M. R.; Gale, M., Jr.; Diamond, M. S. Beta interferon controls West Nile virus infection and pathogenesis in mice. J. Virol. 2011, 85, 7186-7194.
34. Suthar, M. S.; Brassil, M. M.; Blahnik, G.; McMillan, A.; Ramos, H. J.; Proll, S. C.; Belisle, S. E.; Katze, M. G.; Gale, M., Jr. A systems biology approach reveals that tissue tropism to West Nile virus is regulated by antiviral genes and innate immune cellular processes. PLoS Pathog. 2013, 9, e1003168.
35. Samuel, M. A.; Diamond, M. S. Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J. Virol. 2005, 79, 13350-13361.
36. Maheshwari, R. K.; Friedman, R. M. Production of vesicular stomatitis virus with low infectivity by interferon-treated cells. J. Gen. Virol. 1979, 44, 261-264.
37. Wong, P. K.; Yuen, P. H.; MacLeod, R.; Chang, E. H.; Myers, M. W.; Friedman, R. M. The effect of interferon on de novo infection of Moloney murine leukemia virus. Cell 1977, 10, 245-252.
38. Chang, E. H.; Mims, S. J.; Triche, T. J.; Friedman, R. M. Interferon inhibits mouse leukaemia virus release: An electron microscope study. J. Gen. Virol. 1977, 34, 363-367.
39. Munoz, A.; Carrasco, L. Formation of non-infective herpesvirus particles in cultured cells treated with human interferon. J. Gen. Virol. 1984, 65, 1069-1078.
40. Babe, L. M.; Unal, A.; Craik, C. S. Obstruction of HIV-1 particle release by interferon-alpha occurs before viral protease processing and is independent of envelope glycoprotein. J. Interf. Cytokine Res. 1997, 17, 287-293.
41. Hansen, B. D.; Nara, P. L.; Maheshwari, R. K.; Sidhu, G. S.; Bernbaum, J. G.; Hoekzema, D.; Meltzer, M. S.; Gendelman, H. E. Loss of infectivity by progeny virus from alpha interferon-treated human immunodeficiency virus type 1-infected T cells is associated with defective assembly of envelope gp120. J. Virol. 1992, 66, 7543-7548.
42. Rozen-Gagnon, K.; Stapleford, K. A.; Mongelli, V.; Blanc, H.; Failloux, A.-B.; Saleh, M.-C.; Vignuzzi, M. Alphavirus mutator variants present host-specific defects and attenuation in mammalian and insect models. PLoS Pathog. 2014, 10, e1003877.
43. Rodenhuis-Zybert, I. A.; van der Schaar, H. M.; da Silva Voorham, J. M.; van der Ende-Metselaar, H.; Lei, H.-Y.; Wilschut, J.; Smit, J. M. Immature dengue virus: A veiled pathogen? PLoS Pathog. 2010, 6, e1000718.
44. Elshuber, S.; Allison, S. L.; Heinz, F. X.; Mandl, C. W. Cleavage of protein prM is necessary for infection of BHK-21 cells by tick-borne encephalitis virus. J. Gen. Virol. 2003, 84, 183-191.
45. Heinz, F. X.; Stiasny, K.; Puschner-Auer, G.; Holzmann, H.; Allison, S. L.; Mandl, C. W.; Kunz, C. Structural changes and functional control of the tick-borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 1994, 198, 109-117.
46. Liu, W. J.; Chen, H. B.; Wang, X. J.; Huang, H.; Khromykh, A. A. Analysis of Adaptive Mutations in Kunjin Virus Replicon RNA Reveals a Novel Role for the Flavivirus Nonstructural Protein NS2A in Inhibition of Beta Interferon Promoter-Driven Transcription. J. Virol. 2004, 78, 12225-12235.
47. Liu, W. J.; Wang, X. J.; Mokhonov, V. V.; Shi, P.; Randall, R.; Khromykh, A. A. Inhibition of Interferon Signaling by the New York 99 Strain and Kunjin Subtype of West Nile Virus Involves Blockage of STAT1 and STAT2 Activation by Nonstructural Proteins. J. Virol. 2005, 79, 1934-1942.
