Preservation of dendritic cell function during vesicular stomatitis virus infection reflects both intrinsic and acquired mechanisms of resistance to suppression of host gene expression by viral M protein

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11730-11740

  Westcott, Marlena M ^a   Ahmed, Maryam ^b   Smedberg, Jason R ^a   Rajani, Karishma R ^a,d   Hiltbold, Elizabeth M ^c   Lyles, Douglas S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b APPALACHIAN STATE UNIVERSITY   (United States)

^c AUBURN UNIVERSITY   (United States)

^d MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLT3 LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERFERON RECEPTOR; MATRIX PROTEIN; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 7;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE ACTIVATION; VESICULAR STOMATITIS; VESICULAR STOMATITIS VIRUS; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION; VESICULOVIRUS; VIROLOGY;

MURINAE; VESICULAR STOMATITIS VIRUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; GENE EXPRESSION; HOST-PATHOGEN INTERACTIONS; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; VESICULOVIRUS; VIRAL MATRIX PROTEINS;

EID: 84886875693     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00680-13     Document Type: Article

References (47)

1. Gerlier D, Lyles DS. 2011. Interplay between innate immunity and negative- strand RNA viruses: towards a rational model. Microbiol. Mol. Biol. Rev. 75:468-490.
2. Ahmed M, McKenzie MO, Puckett S, Hojnacki M, Poliquin L, Lyles DS. 2003. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 77:4646-4657.
3. Faul EJ, Lyles DS, Schnell MJ. 2009. Interferon response and viral evasion by members of the family Rhabdoviridae. Viruses 1:832-851.
4. Black BL, Rhodes RB, McKenzie M, Lyles DS. 1993. The role of vesicular stomatitis virus matrix protein in inhibition of host-directed gene expression is genetically separable from its function in virus assembly. J. Virol. 67:4814-4821.
5. Ahmed M, Marino TR, Puckett S, Kock ND, Lyles DS. 2008. Immune response in the absence of neurovirulence in mice infected withMprotein mutant vesicular stomatitis virus. J. Virol. 82:9273-9277.
6. Stojdl DF, Lichty BD, ten Oever BR, Paterson JM, Power AT, Knowles S, Marius R, Reynard J, Poliquin L, Atkins H, Brown EG, Durbin RK, Durbin JE, Hiscott J, Bell JC. 2003. VSV strains with defects in their ability to shutdown innate immunity are potent systemic anti-cancer agents. Cancer Cell 4:263-275.
7. Lang KS, Navarini AA, Recher M, Lang PA, Heikenwalder M, Stecher B, Bergthaler A, Odermatt B, Akira S, Honda K, Hengartner H, Zinkernagel RM. 2007. MyD88 protects from lethal encephalitis during infection with vesicular stomatitis virus. Eur. J. Immunol. 37:2434-2440.
8. Zhou S, Kurt-Jones EA, Fitzgerald KA, Wang JP, Cerny AM, Chan M, Finberg RW. 2007. Role of MyD88 in route-dependent susceptibility to vesicular stomatitis virus infection. J. Immunol. 178:5173-5181.
9. Hangartner L, Zinkernagel RM, Hengartner H. 2006. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6:231-243.
10. Muller U, SteinhoffU, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
11. Ahmed M, Mitchell LM, Puckett S, Brzoza-Lewis KL, Lyles DS, Hiltbold EM. 2009. Vesicular stomatitis virus M protein mutant stimulates maturation of Toll-like receptor 7 (TLR7)-positive dendritic cells through TLRdependent and -independent mechanisms. J. Virol. 83:2962-2975.
12. Waibler Z, Detje CN, Bell JC, Kalinke U. 2007. Matrix protein mediated shutdown of host cell metabolism limits vesicular stomatitis virusinduced interferon-alpha responses to plasmacytoid dendritic cells. Immunobiology 212:887-894.
13. Kapsenberg ML. 2003. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3:984-993.
14. Steinman RM. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9:271-296.
15. Heath WR, Belz GT, Behrens GM, Smith CM, Forehan SP, Parish IA, Davey GM, Wilson NS, Carbone FR, Villadangos JA. 2004. Crosspresentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol. Rev. 199:9-26.
16. Inaba K, Inaba M, Romani N, Aya H, Deguchi M, Ikehara S, Muramatsu S, Steinman RM. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176:1693-1702.
17. Naik SH, Proietto AI, Wilson NS, Dakic A, Schnorrer P, Fuchsberger M, Lahoud MH, O'Keeffe M, Shao QX, Chen WF, Villadangos JA, Shortman K, Wu L. 2005. Cutting edge: generation of splenic CD8+ and CD8-dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174:6592-6597.
18. Gilliet M, Boonstra A, Paturel C, Antonenko S, Xu XL, Trinchieri G, O'Garra A, Liu YJ. 2002. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 195:953-958.
