Activated iNKT cells promote memory CD8+ T cell differentiation during viral infection

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Reilly, Emma C ^a   Thompson, Elizabeth A ^a   Aspeslagh, Sandrine ^b   Wands, Jack R ^a   Elewaut, Dirk ^b   Brossay, Laurent ^a  

^a BROWN UNIVERSITY   (United States)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; ALPHA-GALACTOSYLCERAMIDE; CYTOKINE; GALACTOSYLCERAMIDE; IMMUNOLOGICAL ADJUVANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; CENTRAL MEMORY CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE MODEL; EFFECTOR CD8+ T LYMPHOCYTE; IMMUNE RESPONSE; IMMUNITY; INFLAMMATION; INHIBITION KINETICS; INVARIANT NATURAL KILLER T CELL; LYMPHOCYTE COUNT; MEMORY T LYMPHOCYTE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; T LYMPHOCYTE ACTIVATION; VIRUS REACTIVATION; ANIMAL; BLOOD; C57BL MOUSE; CD8+ T LYMPHOCYTE; FLOW CYTOMETRY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; NONPARAMETRIC TEST; VIROLOGY;

CYTOMEGALOVIRUS; MAIZE CHLOROTIC MOTTLE VIRUS;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; CYTOMEGALOVIRUS INFECTIONS; FLOW CYTOMETRY; GALACTOSYLCERAMIDES; IMMUNOLOGIC MEMORY; INFLAMMATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; STATISTICS, NONPARAMETRIC;

EID: 84861367072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037991     Document Type: Article

References (55)

