Early Virus-Host Interactions Dictate the Course of a Persistent Infection

PLoS Pathogens

Volumn 11, Issue 1, 2015, Pages 1-14

  Sullivan, Brian M ^a   Teijaro, John R ^a   de la Torre, Juan Carlos ^a   Oldstone, Michael B A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; CXCL9 CHEMOKINE; EOTAXIN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNE RESPONSE; LYMPHOCYTIC CHORIOMENENGITIS VIRUS; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; SPLEEN; VIRAL CLEARANCE; VIRUS; VIRUS CELL INTERACTION; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CHLOROCEBUS AETHIOPS; CHRONIC DISEASE; HAMSTER; HOST PATHOGEN INTERACTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; PHYSIOLOGY; TIME; VERO CELL LINE; VIROLOGY; VIRUS INFECTION; VIRUS LATENCY;

LYMPHOCYTIC CHORIOMENINGITIS VIRUS;

ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHRONIC DISEASE; CRICETINAE; HOST-PATHOGEN INTERACTIONS; IMMUNE TOLERANCE; IMMUNITY, INNATE; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SPLEEN; TIME FACTORS; VERO CELLS; VIRUS DISEASES; VIRUS LATENCY; VIRUS REPLICATION;

EID: 84923845601     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004588     Document Type: Article

References (73)

