New insights into type I interferon and the immunopathogenesis of persistent viral infections

Current Opinion in Immunology

Volumn 34, Issue , 2015, Pages 91-98

  Snell, Laura M ^a   Brooks, David G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PRINCESS MARGARET HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; INTERFERON; INTERFERON ANTIBODY;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIVIRAL ACTIVITY; CELLULAR IMMUNITY; CHRONIC INFLAMMATION; CYTOKINE PRODUCTION; DISEASE COURSE; DOWN REGULATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; HYPERGAMMAGLOBULINEMIA; IMMUNE DEFICIENCY; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; IMMUNOREGULATION; IMMUNOSTIMULATION; INFECTION CONTROL; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; PERSISTENT VIRUS INFECTION; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TARGET CELL; ANIMAL; CHRONIC DISEASE; DENDRITIC CELL; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE; VIROLOGY; VIRUS INFECTION;

ANIMALS; CHRONIC DISEASE; DENDRITIC CELLS; HUMANS; INTERFERON TYPE I; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; VIRUS DISEASES;

EID: 84924584546     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2015.03.002     Document Type: Review

References (62)

1. Trinchieri G. Type I interferon: friend or foe?. J Exp Med 2010, 207:2053-2063.
2. Clingan J.M., Ostrow K., Hosiawa K.A., Chen Z.J., Matloubian M. Differential roles for RIG-I-like receptors and nucleic acid-sensing TLR pathways in controlling a chronic viral infection. J Immunol 2012, 188:4432-4440.
3. Jung A., Kato H., Kumagai Y., Kumar H., Kawai T., Takeuchi O., Akira S. Lymphocytoid choriomeningitis virus activates plasmacytoid dendritic cells and induces a cytotoxic T-cell response via MyD88. J Virol 2008, 82:196-206.
4. Lee L.N., Burke S., Montoya M., Borrow P. Multiple mechanisms contribute to impairment of type 1 interferon production during chronic lymphocytic choriomeningitis virus infection of mice. J Immunol 2009, 182:7178-7189.
5. Wang Y., Swiecki M., Cella M., Alber G., Schreiber R.D., Gilfillan S., Colonna M. Timing and magnitude of type I interferon responses by distinct sensors impact CD8 T cell exhaustion and chronic viral infection. Cell Host Microbe 2012, 11:631-642.
6. Zhou S., Cerny A.M., Zacharia A., Fitzgerald K.A., Kurt-Jones E.A., Finberg R.W. Induction and inhibition of type I interferon responses by distinct components of lymphocytic choriomeningitis virus. J Virol 2010, 84:9452-9462.
7. Zuniga E.I., Liou L.Y., Mack L., Mendoza M., Oldstone M.B. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 2008, 4:374-386.
8. de Weerd N.A., Vivian J.P., Nguyen T.K., Mangan N.E., Gould J.A., Braniff S.J., Zaker-Tabrizi L., Fung K.Y., Forster S.C., Beddoe T., Reid H.H., Rossjohn J., Hertzog P.J. Structural basis of a unique interferon-beta signaling axis mediated via the receptor IFNAR1. Nat Immunol 2013, 14:901-907.
9. Levin D., Schneider W.M., Hoffmann H.H., Yarden G., Busetto A.G., Manor O., Sharma N., Rice C.M., Schreiber G. Multifaceted activities of type I interferon are revealed by a receptor antagonist. Sci Signal 2014, 7:ra50.
10. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005, 5:375-386.
11. Ivashkiv L.B., Donlin L.T. Regulation of type I interferon responses. Nat Rev Immunol 2014, 14:36-49.
12. Wilson E.B., Yamada D.H., Elsaesser H., Herskovitz J., Deng J., Cheng G., Aronow B.J., Karp C.L., Brooks D.G. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 2013, 340:202-207.
13. Teijaro J.R., Ng C., Lee A.M., Sullivan B.M., Sheehan K.C., Welch M., Schreiber R.D., de la Torre J.C., Oldstone M.B. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 2013, 340:207-211.