1. Dubensky TW Jr, Reed SG, (2010) Adjuvants for cancer vaccines. Semin Immunol 22: 155-161.
2. Caskey M, Lefebvre Fß, Filali-Mouhim A, Cameron MJ, Goulet J-P, et al. (2011) Synthetic double-stranded RNA induces innate immune responses similar to a live viral vaccine in humans. The Journal of Experimental Medicine 208: 2357-2366.
3. Butler NS, Nolz JC, Harty JT, (2011) Immunologic considerations for generating memory CD8 T cells through vaccination. Cell Microbiol 13: 925-933.
4. Wherry EJ, Ahmed R, (2004) Memory CD8 T-Cell Differentiation during Viral Infection. Journal of Virology 78: 5535-5545.
5. Zhang N, Bevan MJ, (2011) CD8(+) T cells: foot soldiers of the immune system. Immunity 35: 161-168.
6. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, et al. (2007) Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27: 281-295.
7. Lefrancois L, Obar JJ, (2010) Once a killer, always a killer: from cytotoxic T cell to memory cell. Immunol Rev 235: 206-218.
8. Gonzalez-Aseguinolaza G, Van Kaer L, Bergmann CC, Wilson JM, Schmieg J, et al. (2002) Natural killer T cell ligand alpha-galactosylceramide enhances protective immunity induced by malaria vaccines. J Exp Med 195: 617-624.
9. Huang Y, Chen A, Li X, Chen Z, Zhang W, et al. (2008) Enhancement of HIV DNA vaccine immunogenicity by the NKT cell ligand, alpha-galactosylceramide. Vaccine 26: 1807-1816.
10. Galli G, Pittoni P, Tonti E, Malzone C, Uematsu Y, et al. (2007) Invariant NKT cells sustain specific B cell responses and memory. Proc Natl Acad Sci U S A 104: 3984-3989.
11. Kamijuku, (2008) Mechanism of NKT cell activation by intranasal coadministration of alpha-galactosylceramide, which can induce cross-protection against influenza viruses. Mucosal Immunology.
12. Ho LP, Denney L, Luhn K, Teoh D, Clelland C, et al. (2008) Activation of invariant NKT cells enhances the innate immune response and improves the disease course in influenza A virus infection. Eur J Immunol 38: 1913-1922.
13. Renneson J, Guabiraba R, Maillet I, Marques RE, Ivanov S, et al. (2011) A detrimental role for invariant natural killer T cells in the pathogenesis of experimental dengue virus infection. Am J Pathol 179: 1872-1883.
14. Kronenberg M, (2004) Toward an Understanding of NKT Cell Biology: Progress and Paradoxes. Annu Rev Immunol 23: 877-900.
15. Wesley JD, Robbins SH, Sidobre S, Kronenberg M, Terrizzi S, et al. (2005) Cutting edge: IFN-gamma signaling to macrophages is required for optimal Valpha14i NK T/NK cell cross-talk. J Immunol 174: 3864-3868.
16. Guillonneau C, Mintern JD, Hubert Fß-X, Hurt AC, Besra GS, et al. (2009) Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proceedings of the National Academy of Sciences 106: 3330-3335.
17. Jordan MC, Shanley JD, Stevens JG, (1977) Immunosuppression reactivates and disseminates latent murine cytomegalovirus. J Gen Virol 37: 419-423.
18. Polic B, Hengel H, Krmpotic A, Trgovcich J, Pavic I, et al. (1998) Hierarchical and Redundant Lymphocyte Subset Control Precludes Cytomegalovirus Replication during Latent Infection. The Journal of Experimental Medicine 188: 1047-1054.
19. Yokoyama WM, Kim S, French AR, (2004) The dynamic life of natural killer cells. Annu Rev Immunol 22: 405-429.
20. Henson D, Strano AJ, (1972) Mouse cytomegalovirus. Necrosis of infected and morphologically normal submaxillary gland acinar cells during termination of chronic infection. Am J Pathol 68: 183-202.
21. Jonjic S, Mutter W, Weiland F, Reddehase MJ, Koszinowski UH, (1989) Site-restricted persistent cytomegalovirus infection after selective long-term depletion of CD4+ T lymphocytes. J Exp Med 169: 1199-1212.
22. Krug A, French AR, Barchet W, Fischer JA, Dzionek A, et al. (2004) TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function. Immunity 21: 107-119.
23. Kakimi K, Guidotti LG, Koezuka Y, Chisari FV, (2000) Natural killer T cell activation inhibits hepatitis B virus replication in vivo. J Exp Med 192: 921-930.
24. Exley MA, Bigley NJ, Cheng O, Tahir SM, Smiley ST, et al. (2001) CD1d-reactive T-cell activation leads to amelioration of disease caused by diabetogenic encephalomyocarditis virus. J Leukoc Biol 69: 713-718.
25. Youn HJ, Ko SY, Lee KA, Ko HJ, Lee YS, et al. (2007) A single intranasal immunization with inactivated influenza virus and alpha-galactosylceramide induces long-term protective immunity without redirecting antigen to the central nervous system. Vaccine 25: 5189-5198.
26. Ko SY, Ko HJ, Chang WS, Park SH, Kweon MN, et al. (2005) alpha-Galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J Immunol 175: 3309-3317.
