Exhausted cd8 t cells downregulate the il-18 receptor and become unresponsive to inflammatory cytokines and bacterial co-infections

PLoS Pathogens

Volumn 7, Issue 9, 2011, Pages

  Ingram, Jennifer T ^a,b   Yi, John S ^b,c   Zajac, Allan J ^b  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 18 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; RHODAMINE 123; AUTACOID; CYTOKINE; IL18R1 PROTEIN, MOUSE; IL2RA PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL INFECTION; BONE MARROW; CD8+ T LYMPHOCYTE; CELL FATE; CONTROLLED STUDY; DOWN REGULATION; IMMUNE RESPONSE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SPLEEN CELL; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DOWN-REGULATION; INFLAMMATION MEDIATORS; INTERLEUKIN-18 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, KNOCKOUT;

EID: 80053452075     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002273     Document Type: Article

References (42)

1. Cox MA, Zajac AJ, (2010) Shaping successful and unsuccessful CD8 T cell responses following infection. J Biomed Biotechnol 2010 pp. 159152.
2. Cui W, Kaech SM, (2010) Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol Rev 236: 151-166.
3. Sareneva T, Matikainen S, Kurimoto M, Julkunen I, (1998) Influenza A virus-induced IFN-alpha/beta and IL-18 synergistically enhance IFN-gamma gene expression in human T cells. J Immunol 160: 6032-6038.
4. Cousens LP, Peterson R, Hsu S, Dorner A, Altman JD, et al. (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.
5. Lertmemongkolchai G, Cai G, Hunter CA, Bancroft GJ, (2001) Bystander activation of CD8+ T cells contributes to the rapid production of IFN-gamma in response to bacterial pathogens. J Immunol 166: 1097-1105.
6. Berg RE, Crossley E, Murray S, Forman J, (2003) Memory CD8+ T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J Exp Med 198: 1583-1593.
7. Kambayashi T, Assarsson E, Lukacher AE, Ljunggren HG, Jensen PE, (2003) Memory CD8+ T cells provide an early source of IFN-gamma. J Immunol 170: 2399-2408.
8. Raue HP, Brien JD, Hammarlund E, Slifka MK, (2004) Activation of virus-specific CD8+ T cells by lipopolysaccharide-induced IL-12 and IL-18. J Immunol 173: 6873-6881.
9. Beadling C, Slifka MK, (2005) Differential regulation of virus-specific T-cell effector functions following activation by peptide or innate cytokines. Blood 105: 1179-1186.
10. Berg RE, Forman J, (2006) The role of CD8 T cells in innate immunity and in antigen non-specific protection. Curr Opin Immunol 18: 338-343.
11. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, et al. (2003) IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J Immunol 170: 5464-5469.
12. Shin H, Wherry EJ, (2007) CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 19: 408-415.
13. Yi JS, Cox MA, Zajac AJ, (2010) T-cell exhaustion: characteristics, causes and conversion. Immunology 129: 474-481.
14. Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, et al. (2007) Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
15. Mackerness KJ, Cox MA, Lilly LM, Weaver CT, Harrington LE, et al. (2010) Pronounced virus-dependent activation drives exhaustion but sustains IFN-gamma transcript levels. J Immunol 185: 3643-3651.
16. Zajac AJ, Blattman JN, Murali-Krishna K, Sourdive DJ, Suresh M, et al. (1998) Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med 188: 2205-2213.
17. Fuller MJ, Khanolkar A, Tebo AE, Zajac AJ, (2004) Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J Immunol 172: 4204-4214.
18. Zhou S, Ou R, Huang L, Price GE, Moskophidis D, (2004) Differential tissue-specific regulation of antiviral CD8+ T-cell immune responses during chronic viral infection. J Virol 78: 3578-3600.
19. 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.
20. Fuller MJ, Zajac AJ, (2003) Ablation of CD8 and CD4 T cell responses by high viral loads. J Immunol 170: 477-486.
21. Turtle CJ, Swanson HM, Fujii N, Estey EH, Riddell SR, (2009) A distinct subset of self-renewing human memory CD8+ T cells survives cytotoxic chemotherapy. Immunity 31: 834-844.
22. Schinkel AH, Jonker JW, (2003) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55: 3-29.
23. Haining WN, Ebert BL, Subrmanian A, Wherry EJ, Eichbaum Q, et al. (2008) Identification of an evolutionarily conserved transcriptional signature of CD8 memory differentiation that is shared by T and B cells. J Immunol 181: 1859-1868.
24. Luckey CJ, Bhattacharya D, Goldrath AW, Weissman IL, Benoist C, et al. (2006) Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc Natl Acad Sci U S A 103: 3304-3309.
25. Haring JS, Harty JT, (2009) Interleukin-18-related genes are induced during the contraction phase but do not play major roles in regulating the dynamics or function of the T-cell response to Listeria monocytogenes infection. Infect Immun 77: 1894-1903.
26. Li W, Kashiwamura S, Ueda H, Sekiyama A, Okamura H, (2007) Protection of CD8+ T cells from activation-induced cell death by IL-18. J Leukoc Biol 82: 142-151.
27. Iwai Y, Hemmi H, Mizenina O, Kuroda S, Suda K, et al. (2008) An IFN-gamma-IL-18 signaling loop accelerates memory CD8+ T cell proliferation. PLoS One 3: e2404.
28. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R, (2004) Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A 101: 16004-16009.
29. Shin H, Blackburn SD, Blattman JN, Wherry EJ, (2007) Viral antigen and extensive division maintain virus-specific CD8 T cells during chronic infection. J Exp Med 204: 941-949.
30. Fuller MJ, Hildeman DA, Sabbaj S, Gaddis DE, Tebo AE, et al. (2005) Cutting edge: emergence of CD127high functionally competent memory T cells is compromised by high viral loads and inadequate T cell help. J Immunol 174: 5926-5930.
31. Lang KS, Recher M, Navarini AA, Harris NL, Lohning M, et al. (2005) Inverse correlation between IL-7 receptor expression and CD8 T cell exhaustion during persistent antigen stimulation. Eur J Immunol 35: 738-745.
32. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, et al. (2003) Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 77: 11708-11717.
33. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
34. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, et al. (2004) Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 200: 761-770.
35. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
36. Jiang W, Lederman MM, Hunt P, Sieg SF, Haley K, et al. (2009) Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis 199: 1177-1185.
37. Virgin HW, Wherry EJ, Ahmed R, (2009) Redefining chronic viral infection. Cell 138: 30-50.
38. Blanden RV, Mims CA, (1973) Macrophage activation in mice infected with ectromelia or lymphocytic choriomeningitis viruses. Aust J Exp Biol Med Sci 51: 393-398.
39. Barton ES, White DW, Cathelyn JS, Brett-McClellan KA, Engle M, et al. (2007) Herpesvirus latency confers symbiotic protection from bacterial infection. Nature 447: 326-329.
40. 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.
41. Sun Y, Brown NK, Ruddy MJ, Miller ML, Lee Y, et al. (2009) B and T lymphocyte attenuator tempers early infection immunity. J Immunol 183: 1946-1951.
42. Yi JS, Ingram JT, Zajac AJ, (2010) IL-21 deficiency influences CD8 T cell quality and recall responses following an acute viral infection. J Immunol 185: 4835-4845.