CD8 T cells in innate immune responses: Using STAT4-Dependent but antigen-independent pathways to gamma interferon during viral infection

mBio

Volumn 5, Issue 5, 2014, Pages

  Suarez Ramirez, Jenny E ^a,c   Tarrio, Margarite L ^a   Kim, Kwangsin ^a,b   Demers, Delia A ^a   Biron, Christine A ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 2 RECEPTOR ALPHA; STAT4 PROTEIN; T LYMPHOCYTE RECEPTOR; STAT4 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; EX VIVO STUDY; IMMUNOREGULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOUSE; MOUSE MODEL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UPREGULATION; VIRUS INFECTION; ANIMAL; ARENAVIRUS INFECTION; IMMUNOLOGY; METABOLISM; MUROMEGALOVIRUS; NATURAL KILLER CELL; SECRETION (PROCESS);

ANIMALS; ARENAVIRIDAE INFECTIONS; CD8-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS INFECTIONS; IMMUNITY, INNATE; INTERFERON-GAMMA; INTERLEUKIN-12; KILLER CELLS, NATURAL; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MICE; MUROMEGALOVIRUS; STAT4 TRANSCRIPTION FACTOR;

EID: 84908441253     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01978-14     Document Type: Article

References (50)

1. Biron CA, Gazzinelli RT. 1995. Effects of IL-12 on immune responses to microbial infections: a key mediator in regulating disease outcome. Curr. Opin. Immunol. 7:485- 496. http://dx.doi.org/10.1016/0952- 7915(95)80093-X.
2. Boehm U, Klamp T, Groot M, Howard JC. 1997. Cellular responses to interferon-gamma. Annu. Rev. Immunol. 15:749-795. http://dx.doi.org/ 10.1146/annurev.immunol.15.1.749.
3. Salazar-Mather TP, Hamilton TA, Biron CA. 2000. A chemokine-tocytokine- to-chemokine cascade critical in antiviral defense. J. Clin. Invest. 105:985-993. http://dx.doi.org/10.1172/JCI9232.
4. Goldszmid RS, Caspar P, Rivollier A, White S, Dzutsev A, Hieny S, Kelsall B, Trinchieri G, Sher A. 2012. NK cell-derived interferon-gamma orchestrates cellular dynamics and the differentiation of monocytes into dendritic cells at the site of infection. Immunity 36:1047-1059. http:// dx.doi.org/10.1016/j.immuni.2012.03.026.
5. _T cell-derived IFN-gamma prevents infection by a second heterologous virus. J. Immunol. 189:5841-5848. http://dx.doi.org/10.4049/jimmunol.1201679.
6. Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A, Gadina M, O'Shea JJ, Biron CA. 2002. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 297:2063-2066. http://dx.doi.org/10.1126/ science.1074900.
7. Miyagi T, Gil MP, Wang X, Louten J, Chu WM, Biron CA. 2007. High basal STAT4 balanced by STAT1 induction to control type 1 interferon effects in natural killer cells. J. Exp. Med. 204:2383-2396. http:// dx.doi.org/10.1084/jem.20070401.
8. Mack EA, Kallal LE, Demers DA, Biron CA. 2011. Type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection. mBio 2(4):e00169-11. http://dx.doi.org/10.1128/mBio.00169-11.
9. Kaplan MH, Sun YL, Hoey T, Grusby MJ. 1996. Impaired IL-12 responses and enhanced development of Th2 cells in Stat4-deficient mice. Nature 382:174-177. http://dx.doi.org/10.1038/382174a0.
10. Lee SH, Fragoso MF, Biron CA. 2012. Cutting edge: a novel mechanism bridging innate and adaptive immunity: IL-12 induction of CD25 to form high-affinity IL-2 receptors on NK cells. J. Immunol. 189:2712-2716. http://dx.doi.org/10.4049/jimmunol.1201528.
11. Gil MP, Ploquin MJ, Watford WT, Lee SH, Kim K, Wang X, Kanno Y, O'Shea JJ, Biron CA. 2012. Regulating type 1 IFN effects in CD8 T cells during viral infections: changing STAT4 and STAT1 expression for function. Blood 120:3718 -3728. http://dx.doi.org/10.1182/blood-2012-05- 428672.
12. Carter LL, Murphy KM. 1999. Lineage-specific requirement for signal transducer and activator of transcription (Stat)4 in interferon gamma production from CD4(_) versus CD8(_) T cells. J. Exp. Med. 189: 1355-1360. http://dx.doi.org/10.1084/jem.189.8.1355.
13. Pien GC, Nguyen KB, Malmgaard L, Satoskar AR, Biron CA. 2002. A unique mechanism for innate cytokine promotion of T cell responses to viral infections. J. Immunol. 169:5827-5837. http://dx.doi.org/10.4049/ jimmunol.169.10.5827.