14. Ou R., Zhou S., Huang L., Moskophidis D. Critical role for alpha/beta and gamma interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J Virol 2001, 75:8407-8423.
15. Arimori Y., Nakamura R., Yamada H., Shibata K., Maeda N., Kase T., Yoshikai Y. Type I interferon limits influenza virus-induced acute lung injury by regulation of excessive inflammation in mice. Antiviral Res 2013, 99:230-237.
16. Goritzka M., Durant L.R., Pereira C., Salek-Ardakani S., Openshaw P.J., Johansson C. Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J Virol 2014, 88:6128-6136.
17. Schneider W.M., Chevillotte M.D., Rice C.M. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 2014, 32:513-545.
18. Lee M.S., Park C.H., Jeong Y.H., Kim Y.J., Ha S.J. Negative regulation of type I IFN expression by OASL1 permits chronic viral infection and CD8(+) T-cell exhaustion. PLoS Pathog 2013, 9:e1003478.
19. Crawford A., Angelosanto J.M., Kao C., Doering T.A., Odorizzi P.M., Barnett B.E., Wherry E.J. Molecular and transcriptional basis of CD4(+) T cell dysfunction during chronic infection. Immunity 2014, 40:289-302.
20. Hyrcza M.D., Kovacs C., Loutfy M., Halpenny R., Heisler L., Yang S., Wilkins O., Ostrowski M., Der S.D. Distinct transcriptional profiles in ex vivo CD4+ and CD8+ T cells are established early in human immunodeficiency virus type 1 infection and are characterized by a chronic interferon response as well as extensive transcriptional changes in CD8+ T cells. J Virol 2007, 81:3477-3486.
21. Boasso A., Hardy A.W., Landay A.L., Martinson J.L., Anderson S.A., Dolan M.J., Clerici M., Shearer G.M. PDL-1 upregulation on monocytes and T cells by HIV via type I interferon: restricted expression of type I interferon receptor by CCR5-expressing leukocytes. Clin Immunol 2008, 129:132-144.
22. Saito K., Ait-Goughoulte M., Truscott S.M., Meyer K., Blazevic A., Abate G., Ray R.B., Hoft D.F., Ray R. Hepatitis C virus inhibits cell surface expression of HLA-DR, prevents dendritic cell maturation, and induces interleukin-10 production. J Virol 2008, 82:3320-3328.
23. Wilson E.B., Kidani Y., Elsaesser H., Barnard J., Raff L., Karp C.L., Bensinger S., Brooks D.G. Emergence of distinct multiarmed immunoregulatory antigen-presenting cells during persistent viral infection. Cell Host Microbe 2012, 11:481-491.
24. Ng C.T., Oldstone M.B. Infected CD8alpha-dendritic cells are the predominant source of IL-10 during establishment of persistent viral infection. Proc Natl Acad Sci U S A 2012, 109:14116-14121.
25. Ohyagi H., Onai N., Sato T., Yotsumoto S., Liu J., Akiba H., Yagita H., Atarashi K., Honda K., Roers A., Muller W., Kurabayashi K., Hosoi-Amaike M., Takahashi N., Hirokawa M., Matsushima K., Sawada K., Ohteki T. Monocyte-derived dendritic cells perform hemophagocytosis to fine-tune excessive immune responses. Immunity 2013, 39:584-598.
26. Hahm B., Trifilo M.J., Zuniga E.I., Oldstone M.B. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 2005, 22:247-257.
27. Agrawal H., Jacob N., Carreras E., Bajana S., Putterman C., Turner S., Neas B., Mathian A., Koss M.N., Stohl W., Kovats S., Jacob C.O. Deficiency of type I IFN receptor in lupus-prone New Zealand mixed 2328 mice decreases dendritic cell numbers and activation and protects from disease. J Immunol 2009, 183:6021-6029.
28. Schreiner B., Mitsdoerffer M., Kieseier B.C., Chen L., Hartung H.P., Weller M., Wiendl H. Interferon-beta enhances monocyte and dendritic cell expression of B7-H1 (PD-L1), a strong inhibitor of autologous T-cell activation: relevance for the immune modulatory effect in multiple sclerosis. J Neuroimmunol 2004, 155:172-182.
29. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008, 26:677-704.