1. Marrack P, Kappler J, Mitchell T, (1999) Type I interferons keep activated T cells alive. J Exp Med 189: 521–530.
2. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF, (2005) Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 174: 4465–4469.
3. Aichele P, Unsoeld H, Koschella M, Schweier O, Kalinke U, et al. (2006) CD8 T cells specific for lymphocytic choriomeningitis virus require type I IFN receptor for clonal expansion. J Immunol 176: 4525–4529.
4. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K, (2005) Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202: 637–650.
5. Bonjardim CA, Ferreira PC, Kroon EG, (2009) Interferons: signaling, antiviral and viral evasion. Immunol Lett 122: 1–11.
6. Park SH, Rehermann B, (2014) Immune responses to HCV and other hepatitis viruses. Immunity 40: 13–24.
7. Goubau D, Deddouche S, Reis e Sousa C, (2013) Cytosolic sensing of viruses. Immunity 38: 855–869.
8. Hayes M, Salvato M, (2012) Arenavirus evasion of host anti-viral responses. Viruses 4: 2182–2196.
9. Taylor KE, Mossman KL, (2013) Recent advances in understanding viral evasion of type I interferon. Immunology 138: 190–197.
10. Bowie AG, Unterholzner L, (2008) Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8: 911–922.
11. Loo YM, Gale M, Jr (2007) Viral regulation and evasion of the host response. Curr Top Microbiol Immunol 316: 295–313.
12. Rustagi A, Gale M, Jr (2014) Innate antiviral immune signaling, viral evasion and modulation by HIV-1. J Mol Biol 426: 1161–1177.
13. Zuniga EI, Hahm B, Oldstone MB, (2007) Type I interferon during viral infections: multiple triggers for a multifunctional mediator. Curr Top Microbiol Immunol 316: 337–357.
14. Fan L, Briese T, Lipkin WI, (2010) Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J Virol 84: 1785–1791.
15. Rodrigo WW, Ortiz-Riano E, Pythoud C, Kunz S, de la Torre JC, et al. (2012) Arenavirus nucleoproteins prevent activation of nuclear factor kappa B. J Virol 86: 8185–8197.
16. Pythoud C, Rodrigo WW, Pasqual G, Rothenberger S, Martinez-Sobrido L, et al. (2012) Arenavirus nucleoprotein targets interferon regulatory factor-activating kinase IKKepsilon. J Virol 86: 7728–7738.
17. Borrow P, Martinez-Sobrido L, de la Torre JC, (2010) Inhibition of the type I interferon antiviral response during arenavirus infection. Viruses 2: 2443–2480.
18. Teijaro JR, Ng C, Lee AM, Sullivan BM, Sheehan KC, et al. (2013) Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340: 207–211.
19. Wilson EB, Yamada DH, Elsaesser H, Herskovitz J, Deng J, et al. (2013) Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340: 202–207.
20. Blasius AL, Krebs P, Sullivan BM, Oldstone MB, Popkin DL, (2012) Slc15a4, a gene required for pDC sensing of TLR ligands, is required to control persistent viral infection. PLoS Pathog 8: e1002915.
21. Wang Y, Swiecki M, Cella M, Alber G, Schreiber RD, et al. (2012) Timing and magnitude of type I interferon responses by distinct sensors impact CD8 T cell exhaustion and chronic viral infection. Cell Host Microbe 11: 631–642.
22. Southern PJ, Singh MK, Riviere Y, Jacoby DR, Buchmeier MJ, et al. (1987) Molecular characterization of the genomic S RNA segment from lymphocytic choriomeningitis virus. Virology 157: 145–155.
23. Buono P, Paolella G, Mancini FP, Izzo P, Salvatore F, (1988) The complete nucleotide sequence of the gene coding for the human aldolase C. Nucleic Acids Res 16: 4733.
24. Riviere Y, Ahmed R, Southern PJ, Buchmeier MJ, Dutko FJ, et al. (1985) The S RNA segment of lymphocytic choriomeningitis virus codes for the nucleoprotein and glycoproteins 1 and 2. J Virol 53: 966–968.
25. Lee KJ, Novella IS, Teng MN, Oldstone MB, de La Torre JC, (2000) NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs. J Virol 74: 3470–3477.
26. Pinschewer DD, Perez M, de la Torre JC, (2003) Role of the virus nucleoprotein in the regulation of lymphocytic choriomeningitis virus transcription and RNA replication. J Virol 77: 3882–3887.
27. Martinez-Sobrido L, Zuniga EI, Rosario D, Garcia-Sastre A, de la Torre JC, (2006) Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 80: 9192–9199.
28. Buchmeier MJ, Southern PJ, Parekh BS, Wooddell MK, Oldstone MB, (1987) Site-specific antibodies define a cleavage site conserved among arenavirus GP-C glycoproteins. J Virol 61: 982–985.
29. Wright KE, Spiro RC, Burns JW, Buchmeier MJ, (1990) Post-translational processing of the glycoproteins of lymphocytic choriomeningitis virus. Virology 177: 175–183.
30. Kunz S, Sevilla N, McGavern DB, Campbell KP, Oldstone MB, (2001) Molecular analysis of the interaction of LCMV with its cellular receptor [alpha]-dystroglycan. J Cell Biol 155: 301–310.
31. Salvato MS, Shimomaye EM, (1989) The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173: 1–10.
32. Strecker T, Eichler R, Meulen J, Weissenhorn W, Dieter Klenk H, et al. (2003) Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J Virol 77: 10700–10705.
33. Perez M, Craven RC, de la Torre JC, (2003) The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc Natl Acad Sci U S A 100: 12978–12983.
34. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB, (1984) Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med 160: 521–540.
35. Salvato M, Borrow P, Shimomaye E, Oldstone MB, (1991) Molecular basis of viral persistence: a single amino acid change in the glycoprotein of lymphocytic choriomeningitis virus is associated with suppression of the antiviral cytotoxic T-lymphocyte response and establishment of persistence. J Virol 65: 1863–1869.
36. Sullivan BM, Emonet SF, Welch MJ, Lee AM, Campbell KP, et al. (2011) Point mutation in the glycoprotein of lymphocytic choriomeningitis virus is necessary for receptor binding, dendritic cell infection, and long-term persistence. Proc Natl Acad Sci U S A 108: 2969–2974.
37. Bergthaler A, Flatz L, Hegazy AN, Johnson S, Horvath E, et al. (2010) Viral replicative capacity is the primary determinant of lymphocytic choriomeningitis virus persistence and immunosuppression. Proc Natl Acad Sci U S A 107: 21641–21646.