14. _T-cell activation mediated by cytokines. Proc. Natl. Acad. Sci. U. S. A. 109:9971-9976. http://dx.doi.org/10.1073/pnas.1203543109.
15. Nguyen KB, Biron CA. 1999. Synergism for cytokine-mediated disease during concurrent endotoxin and viral challenges: roles for NK and T cell IFN-gamma production. J. Immunol. 162:5238-5246.
16. _T cells by lipopolysaccharide-induced IL-12 and IL. J. Immunol. 173:6873- 6881. http://dx.doi.org/10.4049/ jimmunol.173.11.6873.
17. _T cells during primary and secondary viral infections. J. Immunol. 174:5936 -5940. http://dx.doi.org/10.4049/ jimmunol.174.10.5936.
18. Murali-Krishna K, Altman JD, Suresh M, Sourdive DJ, Zajac AJ, Miller JD, Slansky J, Ahmed R. 1998. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 8:177-187. http://dx.doi.org/10.1016/S1074-7613(00)80470-7.
19. Raué HP, Beadling C, Haun J, Slifka MK. 2013. Cytokine-mediated programmed proliferation of virus-specific CD8(_) memory T cells. Immunity 38:131-139. http://dx.doi.org/10.1016/j.immuni.2012.09.019.
20. 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. http://dx.doi.org/ 10.4049/jimmunol.177.3.1746.
21. 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. http://dx.doi.org/10.1084/jem.20050821.
22. Cousens LP, Peterson R, Hsu S, Dorner A, Altman JD, Ahmed R, Biron CA. 1999. Two roads diverged: interferon alpha/beta- and interleukin 12-mediated pathways in promoting T cell interferon gamma responses during viral infection. J. Exp. Med. 189:1315-1328. http://dx.doi.org/ 10.1084/jem.189.8.1315.
23. Wang Y, Swiecki M, Cella M, Alber G, Schreiber RD, Gilfillan S, Colonna M. 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. http://dx.doi.org/10.1016/ j.chom.2012.05.003.
24. Orange JS, Biron CA. 1996. An absolute and restricted requirement for IL-12 in natural killer cell IFN-gamma production and antiviral defense. Studies of natural killer and T cell responses in contrasting viral infections. J. Immunol. 156:1138-1142.
25. Mollo SB, Ingram JT, Kress RL, Zajac AJ, Harrington LE. 2014. Virusspecific CD4 and CD8 T cell responses in the absence of Th1-associated transcription factors. J. Leukoc. Biol. 95:705-713. http://dx.doi.org/ 10.1189/jlb.0813429.
26. Orange JS, Biron CA. 1996. Characterization of early IL-12, IFNalphabeta, and TNF effects on antiviral state and NK cell responses during murine cytomegalovirus infection. J. Immunol. 156:4746-4756.
27. Ruzek MC, Miller AH, Opal SM, Pearce BD, Biron CA. 1997. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J. Exp. Med. 185:1185-1192. http://dx.doi.org/ 10.1084/jem.185.7.1185.
28. Pien GC, Satoskar AR, Takeda K, Akira S, Biron CA. 2000. Cutting edge: selective IL-18 requirements for induction of compartmental IFN-gamma responses during viral infection. J. Immunol. 165:4787- 4791. http:// dx.doi.org/10.4049/jimmunol.165.9.4787.
29. Nguyen KB, Salazar-Mather TP, Dalod MY, Van Deusen JB, Wei XQ, Liew FY, Caligiuri MA, Durbin JE, Biron CA. 2002. Coordinated and distinct roles for IFN-alpha/beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169:4279 - 4287. http:// dx.doi.org/10.4049/jimmunol.169.8.4279.
30. Delale T, Paquin A, Asselin-Paturel C, Dalod M, Brizard G, Bates EE, Kastner P, Chan S, Akira S, Vicari A, Biron CA, Trinchieri G, Brière F. 2005. MyD88-dependent and -independent murine cytomegalovirus sensing for IFN-alpha release and initiation of immune responses in vivo. J. Immunol. 175:6723- 6732. http://dx.doi.org/10.4049/ jimmunol.175.10.6723.
31. _T-cell differentiation. Int. Immunol. 22:619-625. http://dx.doi.org/10.1093/ intimm/dxq053.
32. Bacon CM, Petricoin EF III, Ortaldo JR, Rees RC, Larner AC, Johnston JA, O'Shea JJ. 1995. Interleukin 12 induces tyrosine phosphorylation and activation of STAT4 in human lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 92:7307-7311. http://dx.doi.org/10.1073/pnas.92.16.7307.