30. Mayer-Barber K.D., Andrade B.B., Barber D.L., Hieny S., Feng C.G., Caspar P., Oland S., Gordon S., Sher A. Innate and adaptive interferons suppress IL-1alpha and IL-1beta production by distinct pulmonary myeloid subsets during Mycobacterium tuberculosis infection. Immunity 2011, 35:1023-1034.
31. Mayer-Barber K.D., Andrade B.B., Oland S.D., Amaral E.P., Barber D.L., Gonzales J., Derrick S.C., Shi R., Kumar N.P., Wei W., Yuan X., Zhang G., Cai Y., Babu S., Catalfamo M., Salazar A.M., Via L.E., Barry C.E., Sher A. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 2014, 511:99-103.
32. Norris B.A., Uebelhoer L.S., Nakaya H.I., Price A.A., Grakoui A., Pulendran B. Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity 2013, 38:309-321.
33. Havenar-Daughton C., Kolumam G.A., Murali-Krishna K. 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 2006, 176:3315-3319.
34. Kolumam G.A., Thomas S., Thompson L.J., Sprent J., Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005, 202:637-650.
35. Osokine I., Snell L.M., Cunningham C.R., Yamada D.H., Wilson E.B., Elsaesser H.J., de la Torre J.C., Brooks D. Type I interferon suppresses de novo virus-specific CD4 Th1 immunity during an established persistent viral infection. Proc Natl Acad Sci U S A 2014, 111:7409-7414.
36. Thompson L.J., Kolumam G.A., Thomas S., Murali-Krishna K. 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 2006, 177:1746-1754.
37. McNally J.M., Zarozinski C.C., Lin M.Y., Brehm M.A., Chen H.D., Welsh R.M. Attrition of bystander CD8 T cells during virus-induced T-cell and interferon responses. J Virol 2001, 75:5965-5976.
38. Quigley M., Pereyra F., Nilsson B., Porichis F., Fonseca C., Eichbaum Q., Julg B., Jesneck J.L., Brosnahan K., Imam S., Russell K., Toth I., Piechocka-Trocha A., Dolfi D., Angelosanto J., Crawford A., Shin H., Kwon D.S., Zupkosky J., Francisco L., Freeman G.J., Wherry E.J., Kaufmann D.E., Walker B.D., Ebert B., Haining W.N. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med 2010, 16:1147-1151.
39. Wherry E.J., Ha S.J., Kaech S.M., Haining W.N., Sarkar S., Kalia V., Subramaniam S., Blattman J.N., Barber D.L., Ahmed R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007, 27:670-684.
40. Ng C.T., Snell L.M., Brooks D.G., Oldstone M.B. Networking at the level of host immunity: immune cell interactions during persistent viral infections. Cell Host Microbe 2013, 13:652-664.
41. Harker J.A., Dolgoter A., Zuniga E.I. Cell-intrinsic IL-27 and gp130 cytokine receptor signaling regulates virus-specific CD4(+) T cell responses and viral control during chronic infection. Immunity 2013, 39:548-559.
42. Molle C., Goldman M., Goriely S. Critical role of the IFN-stimulated gene factor 3 complex in TLR-mediated IL-27p28 gene expression revealing a two-step activation process. J Immunol 2010, 184:1784-1792.
43. Ray J.P., Marshall H.D., Laidlaw B.J., Staron M.M., Kaech S.M., Craft J. Transcription factor STAT3 and type I interferons are corepressive insulators for differentiation of follicular helper and T helper 1 cells. Immunity 2014, 40:367-377.
44. Fahey L.M., Wilson E.B., Elsaesser H., Fistonich C.D., McGavern D.B., Brooks D.G. Viral persistence redirects CD4 T cell differentiation toward T follicular helper cells. J Exp Med 2011, 208:987-999.
45. Feng J., Hu X., Guo H., Sun X., Wang J., Xu L., Jiang Z., Xu B., Niu J., Jiang Y. Patients with chronic hepatitis C express a high percentage of CD4(+)CXCR5(+) T follicular helper cells. J Gastroenterol 2012, 47:1048-1056.