48. Liu, W. J.; Wang, X. J.; Clark, D. C.; Lobigs, M.; Hall, R. A.; Khromykh, A. A. A Single Amino Acid Substitution in the West Nile Virus Nonstructural Protein NS2A Disables Its Ability To Inhibit Alpha/Beta Interferon Induction and Attenuates Virus Virulence in Mice. J. Virol. 2006, 80, 2396-2404.
49. Wilson, J. R.; de Sessions, P. F.; Leon, M.; Scholle, F. West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J. Virol. 2008, 82, 8262-8271.
50. Arjona, A.; Ledizet, M.; Anthony, K.; Bonafé, N.; Modis, Y.; Town, T.; Fikrig, E. West Nile virus envelope protein inhibits dsRNA-induced innate immune responses. J. Immunol. 2007, 179, 8403-8409.
51. Baronti, C.; Sire, J.; de Lamballerie, X.; Quérat, G. Nonstructural NS1 proteins of several mosquito-borne Flavivirus do not inhibit TLR3 signaling. Virology 2010, 404, 319-330.
52. Best, S. M.; Morris, K. L.; Shannon, J. G.; Robertson, J.; Mitzel, D. N.; Park, G. S.; Boer, E.; Wolfinbarger, J. B.; Bloom, M. E.; Robertson, S. J. Inhibition of Interferon-Stimulated JAK-STAT Signaling by a Tick-Borne Flavivirus and Identification of NS5 as an Interferon Antagonist. J. Virol. 2005, 79, 12828-12839.
53. Guo, J.; Hayashi, J.; Seeger, C. West Nile Virus Inhibits the Signal Transduction Pathway of Alpha Interferon. J. Virol. 2005, 79, 1343-1350.
54. Muñoz-Jordan, J. L.; Sánchez-Burgos, G. G.; Laurent-Rolle, M.; García-Sastre, A. Inhibition of interferon signaling by dengue virus. Proc. Natl. Acad. Sci. USA 2003, 100, 14333-14338.
55. Diamond, M. S. Mechanisms of evasion of the type I interferon antiviral response by flaviviruses. J. Interf. Cytokine Res. 2009, 29, 521-530.
56. Fredericksen, B. L.; Smith, M.; Katze, M. G.; Shi, P.; Gale, M. The Host Response to West Nile Virus Infection Limits Viral Spread through the Activation of the Interferon Regulatory Factor 3 Pathway. J. Virol. 2004, 78, 7737-7747.
57. Cho, H.; Proll, S. C.; Szretter, K. J.; Katze, M. G.; Gale, M., Jr.; Diamond, M. S. Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positive-stranded RNA viruses. Nat. Med. 2013, 19, 458-464.
58. Venter, M.; Myers, T. G.; Wilson, M. A.; Kindt, T. J.; Pawaska, J. T.; Burt, F. J.; Leman, P. A.; Swanepoel, R. Gene expression in mice infected with West Nile virus strains of different neurovirulence. Virology 2005, 342, 119-140.
59. Scherbik, S. V.; Stockman, B. M.; Brinton, M. A. Differential Expression of Interferon (IFN) Regulatory Factors and IFN-Stimulated Genes at Early Times after West Nile Virus Infection of Mouse Embryo Fibroblasts. J. Virol. 2007, 81, 12005-12018.
60. Hoenen, A.; Gillespie, L.; Morgan, G.; Heide, P.; Khromykh, A.; Mackensie, J. The West Nile virus assembly process evades the conserved antiviral mechanism of the interferon-induced MxA protein. Virology 2014, 448, 104-116.
61. Szretter, K. J.; Daniels, B. P.; Cho, H.; Gainey, M. D.; Yokoyama, W. M.; Gale, M.; Virgin, H. W.; Klein, R. S.; Sen, G. C.; Diamond, M. S. 2′-O Methylation of the Viral mRNA Cap by West Nile Virus Evades Ifit1-Dependent and-Independent Mechanisms of Host Restriction in vivo. PLoS Pathog. 2012, 8, e1002698.