Overcoming CD4 Th1 Cell Fate Restrictions to Sustain Antiviral CD8 T Cells and Control Persistent Virus Infection

Cell Reports

Volumn 16, Issue 12, 2016, Pages 3286-3296

  Yamada, Douglas H ^b,e   Osokine, Ivan ^b,d   De la Fuente, Justin Rafael ^b   Elsaesser, Heidi J ^a   Brooks, David G ^a,c  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e JANSSEN RESEARCH AND DEVELOPMENT   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; PROGRAMMED DEATH 1 LIGAND 1; CD274 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FATE; CELL ISOLATION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; VIRUS INFECTION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; IMMUNOLOGY; LYMPHOCYTIC CHORIOMENINGITIS; TRANSGENIC MOUSE;

ANIMALS; B7-H1 ANTIGEN; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; INTERLEUKIN-10; LYMPHOCYTIC CHORIOMENINGITIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; TH1 CELLS;

EID: 84990070032     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.08.065     Document Type: Article

References (47)

1. Ahmed, R., Salmi, A., Butler, L.D., Chiller, J.M., Oldstone, M.B., 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 (1984), 521–540.
2. Aubert, R.D., Kamphorst, A.O., Sarkar, S., Vezys, V., Ha, S.J., Barber, D.L., Ye, L., Sharpe, A.H., Freeman, G.J., Ahmed, R., Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc. Natl. Acad. Sci. USA 108 (2011), 21182–21187.
3. Barber, D.L., Wherry, E.J., Masopust, D., Zhu, B., Allison, J.P., Sharpe, A.H., Freeman, G.J., Ahmed, R., Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439 (2006), 682–687.
4. Barber, D.L., Mayer-Barber, K.D., Feng, C.G., Sharpe, A.H., Sher, A., CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J. Immunol. 186 (2011), 1598–1607.
5. Battegay, M., Moskophidis, D., Rahemtulla, A., Hengartner, H., Mak, T.W., Zinkernagel, R.M., Enhanced establishment of a virus carrier state in adult CD4+ T-cell-deficient mice. J. Virol. 68 (1994), 4700–4704.
6. Bergthaler, A., Flatz, L., Verschoor, A., Hegazy, A.N., Holdener, M., Fink, K., Eschli, B., Merkler, D., Sommerstein, R., Horvath, E., et al. Impaired antibody response causes persistence of prototypic T cell-contained virus. PLoS Biol., 7, 2009, e1000080.
7. Brooks, D.G., Teyton, L., Oldstone, M.B., McGavern, D.B., Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J. Virol. 79 (2005), 10514–10527.
8. Brooks, D.G., Trifilo, M.J., Edelmann, K.H., Teyton, L., McGavern, D.B., Oldstone, M.B., Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12 (2006), 1301–1309.
9. Brooks, D.G., Walsh, K.B., Elsaesser, H., Oldstone, M.B., IL-10 directly suppresses CD4 but not CD8 T cell effector and memory responses following acute viral infection. Proc. Natl. Acad. Sci. USA 107 (2010), 3018–3023.
10. Crotty, S., T follicular helper cell differentiation, function, and roles in disease. Immunity 41 (2014), 529–542.
11. Cunningham, C.R., Champhekar, A., Tullius, M.V., Dillon, B.J., Zhen, A., de la Fuente, J.R., Herskovitz, J., Elsaesser, H., Snell, L.M., Wilson, E.B., et al. Type I and Type II Interferon Coordinately Regulate Suppressive Dendritic Cell Fate and Function during Viral Persistence. PLoS Pathog., 12, 2016, e1005356.
12. Day, C.L., Kaufmann, D.E., Kiepiela, P., Brown, J.A., Moodley, E.S., Reddy, S., Mackey, E.W., Miller, J.D., Leslie, A.J., DePierres, C., et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443 (2006), 350–354.
13. Detje, C.N., Meyer, T., Schmidt, H., Kreuz, D., Rose, J.K., Bechmann, I., Prinz, M., Kalinke, U., Local type I IFN receptor signaling protects against virus spread within the central nervous system. J. Immunol. 182 (2009), 2297–2304.
14. Dobrzanski, M.J., Expanding roles for CD4 T cells and their subpopulations in tumor immunity and therapy. Front. Oncol., 3, 2013, 63.
15. Ejrnaes, M., Filippi, C.M., Martinic, M.M., Ling, E.M., Togher, L.M., Crotty, S., von Herrath, M.G., Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203 (2006), 2461–2472.
16. Elsaesser, H., Sauer, K., Brooks, D.G., IL-21 is required to control chronic viral infection. Science 324 (2009), 1569–1572.
17. 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. 208 (2011), 987–999.
18. 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. 47 (2012), 1048–1056.
19. Fröhlich, A., Kisielow, J., Schmitz, I., Freigang, S., Shamshiev, A.T., Weber, J., Marsland, B.J., Oxenius, A., Kopf, M., IL-21R on T cells is critical for sustained functionality and control of chronic viral infection. Science 324 (2009), 1576–1580.
20. Gazzinelli, R.T., Wysocka, M., Hieny, S., Scharton-Kersten, T., Cheever, A., Kühn, R., Müller, W., Trinchieri, G., Sher, A., In the absence of endogenous IL-10, mice acutely infected with Toxoplasma gondii succumb to a lethal immune response dependent on CD4+ T cells and accompanied by overproduction of IL-12, IFN-gamma and TNF-alpha. J. Immunol. 157 (1996), 798–805.
