IL-12 is required for mTOR regulation of memory CTLs during viral infection

Genes and Immunity

Volumn 15, Issue 6, 2014, Pages 413-423

  Garcia, K ^a   Sun, Z ^a   Mattson, E ^a   Li, L ^a   Smyth, K ^a   Xiao, Z ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR BETA2; L SELECTIN; MAMMALIAN TARGET OF RAPAMYCIN; RAPAMYCIN; STAT4 PROTEIN; TRANSCRIPTION FACTOR T BET; IMMUNOSUPPRESSIVE AGENT; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 2; MTOR PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T-BOX TRANSCRIPTION FACTOR TBX21; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; DRUG MEGADOSE; IMMUNE RESPONSE; IMMUNOSTIMULATION; LOW DRUG DOSE; LYMPHOCYTE PROLIFERATION; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VACCINIA VIRUS; VIRUS INFECTION; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL PROLIFERATION; DEFICIENCY; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE; VACCINIA; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; IMMUNOLOGIC MEMORY; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-2; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, INTERLEUKIN-12; SIGNAL TRANSDUCTION; SIROLIMUS; STAT4 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TOR SERINE-THREONINE KINASES; VACCINIA; VACCINIA VIRUS;

EID: 84901730344     PISSN: 14664879     EISSN: 14765470     Source Type: Journal    
DOI: 10.1038/gene.2014.33     Document Type: Article

References (75)

1. Wherry EJ, Teichgraber V, Becker T.C., Masopust D., Kaech SM, Antia R et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003; 4: 225-234.
2. Kaech SM, Wherry EJ, Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002; 2: 251-262.
3. Mescher MF, Curtsinger JM, Agarwal P, Casey K.A., Gerner M., Hammerbeck CD et al. Signals required for programming effector and memory development by CD8 + T cells. Immunol Rev 2006; 211: 81-92.
4. Ahmed R, Bevan MJ, Reiner S.L., Fearon DT. The precursors of memory: models and controversies. Nat Rev Immunol 2009; 9: 662-668.
5. Jameson SC, Masopust D. Diversity in T cell memory: an embarrassment of riches. Immunity 2009; 31: 859-871.
6. Curtsinger JM, Mescher MF Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol 2010; 22: 333-340.
7. Williams MA, Bevan MJ Effector and memory CTL differentiation. Annu Rev Immunol 2007; 25: 171-192.
8. Kolumam GA, 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.
9. Xiao Z, Casey KA, Jameson S.C., Curtsinger JM, Mescher MF. Programming for CD8 T cell memory development requires IL-12 or type I IFN. J Immunol 2009; 182: 2786-2794.
10. Li X, Garcia K, Sun Z., Xiao Z. Temporal regulation of rapamycin on memory CTL programming by IL-12. PLoS ONE 2011; 6: e25177.
11. Rao RR, Li Q, Odunsi K., Shrikant PA. The mTOR kinase determines effector versus memory CD8 + T cell fate by regulating the expression of transcription factors T-bet and Eomesodermin. Immunity 2010; 32: 67-78.
12. Jinushi M, Tahara H. Cytokine gene-mediated immunotherapy: current status and future perspectives. Cancer Sci 2009; 100: 1389-1396.
13. Schmidt CS, Mescher MF Adjuvant effect of IL-12: conversion of peptide antigen administration from tolerizing to immunizing for CD8 + T cells in vivo. J Immunol 1999; 163: 2561-2567.
14. Schmidt CS, Mescher MF Peptide antigen priming of naive, but not memory, CD8 T cells requires a third signal that can be provided by IL-12. J Immunol 2002; 168: 5521-5529.
15. Rubinstein MP, Cloud CA, Garrett T.E., Moore CJ, Schwartz KM, Johnson CB et al. Ex vivo interleukin-12-priming during CD8(+) T cell activation dramatically improves adoptive T cell transfer antitumor efficacy in a lymphodepleted host. J Am Coll Surg 2012; 214: 700-707.