27. Johnson TR, Hong S, Van Kaer L, Koezuka Y, Graham BS, (2002) NK T cells contribute to expansion of CD8(+) T cells and amplification of antiviral immune responses to respiratory syncytial virus. J Virol 76: 4294-4303.
28. van Dommelen SL, Tabarias HA, Smyth MJ, Degli-Esposti MA, (2003) Activation of natural killer (NK) T cells during murine cytomegalovirus infection enhances the antiviral response mediated by NK cells. J Virol 77: 1877-1884.
29. Munks MW, Cho KS, Pinto AK, Sierro S, Klenerman P, et al. (2006) Four distinct patterns of memory CD8 T cell responses to chronic murine cytomegalovirus infection. J Immunol 177: 450-458.
30. Snyder CM, Cho KS, Bonnett EL, van Dommelen S, Shellam GR, et al. (2008) Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29: 650-659.
31. Sierro S, Rothkopf R, Klenerman P, (2005) Evolution of diverse antiviral CD8+ T cell populations after murine cytomegalovirus infection. Eur J Immunol 35: 1113-1123.
32. Harty JT, Badovinac VP, (2008) Shaping and reshaping CD8+ T-cell memory. Nat Rev Immunol 8: 107-119.
33. Pearce EL, Shen H, (2007) Generation of CD8 T Cell Memory Is Regulated by IL-12. The Journal of Immunology 179: 2074-2081.
34. Wiesel M, Crouse J, Bedenikovic G, Sutherland A, Joller N, et al. (2011) Type-I IFN drives the differentiation of short-lived effector CD8(+) T cells in vivo. Eur J Immunol.
35. Sarkar S, Teichgräber V, Kalia V, Polley A, Masopust D, et al. (2007) Strength of Stimulus and Clonal Competition Impact the Rate of Memory CD8 T Cell Differentiation. The Journal of Immunology 179: 6704-6714.
36. Badovinac VP, Haring JS, Harty JT, (2007) Initial T cell receptor transgenic cell precursor frequency dictates critical aspects of the CD8(+) T cell response to infection. Immunity 26: 827-841.
37. Nolz JC, Harty JT, (2012) Strategies and Implications for Prime-Boost Vaccination to Generate Memory CD8 T Cells. Adv Exp Med Biol 780: 69-83.
38. Bendelac A, Savage PB, Teyton L, (2006) The Biology of NKT Cells. Annu Rev Immunol 25: 297-336.
39. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, et al. (1999) Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol 163: 4647-4650.
40. Eberl G, MacDonald HR, (2000) Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells. Eur J Immunol 30: 985-992.
41. Hermans IF, Silk JD, Gileadi U, Salio M, Mathew B, et al. (2003) NKT cells enhance CD4+ and CD8+ T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol 171: 5140-5147.
42. Miyamoto K, Miyake S, Yamamura T, (2001) A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 413: 531-534.
43. Oki S, Chiba A, Yamamura T, Miyake S, (2004) The clinical implication and molecular mechanism of preferential IL-4 production by modified glycolipid-stimulated NKT cells. J Clin Invest 113: 1631-1640.
44. Yu KO, Im JS, Molano A, Dutronc Y, Illarionov PA, et al. (2005) Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides. Proc Natl Acad Sci U S A 102: 3383-3388.
45. Schmieg J, Yang G, Franck RW, Tsuji M, (2003) Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand alpha-Galactosylceramide. J Exp Med 198: 1631-1641.
46. Fujii S, Shimizu K, Kronenberg M, Steinman RM, (2002) Prolonged IFN-gamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs. Nat Immunol 3: 867-874.
47. Schneiders FL, Scheper RJ, von Blomberg BM, Woltman AM, Janssen HL, et al. (2011) Clinical experience with alpha-galactosylceramide (KRN7000) in patients with advanced cancer and chronic hepatitis B/C infection. Clin Immunol 140: 130-141.
48. Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L, (2012) Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12: 239-252.
49. Parekh VV, Wilson MT, Olivares-Villagomez D, Singh AK, Wu L, et al. (2005) Glycolipid antigen induces long-term natural killer T cell anergy in mice. J Clin Invest 115: 2572-2583.
50. Kim S, Lalani S, Parekh VV, Vincent TL, Wu L, et al. (2008) Impact of bacteria on the phenotype, functions, and therapeutic activities of invariant NKT cells in mice. J Clin Invest 118: 2301-2315.
51. Wesley JD, Tessmer MS, Chaukos D, Brossay L, (2008) NK cell-like behavior of Valpha14i NK T cells during MCMV infection. PLoS Pathog 4: e1000106.
52. Haring JS, Badovinac VP, Harty JT, (2006) Inflaming the CD8+ T cell response. Immunity 25: 19-29.
53. Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, et al. (2006) Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev 211: 81-92.
54. Dhodapkar MV, Richter J, (2011) Harnessing natural killer T (NKT) cells in human myeloma: progress and challenges. Clin Immunol 140: 160-166.
55. Robbins SH, Nguyen KB, Takahashi N, Mikayama T, Biron CA, et al. (2002) Cutting edge: inhibitory functions of the killer cell lectin-like receptor G1 molecule during the activation of mouse NK cells. J Immunol 168: 2585-2589.