33. Watford WT, Hissong BD, Durant LR, Yamane H, Muul LM, Kanno Y, Tato CM, Ramos HL, Berger AE, Mielke L, Pesu M, Solomon B, Frucht DM, Paul WE, Sher A, Jankovic D, Tsichlis PN, O'Shea JJ. 2008. Tpl2 kinase regulates T cell interferon-gamma production and host resistance to Toxoplasma gondii. J. Exp. Med. 205:2803-2812. http://dx.doi.org/ 10.1084/jem.20081461.
34. Rossjohn J, Pellicci DG, Patel O, Gapin L, Godfrey DI. 2012. Recognition of CD1d-restricted antigens by natural killer T cells. Nat. Rev. Immunol. 12:845-857. http://dx.doi.org/10.1038/nri3328.
35. Pei B, Vela JL, Zajonc D, Kronenberg M. 2012. Interplay between carbohydrate and lipid in recognition of glycolipid antigens by natural killer T cells. Ann. N. Y. Acad. Sci. 1253:68-79. http://dx.doi.org/10.1111/ j.1749-6632.2011.06435.x.
36. Tyznik AJ, Verma S, Wang Q, Kronenberg M, Benedict CA. 2014. Distinct requirements for activation of NKT and NK cells during viral infection. J. Immunol. 192:3676 -3685. http://dx.doi.org/10.4049/ jimmunol.1300837.
37. Holzapfel KL, Tyznik AJ, Kronenberg M, Hogquist KA. 2014. Antigendependent versus -independent activation of invariant NKT cells during infection. J. Immunol. 192:5490 -5498. http://dx.doi.org/10.4049/ jimmunol.1400722.
38. Vidal SM, Khakoo SI, Biron CA. 2011. Natural killer cell responses during viral infections: flexibility and conditioning of innate immunity by experience. Curr. Opin. Virol. 1:497-512. http://dx.doi.org/10.1016/ j.coviro.2011.10.017.
39. Dokun AO, Kim S, Smith HR, Kang HS, Chu DT, Yokoyama WM. 2001. Specific and nonspecific NK cell activation during virus infection. Nat. Immunol. 2:951-956. http://dx.doi.org/10.1038/ni714.
40. Lee SH, Kim KS, Fodil-Cornu N, Vidal SM, Biron CA. 2009. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 206: 2235-2251. http://dx.doi.org/10.1084/jem.20082387.
41. Biron CA. 2010. Expansion, maintenance, and memory in NK and T cells during viral infections: responding to pressures for defense and regulation. PLoS Pathog. 6(3):e1000816. http://dx.doi.org/10.1371/ journal.ppat.1000816.
42. Eberl G, MacDonald HR. 1998. Rapid death and regeneration of NKT cells in anti-CD3epsilon- or IL-12-treated mice: a major role for bone marrow inNKTcell homeostasis. Immunity 9:345-353. http://dx.doi.org/ 10.1016/S1074-7613(00)80617-2.
43. Wesley JD, Tessmer MS, Chaukos D, Brossay L. 2008. NK cell-like behavior of Valpha14i NK T cells during MCMV infection. PLoS Pathog. 4(7):e1000106. http://dx.doi.org/10.1371/journal.ppat.1000106.
44. Velázquez P, Cameron TO, Kinjo Y, Nagarajan N, Kronenberg M, Dustin ML. 2008. Cutting edge: activation by innate cytokines or microbial antigens can cause arrest of natural killer T cell patrolling of liver sinusoids. J. Immunol. 180:2024 -2028. http://dx.doi.org/10.4049/ jimmunol.180.4.2024.
45. Starbeck-Miller GR, Xue HH, Harty JT. 2014. IL-12 and type I interferon prolong the division of activated CD8 T cells by maintaining high-affinity IL-2 signaling in vivo. J. Exp. Med. 211:105-120. http://dx.doi.org/ 10.1084/jem.20130901.
46. Curtsinger JM, Mescher MF. 2010. Inflammatory cytokines as a third signal for T cell activation. Curr. Opin. Immunol. 22:333-340. http:// dx.doi.org/10.1016/j.coi.2010.02.013.
47. Soudja SM, Ruiz AL, Marie JC, Lauvau G. 2012. Inflammatory monocytes activate memory CD8(_) T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 37:549-562. http://dx.doi.org/10.1016/j.immuni.2012.05.029.
48. Kallal LE, Biron CA. 2013. Changing partners at the dance: variations in STAT concentrations for shaping cytokine function and immune responses to viral infections. JAKSTAT 2(1):e23504. http://dx.doi.org/ 10.4161/jkst.23504.
49. Wu C, Wang X, Gadina M, O'Shea JJ, Presky DH, Magram J. 2000. IL-12 receptor beta 2 (IL-12R beta 2)-deficient mice are defective in IL- 12-mediated signaling despite the presence of high affinity IL-12 binding sites. J. Immunol. 165:6221- 6228. http://dx.doi.org/10.4049/ jimmunol.165.11.6221.
50. Durbin JE, Hackenmiller R, Simon MC, Levy DE. 1996. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 84:443-450.