Negative Regulation of Type I IFN Expression by OASL1 Permits Chronic Viral Infection and CD8+ T-Cell Exhaustion

PLoS Pathogens

Volumn 9, Issue 7, 2013, Pages

  Lee, Myeong Sup ^a   Park, Chan Hee ^a   Jeong, Yun Hee ^a   Kim, Young Joon ^a   Ha, Sang Jun ^a  

^a Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2', 5' OLIGOADENYLATE SYNTHETASE; 7 AMINODACTINOMYCIN; GAMMA INTERFERON; INTERFERON; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; KI 67 ANTIGEN; LIPOCORTIN 5; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL SELECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME REGULATION; EXHAUSTION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPIC VARIATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; VIREMIA; VIRUS DETECTION; VIRUS INFECTION;

EID: 84884741768     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003478     Document Type: Article

References (71)

1. Lee MS, Kim YJ, (2007) Signaling pathways downstream of pattern-recognition receptors and their cross talk. Annu Rev Biochem 76: 447-480.
2. Takeuchi O, Akira S, (2009) Innate immunity to virus infection. Immunol Rev 227: 75-86.
3. Barbalat R, Ewald SE, Mouchess ML, Barton GM, (2011) Nucleic acid recognition by the innate immune system. Annu Rev Immunol 29: 185-214.
4. Kawai T, Akira S, (2006) Innate immune recognition of viral infection. Nat Immunol 7: 131-137.
5. Iwasaki A, Medzhitov R, (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995.
6. Iwasaki A, Medzhitov R, (2010) Regulation of adaptive immunity by the innate immune system. Science 327: 291-295.
7. Virgin HW, Wherry EJ, Ahmed R, (2009) Redefining chronic viral infection. Cell 138: 30-50.
8. West EE, Youngblood B, Tan WG, Jin HT, Araki K, et al. (2011) Tight regulation of memory CD8(+) T cells limits their effectiveness during sustained high viral load. Immunity 35: 285-298.
9. 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.
10. Petrovas C, Casazza JP, Brenchley JM, Price DA, Gostick E, et al. (2006) PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med 203: 2281-2292.
11. 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.
12. Kaufmann DE, Kavanagh DG, Pereyra F, Zaunders JJ, Mackey EW, et al. (2007) Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat Immunol 8: 1246-1254.
13. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, et al. (2009) Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 10: 29-37.
14. Jin HT, Jeong YH, Park HJ, Ha SJ, (2011) Mechanism of T cell exhaustion in a chronic environment. BMB Rep 44: 217-231.
15. Abbas AK, Sharpe AH, (2005) Dendritic cells giveth and taketh away. Nat Immunol 6: 227-228.
16. Ebinuma H, Nakamoto N, Li Y, Price DA, Gostick E, et al. (2008) Identification and in vitro expansion of functional antigen-specific CD25+ FoxP3+ regulatory T cells in hepatitis C virus infection. J Virol 82: 5043-5053.
17. Vignali DA, Collison LW, Workman CJ, (2008) How regulatory T cells work. Nat Rev Immunol 8: 523-532.
18. 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.
19. 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.
20. Alatrakchi N, Graham CS, van der Vliet HJ, Sherman KE, Exley MA, et al. (2007) Hepatitis C virus (HCV)-specific CD8+ cells produce transforming growth factor beta that can suppress HCV-specific T-cell responses. J Virol 81: 5882-5892.
21. Li MO, Sanjabi S, Flavell RA, (2006) Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and-independent mechanisms. Immunity 25: 455-471.
22. Kanto T, Inoue M, Miyatake H, Sato A, Sakakibara M, et al. (2004) Reduced numbers and impaired ability of myeloid and plasmacytoid dendritic cells to polarize T helper cells in chronic hepatitis C virus infection. J Infect Dis 190: 1919-1926.
23. Duan XZ, Wang M, Li HW, Zhuang H, Xu D, et al. (2004) Decreased frequency and function of circulating plasmocytoid dendritic cells (pDC) in hepatitis B virus infected humans. J Clin Immunol 24: 637-646.
24. Finke JS, Shodell M, Shah K, Siegal FP, Steinman RM, (2004) Dendritic cell numbers in the blood of HIV-1 infected patients before and after changes in antiretroviral therapy. J Clin Immunol 24: 647-652.
25. Altfeld M, Fadda L, Frleta D, Bhardwaj N, (2011) DCs and NK cells: critical effectors in the immune response to HIV-1. Nat Rev Immunol 11: 176-186.
26. Zuniga EI, Liou LY, Mack L, Mendoza M, Oldstone MB, (2008) Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 4: 374-386.
27. Lee LN, Burke S, Montoya M, Borrow P, (2009) Multiple mechanisms contribute to impairment of type 1 interferon production during chronic lymphocytic choriomeningitis virus infection of mice. J Immunol 182: 7178-7189.
28. Richards KH, Macdonald A, (2011) Putting the brakes on the anti-viral response: negative regulators of type I interferon (IFN) production. Microbes Infect 13: 291-302.
29. Bowie AG, Unterholzner L, (2008) Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8: 911-922.
30. Akhtar LN, Benveniste EN, (2011) Viral exploitation of host SOCS protein functions. J Virol 85: 1912-1921.
31. Aghemo A, Rumi MG, Colombo M, (2010) Pegylated interferons alpha2a and alpha2b in the treatment of chronic hepatitis C. Nat Rev Gastroenterol Hepatol 7: 485-494.
32. Lee MS, Kim B, Oh GT, Kim YJ, (2013) OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7. Nat Immunol 14: 346-355.
33. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R, (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77: 4911-4927.
34. Wherry EJ, Ahmed R, (2004) Memory CD8 T-cell differentiation during viral infection. J Virol 78: 5535-5545.
35. Gonzalez-Navajas JM, Lee J, David M, Raz E, (2012) Immunomodulatory functions of type I interferons. Nat Rev Immunol 12: 125-135.
36. Chang EY, Guo B, Doyle SE, Cheng G, (2007) Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J Immunol 178: 6705-6709.
37. Mancuso G, Midiri A, Biondo C, Beninati C, Zummo S, et al. (2007) Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J Immunol 178: 3126-3133.
38. Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, et al. (2002) Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297: 2063-2066.
39. Zhu J, Huang X, Yang Y, (2007) Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and-independent pathways. J Virol 81: 3170-3180.
40. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, et al. (2005) A critical function for type I interferons in cancer immunoediting. Nat Immunol 6: 722-729.
41. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, et al. (2006) Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res 26: 804-819.
42. Martinez-Sobrido L, Emonet S, Giannakas P, Cubitt B, Garcia-Sastre A, et al. (2009) Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 83: 11330-11340.
43. Martinez-Sobrido L, Giannakas P, Cubitt B, Garcia-Sastre A, de la Torre JC, (2007) Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J Virol 81: 12696-12703.
44. 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.
45. 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.
46. 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.
47. Kawai T, Akira S, (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
48. Dai J, Megjugorac NJ, Amrute SB, Fitzgerald-Bocarsly P, (2004) Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J Immunol 173: 1535-1548.
49. Izaguirre A, Barnes BJ, Amrute S, Yeow WS, Megjugorac N, et al. (2003) Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 74: 1125-1138.
50. Honda K, Takaoka A, Taniguchi T, (2006) Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25: 349-360.
51. 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.
52. 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.
53. Thompson LJ, Kolumam GA, Thomas S, Murali-Krishna K, (2006) Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J Immunol 177: 1746-1754.
54. Cervantes-Barragan L, Lewis KL, Firner S, Thiel V, Hugues S, et al. (2012) Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc Natl Acad Sci U S A 109: 3012-3017.
55. Wiesel M, Kratky W, Oxenius A, (2011) Type I IFN substitutes for T cell help during viral infections. J Immunol 186: 754-763.
56. Pinto AK, Daffis S, Brien JD, Gainey MD, Yokoyama WM, et al. (2011) A temporal role of type I interferon signaling in CD8+ T cell maturation during acute West Nile virus infection. PLoS Pathog 7: e1002407.
57. Havenar-Daughton C, Kolumam GA, Murali-Krishna K, (2006) Cutting Edge: The direct action of type I IFN on CD4 T cells is critical for sustaining clonal expansion in response to a viral but not a bacterial infection. J Immunol 176: 3315-3319.
58. Huber JP, Farrar JD, (2011) Regulation of effector and memory T-cell functions by type I interferon. Immunology 132: 466-474.
59. Matikainen S, Paananen A, Miettinen M, Kurimoto M, Timonen T, et al. (2001) IFN-alpha and IL-18 synergistically enhance IFN-gamma production in human NK cells: differential regulation of Stat4 activation and IFN-gamma gene expression by IFN-alpha and IL-12. Eur J Immunol 31: 2236-2245.
60. Strengell M, Julkunen I, Matikainen S, (2004) IFN-alpha regulates IL-21 and IL-21R expression in human NK and T cells. J Leukoc Biol 76: 416-422.
61. Gallucci S, Lolkema M, Matzinger P, (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5: 1249-1255.
62. Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, et al. (1998) Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 161: 1947-1953.
63. Montoya M, Schiavoni G, Mattei F, Gresser I, Belardelli F, et al. (2002) Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood 99: 3263-3271.
64. Elsaesser H, Sauer K, Brooks DG, (2009) IL-21 is required to control chronic viral infection. Science 324: 1569-1572.
65. Frohlich A, Kisielow J, Schmitz I, Freigang S, Shamshiev AT, et al. (2009) IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 324: 1576-1580.
66. Pellegrini M, Calzascia T, Toe JG, Preston SP, Lin AE, et al. (2011) IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 144: 601-613.
67. Yu Y, Hayward GS, (2010) The ubiquitin E3 ligase RAUL negatively regulates type i interferon through ubiquitination of the transcription factors IRF7 and IRF3. Immunity 33: 863-877.
68. Naka T, Fujimoto M, Tsutsui H, Yoshimura A, (2005) Negative regulation of cytokine and TLR signalings by SOCS and others. Adv Immunol 87: 61-122.
69. Shuai K, Liu B, (2003) Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol 3: 900-911.
70. Murali-Krishna K, Altman JD, Suresh M, Sourdive DJ, Zajac AJ, et al. (1998) Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8: 177-187.
71. Ha SJ, Mueller SN, Wherry EJ, Barber DL, Aubert RD, et al. (2008) Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J Exp Med 205: 543-555.