16. Sabel MS, Arora A, Su G., Griffith KA, Mathiowitz E, Reineke JJ et al. Generation of a tumor-specific systemic response after intratumoral injection of IL-12 and IL-18-loaded polylactic acid microspheres. J Immunother 2007; 30: 808-816.
17. Gerner MY, Heltemes-Harris LM, Fife B.T., Mescher MF. Cutting edge: IL-12 and type I IFN differentially program CD8 T cells for programmed death 1 re-expression levels and tumor control. J Immunol 2013; 191: 1011-1015.
18. Chi H. Regulation and function of mTOR signalling in T cell fate decisions. Nat Rev Immunol 2012; 12: 325-338.
19. Thomson AW, Turnquist HR, Raimondi G. Immunoregulatory functions of mTOR inhibition. Nat Rev Immunol 2009; 9: 324-337.
20. Katzman SD, O'Gorman WE, Villarino AV, Gallo E, Friedman R.S., Krummel MF et al. Duration of antigen receptor signaling determines T-cell tolerance or activation. Proc Natl Acad Sci USA 2010; 107: 18085-18090.
21. Turner MS, Kane LP, Morel PA Dominant role of antigen dose in CD4 + Foxp3 + regulatory T cell induction and expansion. J Immunol 2009; 183: 4895-4903.
22. Delgoffe GM, Kole TP, Zheng Y, Zarek P.E., Matthews KL, Xiao B et al. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity 2009; 30: 832-844.
23. Delgoffe GM, Pollizzi KN, Waickman A.T., Heikamp E., Meyers DJ, Horton MR et al. The kinase mTOR regulates the differentiation of helper T cells through the selective activation of signaling by mTORC1 and mTORC2. Nat Immunol 2011; 12: 295-303.
24. Powell JD, Delgoffe GM The mammalian target of rapamycin: linking T cell differentiation, function, and metabolism. Immunity 2010; 33: 301-311.
25. Finlay D, Cantrell DA Metabolism, migration and memory in cytotoxic T cells. Nat Rev Immunol 2011; 11: 109-117.
26. Araki K, Turner AP, Shaffer V.O., Gangappa S., Keller SA, Bachmann MF et al. mTOR regulates memory CD8 T-cell differentiation. Nature 2009; 460: 108-112.
27. Pearce EL, Walsh MC, Cejas P.J., Harms GM, Shen H, Wang LS et al. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 2009; 460: 103-107.
28. Xiao Z, Mescher MF, Jameson SC Detuning CD8 T cells: down-regulation of CD8 expression, tetramer binding, and response during CTL activation. J Exp Med 2007; 204: 2667-2677.
29. Smyth K, Garcia K, Sun Z., Tuo W, Xiao Z. Repetitive peptide boosting progressively enhances functional memory CTLs. Biochem Biophys Res Commun 2012; 424: 635-640.
30. Mueller SN, Ahmed R. High antigen levels are the cause of T cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA 2009; 106: 8623-8628.
31. Wherry EJ, Ha SJ, Kaech S.M., Haining WN, Sarkar S, Kalia V et al. Molecular signature of CD8 + T cell exhaustion during chronic viral infection. Immunity 2007; 27: 670-684.
32. Day CL, Kaufmann DE, Kiepiela P, Brown J.A., Moodley ES, Reddy S et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443: 350-354.
33. Harty JT, Badovinac VP Shaping and reshaping CD8 + T-cell memory. Nat Rev Immunol 2008; 8: 107-119.
34. Keppler SJ, Aichele P. Signal 3 requirement for memory CD8 + T-cell activation is determined by the infectious pathogen. Eur J Immunol 2011; 41: 3176-3186.
35. Jacobson NG, Szabo SJ, Weber-Nordt RM, Zhong Z., Schreiber RD, Darnell Jr. JE et al. Interleukin 12 signaling in T helper type 1 (Th1) cells involves tyrosine phosphorylation of signal transducer and activator of transcription (Stat) 3 and Stat4. J Exp Med 1995; 181: 1755-1762.