46. Lindqvist M., van Lunzen J., Soghoian D.Z., Kuhl B.D., Ranasinghe S., Kranias G., Flanders M.D., Cutler S., Yudanin N., Muller M.I., Davis I., Farber D., Hartjen P., Haag F., Alter G., Schulze Zur Wiesch J., Streeck H. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J Clin Invest 2012, 122:3271-3280.
47. Petrovas C., Yamamoto T., Gerner M.Y., Boswell K.L., Wloka K., Smith E.C., Ambrozak D.R., Sandler N.G., Timmer K.J., Sun X., Pan L., Poholek A., Rao S.S., Brenchley J.M., Alam S.M., Tomaras G.D., Roederer M., Douek D.C., Seder R.A., Germain R.N., Haddad E.K., Koup R.A. CD4 T follicular helper cell dynamics during SIV infection. J Clin Invest 2012, 122:3281-3294.
48. Harker J.A., Lewis G.M., Mack L., Zuniga E.I. Late interleukin-6 escalates T follicular helper cell responses and controls a chronic viral infection. Science 2011, 334:825-829.
49. Herbeuval J.P., Grivel J.C., Boasso A., Hardy A.W., Chougnet C., Dolan M.J., Yagita H., Lifson J.D., Shearer G.M. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 2005, 106:3524-3531.
50. Doitsh G., Galloway N.L., Geng X., Yang Z., Monroe K.M., Zepeda O., Hunt P.W., Hatano H., Sowinski S., Munoz-Arias I., Greene W.C. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 2014, 505:509-514.
51. Chang J.J., Altfeld M. Innate immune activation in primary HIV-1 infection. J Infect Dis 2010, 202(Suppl 2):S297-S301.
52. Rajasuriar R., Khoury G., Kamarulzaman A., French M.A., Cameron P.U., Lewin S.R. Persistent immune activation in chronic HIV infection: do any interventions work?. AIDS 2013, 27:1199-1208.
53. Sandler N.G., Bonsinger S.E., Estes J.D., Zheu R.T., Tharp G.K., Boritz E., Levin D., Wijeyesinghe S., Makamdop K.N., del Prete G.Q., Hill B.J., Timmer J.K., Reiss E., Darko S., Contijoch E., Todd J.P., Silvestri G., Nason M., Norgren R.B., Keele B.F., Rao S., Langer J.A., Lifson J.D., Schreiber G., Douek D.C. Type I IFN responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 2014, 511:601-605.
54. Cha L., Berry C.M., Nolan D., Castley A., Fernandez S., French M.A. Interferon-alpha, immune activation and immune dysfunction in treated HIV infection. Clin Transl Immunol 2014, 3:e10.
55. Appay V., Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. J Pathol 2008, 214:231-241.
56. Klatt N.R., Chomont N., Douek D.C., Deeks S.G. Immune activation and HIV persistence: implications for curative approaches to HIV infection. Immunol Rev 2013, 254:326-342.
57. Heim M.H. 25 years of interferon-based treatment of chronic hepatitis C: an epoch coming to an end. Nat Rev Immunol 2013, 13:535-542.
58. Chen L., Borozan I., Feld J., Sun J., Tannis L.L., Coltescu C., Heathcote J., Edwards A.M., McGilvray I.D. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005, 128:1437-1444.
59. Sarasin-Filipowicz M., Oakeley E.J., Duong F.H., Christen V., Terracciano L., Filipowicz W., Heim M.H. Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 2008, 105:7034-7039.
60. Bohne F., Londono M., Benitez C., Miquesl R., Llordella M., Russo C., Ortiz C., Bonaccorsi-Riani E., Brander C., Bauer T., Protzer U., Jaeckel E., Taubert R., Forns X.N., Berenguer M.M., Rimola A., Lozano J., Sanchez-Fueyo A. HCV-induced immune responses influence the development operational tolerance after liver transplantation in humans. Sci Transl Med 2014, 6:242ra81.
61. Azzoni L., Foulkes A.S., Papasavvas E., Mexas A.M., Lynn K.M., Mounzer K., Tebas P., Jacobson J.M., Frank I., Busch M.P., Deeks S.G., Carrington M., O'Doherty U., Kostman J., Montaner L.J. Pegylated Interferon alfa-2a monotherapy results in suppression of HIV type 1 replication and decreased cell-associated HIV DNA integration. J Infect Dis 2013, 207:213-222.
62. Wilson E.B., Brooks D.G. Interfering with type I interferon: a novel approach to purge persistent viral infection. Cell Cycle 2013, 12:2919-2920.