38. Smelt SC, Borrow P, Kunz S, Cao W, Tishon A, et al. (2001) Differences in affinity of binding of lymphocytic choriomeningitis virus strains to the cellular receptor alpha-dystroglycan correlate with viral tropism and disease kinetics. J Virol 75: 448–457.
39. Sevilla N, Kunz S, Holz A, Lewicki H, Homann D, et al. (2000) Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J Exp Med 192: 1249–1260.
40. Cao W, Henry MD, Borrow P, Yamada H, Elder JH, et al. (1998) Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 282: 2079–2081.
41. Matloubian M, Kolhekar SR, Somasundaram T, Ahmed R, (1993) Molecular determinants of macrophage tropism and viral persistence: importance of single amino acid changes in the polymerase and glycoprotein of lymphocytic choriomeningitis virus. J Virol 67: 7340–7349.
42. Lee AM, Cruite J, Welch MJ, Sullivan B, Oldstone MB, (2013) Pathogenesis of Lassa fever virus infection: I. Susceptibility of mice to recombinant Lassa Gp/LCMV chimeric virus. Virology 442: 114–121.
43. Macal M, Lewis GM, Kunz S, Flavell R, Harker JA, et al. (2012) Plasmacytoid dendritic cells are productively infected and activated through TLR-7 early after arenavirus infection. Cell Host Microbe 11: 617–630.
44. Ng CT, Oldstone MB, (2012) Infected CD8alpha- dendritic cells are the predominant source of IL-10 during establishment of persistent viral infection. Proc Natl Acad Sci U S A 109: 14116–14121.
45. Mueller SN, Matloubian M, Clemens DM, Sharpe AH, Freeman GJ, et al. (2007) Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection. Proc Natl Acad Sci U S A 104: 15430–15435.
46. Ng CT, Nayak BP, Schmedt C, Oldstone MB, (2012) Immortalized clones of fibroblastic reticular cells activate virus-specific T cells during virus infection. Proc Natl Acad Sci U S A 109: 7823–7828.
47. Borrow P, Evans CF, Oldstone MB, (1995) Virus-induced immunosuppression: immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J Virol 69: 1059–1070.
48. Sevilla N, Kunz S, McGavern D, Oldstone MB, (2003) Infection of dendritic cells by lymphocytic choriomeningitis virus. Curr Top Microbiol Immunol 276: 125–144.
49. Sevilla N, McGavern DB, Teng C, Kunz S, Oldstone MB, (2004) Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J Clin Invest 113: 737–745.
50. Muller S, Hunziker L, Enzler S, Buhler-Jungo M, Di Santo JP, et al. (2002) Role of an intact splenic microarchitecture in early lymphocytic choriomeningitis virus production. J Virol 76: 2375–2383.
51. Odermatt B, Eppler M, Leist TP, Hengartner H, Zinkernagel RM, (1991) Virus-triggered acquired immunodeficiency by cytotoxic T-cell-dependent destruction of antigen-presenting cells and lymph follicle structure. Proc Natl Acad Sci U S A 88: 8252–8256.
52. Tishon A, Borrow P, Evans C, Oldstone MB, (1993) Virus-induced immunosuppression. 1. Age at infection relates to a selective or generalized defect. Virology 195: 397–405.
53. Jin HT, Anderson AC, Tan WG, West EE, Ha SJ, et al. (2010) Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci U S A 107: 14733–14738.
54. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, et al. (2006) Interleukin-10 determines viral clearance or persistence in vivo. Nat Med 12: 1301–1309.
55. Ejrnaes M, Filippi CM, Martinic MM, Ling EM, Togher LM, et al. (2006) Resolution of a chronic viral infection after interleukin-10 receptor blockade. J Exp Med 203: 2461–2472.
56. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, et al. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682–687.
57. Zajac AJ, Blattman JN, Murali-Krishna K, Sourdive DJ, Suresh M, et al. (1998) Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med 188: 2205–2213.
58. Brooks DG, Teyton L, Oldstone MB, McGavern DB, (2005) Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J Virol 79: 10514–10527.
59. Brooks DG, Walsh KB, Elsaesser H, Oldstone MB, (2010) IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc Natl Acad Sci U S A 107: 3018–3023.
60. Mackerness KJ, Cox MA, Lilly LM, Weaver CT, Harrington LE, et al. (2010) Pronounced virus-dependent activation drives exhaustion but sustains IFN-gamma transcript levels. J Immunol 185: 3643–3651.
61. Oldstone MB, Blount P, Southern PJ, Lampert PW, (1986) Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system. Nature 321: 239–243.
62. Waggoner SN, Cornberg M, Selin LK, Welsh RM, (2012) Natural killer cells act as rheostats modulating antiviral T cells. Nature 481: 394–398.
63. Blasius AL, Arnold CN, Georgel P, Rutschmann S, Xia Y, et al. (2010) Slc15a4, AP-3, and Hermansky-Pudlak syndrome proteins are required for Toll-like receptor signaling in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 107: 19973–19978.
64. Richter K, Perriard G, Behrendt R, Schwendener RA, Sexl V, et al. (2013) Macrophage and T cell produced IL-10 promotes viral chronicity. PLoS Pathog 9: e1003735.
65. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C, (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529–1531.
66. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526–1529.
67. Walsh KB, Teijaro JR, Zuniga EI, Welch MJ, Fremgen DM, et al. (2012) Toll-like receptor 7 is required for effective adaptive immune responses that prevent persistent virus infection. Cell Host Microbe 11: 643–653.
68. Oldstone MB, Campbell KP, (2011) Decoding arenavirus pathogenesis: essential roles for alpha-dystroglycan-virus interactions and the immune response. Virology 411: 170–179.
69. Zhou S, Cerny AM, Zacharia A, Fitzgerald KA, Kurt-Jones EA, et al. (2010) Induction and inhibition of type I interferon responses by distinct components of lymphocytic choriomeningitis virus. J Virol 84: 9452–9462.
70. Wieland SF, Takahashi K, Boyd B, Whitten-Bauer C, Ngo N, et al. (2014) Human plasmacytoid dendritic cells sense lymphocytic choriomeningitis virus-infected cells in vitro. J Virol 88: 752–757.
71. Dreux M, Garaigorta U, Boyd B, Decembre E, Chung J, et al. (2012) Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe 12: 558–570.
72. Sanchez AB, de la Torre JC, (2006) Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 350: 370–380.
73. Battegay M, Cooper S, Althage A, Banziger J, Hengartner H, et al. (1991) Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J Virol Methods 33: 191–198.