19. Merad M, Sathe P, Helft J, Miller J, Mortha A. 2013. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31:563-604.
20. Ahmed M, Brzoza KL, Hiltbold EM. 2006. Matrix protein mutant of vesicular stomatitis virus stimulates maturation of myeloid dendritic cells. J. Virol. 80:2194-2205.
21. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
22. Colonna M, Trinchieri G, Liu YJ. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5:1219-1226.
23. Gilliet M, Cao W, Liu YJ. 2008. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8:594-606.
24. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. U. S. A. 101:5598-5603.
25. Takeda K, Akira S. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
26. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S. 1998. Targeted disruption of the MyD88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9:143-150.
27. Brandle D, Brduscha-Riem K, Hayday AC, Owen MJ, Hengartner H, Pircher H. 1995. T cell development and repertoire of mice expressing a single T cell receptor alpha chain. Eur. J. Immunol. 25:2650-2655.
28. Lyles DS, Puddington L, McCreedy BJ, Jr. 1988. Vesicular stomatitis virus M protein in the nuclei of infected cells. J. Virol. 62:4387-4392.
29. Naik SH, O'Keeffe M, Proietto A, Shortman HH, Wu L. 2010. CD8+, CD8-, and plasmacytoid dendritic cell generation in vitro using flt3 ligand. Methods Mol. Biol. 595:167-176.
30. Kopecky SA, Willingham MC, Lyles DS. 2001. Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J. Virol. 75:12169-12181.
31. Lyons AB, Hasbold J, Hodgkin PD. 2001. Flow cytometric analysis of cell division history using dilution of carboxyfluorescein diacetate succinimidyl ester, a stably integrated fluorescent probe. Methods Cell Biol. 63:375-398.
32. Connor JH, Lyles DS. 2005. Inhibition of host and viral translation during vesicular stomatitis virus infection. eIF2 is responsible for the inhibition of viral but not host translation. J. Biol. Chem. 280:13512-13519.
33. Rajani KR, Pettit Kneller EL, McKenzie MO, Horita DA, Chou JW, Lyles DS. 2012. Complexes of vesicular stomatitis virus matrix protein with host Rae1 and Nup98 involved in inhibition of host transcription. PLoS Pathog. 8:e1002929. doi:10.1371/journal.ppat.1002929.
34. Scheu S, Dresing P, Locksley RM. 2008. Visualization of IFNbeta production by plasmacytoid versus conventional dendritic cells under specific stimulation conditions in vivo. Proc. Natl. Acad. Sci. U. S. A. 105:20416-20421.
35. Koyama AH. 1995. Induction of apoptotic DNA fragmentation by the infection of vesicular stomatitis virus. Virus Res. 37:285-290.
36. Oehen S, Odermatt B, Karrer U, Hengartner H, Zinkernagel R, Lopez- Macias C. 2002. Marginal zone macrophages and immune responses against viruses. J. Immunol. 169:1453-1458.
37. Shi Z, Cai Z, Sanchez A, Zhang T, Wen S, Wang J, Yang J, Fu S, Zhang D. 2011. A novel Toll-like receptor that recognizes vesicular stomatitis virus. J. Biol. Chem. 286:4517-4524.
38. Blasius AL, Beutler B. 2010. Intracellular Toll-like receptors. Immunity 32:305-315.
39. Edelmann KH, Richardson-Burns S, Alexopoulou L, Tyler KL, Flavell RA, Oldstone MB. 2004. Does Toll-like receptor 3 play a biological role in virus infections? Virology 322:231-238.
40. Stetson DB, Medzhitov R. 2006. Type I interferons in host defense. Immunity 25:373-381.
41. Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M. 2010. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33:955-966.
42. Fitzgerald-Bocarsly P, Feng D. 2007. The role of type I interferon production by dendritic cells in host defense. Biochimie 89:843-855.
43. Ludewig B, Maloy KJ, Lopez-Macias C, Odermatt B, Hengartner H, Zinkernagel RM. 2000. Induction of optimal anti-viral neutralizing B cell responses by dendritic cells requires transport and release of virus particles in secondary lymphoid organs. Eur. J. Immunol. 30:185-196.
44. Borderia AV, Hartmann BM, Fernandez-Sesma A, Moran TM, Sealfon SC. 2008. Antiviral-activated dendritic cells: a paracrine-induced response state. J. Immunol. 181:6872-6881.
45. Phipps-Yonas H, Seto J, Sealfon SC, Moran TM, Fernandez-Sesma A. 2008. Interferon-beta pretreatment of conventional and plasmacytoid human dendritic cells enhances their activation by influenza virus. PLoS Pathog. 4:e1000193. doi:10.1371/journal.ppat.1000193.
46. Faria PA, Chakraborty P, Levay A, Barber GN, Ezelle HJ, Enninga J, Arana C, van Deursen J, Fontoura BM. 2005. VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol. Cell 17:93-102.
47. Harris RS, Hultquist JF, Evans DT. 2012. The restriction factors of human immunodeficiency virus. J. Biol. Chem. 287:40875-40883.