36. Zhong Z, Wen Z, Darnell Jr JE. Stat3 and Stat4: members of the family of signal transducers and activators of transcription. Proc Natl Acad Sci USA 1994; 91: 4806-4810.
37. Watford WT, Moriguchi M, Morinobu A., O'Shea JJ. The biology of IL-12: coordinating innate and adaptive immune responses. Cytokine Growth Factor Rev 2003; 14: 361-368.
38. Kindt TJ, Goldsby RA, Osborne BA Kuby Immunology. 6th edn. (W.H. Freeman and Company: New York, NY, USA, 2007).
39. Szabo SJ, Dighe AS, Gubler U, Murphy KM Regulation of the interleukin (IL)-12R b2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J Exp Med 1997; 185: 817-824.
40. Agarwal P, Raghavan A, Nandiwada S.L., Curtsinger JM, Bohjanen PR, Mueller DL et al. Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J Immunol 2009; 183: 1695-1704.
41. Gil MP, Ploquin MJ, Watford W.T., Lee SH, Kim K, Wang X et al. Regulating type 1 IFN effects in CD8 T cells during viral infections: changing STAT4 and STAT1 expression for function. Blood 2012; 120: 3718-3728.
42. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol 2005; 5: 375-386.
43. Nguyen KB, Watford WT, Salomon R, Hofmann S.R., Pien GC, Morinobu A et al. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 2002; 297: 2063-2066.
44. Banerjee A, Gordon SM, Intlekofer A.M., Paley MA, Mooney EC, Lindsten T et al. Cutting edge: The transcription factor eomesodermin enables CD8 + T cells to compete for the memory cell niche. J Immunol 2010; 185: 4988-4992.
45. Szabo SJ, Kim ST, Costa G.L., Zhang X., Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000; 100: 655-669.
46. Sun Z, Smyth K, Garcia K., Mattson E, Li L, Xiao Z. Nicotine inhibits memory CTL programming. PLoS ONE 2013; 8: e68183.
47. van Den Broek M, Bachmann MF, Kohler G, Barner M, Escher R, Zinkernagel R et al. IL-4 and IL-10 antagonize IL-12-mediated protection against acute vaccinia virus infection with a limited role of IFN-gamma and nitric oxide synthetase 2. J Immunol 2000; 164: 371-378.
48. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol 2003; 3: 133-146.
49. Obar JJ, Crist SG, Leung E.K., Usherwood EJ. IL-15-independent proliferative renewal of memory CD8 + T cells in latent gammaherpesvirus infection. J Immunol 2004; 173: 2705-2714.
50. Sandau MM, Kohlmeier JE, Woodland D.L., Jameson SC. IL-15 regulates both quantitative and qualitative features of the memory CD8 T cell pool. J Immunol 2010; 184: 35-44.
51. Melchionda F, Fry TJ, Milliron M.J., McKirdy MA, Tagaya Y, Mackall CL. Adjuvant IL-7 or IL-15 overcomes immunodominance and improves survival of the CD8 + memory cell pool. J Clin Invest 2005; 115: 1177-1187.
52. Klonowski KD, Williams KJ, Marzo A.L., Lefrancois L. Cutting edge: IL-7-independent regulation of IL-7 receptor alpha expression and memory CD8 T cell development. J Immunol 2006; 177: 4247-4251.
53. Joshi NS, Cui W, Chandele A., Lee HK, Urso DR, Hagman J et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007; 27: 281-295.
54. Jonjic S. Functional plasticity and robustness are essential characteristics of biological systems: lessons learned from KLRG1-deficient mice. Eur J Immunol 2010; 40: 1241-1243.
55. Masopust D. Developing an HIV cytotoxic T-lymphocyte vaccine: issues of CD8 T-cell quantity, quality and location. J Intern Med 2009; 265: 125-137.
56. Woodland DL. Jump-starting the immune system: prime-boosting comes of age. Trends Immunol 2004; 25: 98-104.
57. Ramshaw IA, Ramsay AJ The prime-boost strategy: exciting prospects for improved vaccination. Immunol Today 2000; 21: 163-165.