21. Gerlach, J.T., Diepolder, H.M., Jung, M.C., Gruener, N.H., Schraut, W.W., Zachoval, R., Hoffmann, R., Schirren, C.A., Santantonio, T., Pape, G.R., Recurrence of hepatitis C virus after loss of virus-specific CD4(+) T-cell response in acute hepatitis C. Gastroenterology 117 (1999), 933–941.
22. Haynes, N.M., Allen, C.D., Lesley, R., Ansel, K.M., Killeen, N., Cyster, J.G., Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol. 179 (2007), 5099–5108.
23. Hegazy, A.N., Peine, M., Helmstetter, C., Panse, I., Fröhlich, A., Bergthaler, A., Flatz, L., Pinschewer, D.D., Radbruch, A., Löhning, M., Interferons direct Th2 cell reprogramming to generate a stable GATA-3(+)T-bet(+) cell subset with combined Th2 and Th1 cell functions. Immunity 32 (2010), 116–128.
24. Kao, C., Oestreich, K.J., Paley, M.A., Crawford, A., Angelosanto, J.M., Ali, M.A., Intlekofer, A.M., Boss, J.M., Reiner, S.L., Weinmann, A.S., Wherry, E.J., Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat. Immunol. 12 (2011), 663–671.
25. Lichterfeld, M., Kaufmann, D.E., Yu, X.G., Mui, S.K., Addo, M.M., Johnston, M.N., Cohen, D., Robbins, G.K., Pae, E., Alter, G., et al. Loss of HIV-1-specific CD8+ T cell proliferation after acute HIV-1 infection and restoration by vaccine-induced HIV-1-specific CD4+ T cells. J. Exp. Med. 200 (2004), 701–712.
26. 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., et al. Expansion of HIV-specific T follicular helper cells in chronic HIV infection. J. Clin. Invest. 122 (2012), 3271–3280.
27. MacDonald, A.S., Patton, E.A., La Flamme, A.C., Araujo, M.I., Huxtable, C.R., Bauman, B., Pearce, E.J., Impaired Th2 development and increased mortality during Schistosoma mansoni infection in the absence of CD40/CD154 interaction. J. Immunol. 168 (2002), 4643–4649.
28. Matloubian, M., Concepcion, R.J., Ahmed, R., CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J. Virol. 68 (1994), 8056–8063.
29. Moeller, M., Kershaw, M.H., Cameron, R., Westwood, J.A., Trapani, J.A., Smyth, M.J., Darcy, P.K., Sustained antigen-specific antitumor recall response mediated by gene-modified CD4+ T helper-1 and CD8+ T cells. Cancer Res. 67 (2007), 11428–11437.
30. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., O'Garra, A., Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19 (2001), 683–765.
31. Nance, J.P., Bélanger, S., Johnston, R.J., Takemori, T., Crotty, S., Cutting edge: T follicular helper cell differentiation is defective in the absence of Bcl6 BTB repressor domain function. J. Immunol. 194 (2015), 5599–5603.
32. 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 13 (2013), 652–664.
33. Ng, C.T., Sullivan, B.M., Teijaro, J.R., Lee, A.M., Welch, M., Rice, S., Sheehan, K.C., Schreiber, R.D., Oldstone, M.B., Blockade of interferon Beta, but not interferon alpha, signaling controls persistent viral infection. Cell Host Microbe 17 (2015), 653–661.
34. Nguyen, L.T., Ohashi, P.S., Clinical blockade of PD1 and LAG3–potential mechanisms of action. Nat. Rev. Immunol. 15 (2015), 45–56.
35. Nishimura, T., Iwakabe, K., Sekimoto, M., Ohmi, Y., Yahata, T., Nakui, M., Sato, T., Habu, S., Tashiro, H., Sato, M., Ohta, A., Distinct role of antigen-specific T helper type 1 (Th1) and Th2 cells in tumor eradication in vivo. J. Exp. Med. 190 (1999), 617–627.
36. 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. USA 111 (2014), 7409–7414.
37. 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., et al. CD4 T follicular helper cell dynamics during SIV infection. J. Clin. Invest. 122 (2012), 3281–3294.
38. Poholek, A.C., Hansen, K., Hernandez, S.G., Eto, D., Chandele, A., Weinstein, J.S., Dong, X., Odegard, J.M., Kaech, S.M., Dent, A.L., et al. In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 185 (2010), 313–326.
39. Rosenberg, E.S., Billingsley, J.M., Caliendo, A.M., Boswell, S.L., Sax, P.E., Kalams, S.A., Walker, B.D., Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278 (1997), 1447–1450.
40. Sun, J., Madan, R., Karp, C.L., Braciale, T.J., Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15 (2009), 277–284.
41. Thimme, R., Oldach, D., Chang, K.M., Steiger, C., Ray, S.C., Chisari, F.V., Determinants of viral clearance and persistence during acute hepatitis C virus infection. J. Exp. Med. 194 (2001), 1395–1406.
42. Wherry, E.J., Kurachi, M., Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15 (2015), 486–499.
43. Wherry, E.J., Blattman, J.N., Murali-Krishna, K., van der Most, R., Ahmed, R., Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 77 (2003), 4911–4927.
44. 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 11 (2012), 481–491.
45. 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 340 (2013), 202–207.
46. Yi, J.S., Du, M., Zajac, A.J., A vital role for interleukin-21 in the control of a chronic viral infection. Science 324 (2009), 1572–1576.
47. ∗). Annu. Rev. Immunol. 28 (2010), 445–489.