58. Brierley MM, Fish EN Review: IFN-alpha/beta receptor interactions to biologic outcomes: understanding the circuitry. J Interferon Cytokine Res 2002; 22: 835-845.
59. Bacon CM, McVicar DW, Ortaldo J.R., Rees RC, O'Shea JJ, Johnston JA. Interleukin 12 (IL-12) induces tyrosine phosphorylation of JAK2 and TYK2: differential use of Janus family tyrosine kinases by IL-2 and IL-12. J Exp Med 1995; 181: 399-404.
60. Muller M, Briscoe J, Laxton C., Guschin D, Ziemiecki A, Silvennoinen O et al. The protein tyrosine kinase JAK1 complements defects in interferon-alpha/beta and - gamma signal transduction. Nature 1993; 366: 129-135.
61. Laurence A, Pesu M, Silvennoinen O., O'Shea J. JAK kinases in health and disease: an update. Open Rheumatoly J 2012; 6: 232-244.
62. Neubauer H, Cumano A, Muller M., Wu H, Huffstadt U, Pfeffer K. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 1998; 93: 397-409.
63. O'Shea JJ. Jaks, STATs, cytokine signal transduction, and immunoregulation: are we there yet? Immunity 1997; 7: 1-11.
64. Pazdrak K, Stafford S, Alam R. The activation of the Jak-STAT 1 signaling pathway by IL-5 in eosinophils. J Immunol 1995; 155: 397-402.
65. Silvennoinen O, Witthuhn BA, Quelle F.W., Cleveland JL, Yi T, Ihle JN. Structure of the murine Jak2 protein-tyrosine kinase and its role in interleukin 3 signal transduction. Proc Natl Acad Sci USA 1993; 90: 8429-8433.
66. Argetsinger LS, Campbell GS, Yang X, Witthuhn B.A., Silvennoinen O., Ihle JN et al. Identification of JAK2 as a growth hormone receptor-associated tyrosine kinase. Cell 1993; 74: 237-244.
67. Belz GT, Wilson NS, Smith C.M., Mount AM, Carbone FR, Heath WR. Bone marrow-derived cells expand memory CD8 + T cells in response to viral infections of the lung and skin. Eur J Immunol 2006; 36: 327-335.
68. Zammit DJ, Cauley LS, Pham Q.M., Lefrancois L. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 2005; 22: 561-570.
69. Borowski AB, Boesteanu AC, Mueller Y.M., Carafides C., Topham DJ, Altman JD et al. Memory CD8 + T cells require CD28 costimulation. J Immunol 2007; 179: 6494-6503.
70. Woodberry T, Gardner J, Elliott S.L., Leyrer S., Purdie DM, Chaplin P et al. Prime boost vaccination strategies: CD8 T cell numbers, protection, and Th1 bias. J Immunol 2003; 170: 2599-2604.
71. Speiser DE, Lienard D, Rufer N., Rubio-Godoy V, Rimoldi D, Lejeune F et al. Rapid and strong human CD8 + T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest 2005; 115: 739-746.
72. Hogquist K, Jameson S, Heath W., Howard J, Bevan M, Carbone F. T cell receptor antagonist peptides induce positive selection. Cell 1994; 76: 17-27.
73. Karupiah G, Coupar B, Ramshaw I., Boyle D, Blanden R, Andrew M. Vaccinia virusmediated damage of murine ovaries and protection by virus-expressed inter-leukin-2. Immunol Cell Biol 1990; 68(Pt 5): 325-333.
74. Zhao Y, Adams YF, Croft M. Preferential replication of vaccinia virus in the ovaries is independent of immune regulation through IL-10 and TGF-beta. Viral Immunol 2011; 24: 387-396.
75. Xiao Z, Curtsinger JM, Prlic M, Jameson S.C., Mescher MF. The CD8 T cell response to vaccinia virus exhibits site-dependent heterogeneity of functional responses. Int Immunol 2007; 19: 733-743.