Tonsilar NK cells restrict B cell transformation by the epstein-barr virus via IFN-γ

PLoS Pathogens

Volumn 4, Issue 2, 2008, Pages

  Strowig, Till ^a   Brilot, Fabienne ^a   Arrey, Frida ^a   Bougras, Gwenola ^a   Thomas, Dolca ^b   Muller, William A ^b   Münz, Christian ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 18; FC RECEPTOR; T LYMPHOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE TRANSFORMATION; LYMPHOID TISSUE; NATURAL KILLER CELL; TONSIL CELL; VIRUS INFECTION; VIRUS PATHOGENESIS; CYTOLOGY; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; SPLEEN; TONSIL; VIROLOGY;

HUMAN HERPESVIRUS 4;

ANTIGENS, CD56; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; B-LYMPHOCYTES; DENDRITIC CELLS; HERPESVIRUS 4, HUMAN; HUMANS; INTERFERON TYPE II; KILLER CELLS, NATURAL; LYMPH NODES; LYMPHOCYTE ACTIVATION; RECEPTORS, IGG; SPLEEN; TONSIL;

EID: 40349084108     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0040027     Document Type: Article

References (66)

1. Thorley-Lawson DA (2001) Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol 1: 75-82.
2. Young LS, Rickinson AB (2004) Epstein-Barr virus: 40 years on. Nat Rev Cancer 4: 757-768.
3. Küppers R (2003) B cells under influence: transformation of B cells by Epstein-Barr virus. Nat Rev Immunol 3: 801-812.
4. Hislop AD, Taylor GS, Sauce D, Rickinson AB (2007) Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu Rev Immunol 25: 587-617.
5. Benoit L, Wang X, Pabst HF, Dutz J, Tan R (2000) Defective NK cell activation in X-linked lymphoproliferative disease. J Immunol 165: 3549-3553.
6. Morra M, Howie D, Grande MS, Sayos J, Wang N, et al. (2001) X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu Rev Immunol 19: 657-682.
7. Parolini S, Bottino C, Falco M, Augugliaro R, Giliani S, et al. (2000) X-linked lymphoproliferative disease. 2B4 molecules displaying inhibitory rather than activating function are responsible for the inability of natural killer cells to kill Epstein-Barr virus-infected cells. J Exp Med 192: 337-346.
8. Masucci MG, Bejarano MT, Masucci G, Klein E (1983) Large granular lymphocytes inhibit the in vitro growth of autologous Epstein-Barr virus-infected B cells. Cell Immunol 76: 311-321.
9. Wilson AD, Morgan AJ (2002) Primary immune responses by cord blood CD4+ T cells and NK cells inhibit Epstein-Barr virus B-cell transformation in vitro. J Virol 76: 5071-5081.
10. Kaplan J, Shope TC (1985) Natural killer cells inhibit outgrowth of autologous Epstein-Barr virus-infected B lymphocytes. Nat Immun Cell Growth Regul 4: 40-47.
11. Baiocchi RA, Ward JS, Carrodeguas L, Eisenbeis CF, Peng R, et al. (2001) GM-CSF and IL-2 induce specific cellular immunity and provide protection against Epstein-Barr virus lymphoproliferative disorder. J Clin Invest 108: 887-894.
12. Pappworth IY, Wang EC, Rowe M (2007) The switch from latent to productive infection in Epstein-Barr virus-infected B cells is associated with sensitization to NK cell killing. J Virol 81: 474-482.
13. Eidenschenk C, Dunne J, Jouanguy E, Fourlinnie C, Gineau L, et al. (2006) A novel primary immunodeficiency with specific natural-killer cell deficiency maps to the centromeric region of chromosome 8. Am J Hum Genet 78: 721-727.
14. Trinchieri G (1989) Biology of natural killer cells. Adv Immunol 47: 187-376.
15. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP (1999) Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 17: 189-220.
16. Bukowski JF, Woda BA, Habu S, Okumura K, Welsh RM (1983) Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J Immunol 131: 1531-1538.
17. Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, et al. (2001) Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med 194: 29-44.
18. Andoniou CE, van Dommelen SL, Voigt V, Andrews DM, Brizard G, et al. (2005) Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat Immunol 6: 1011-1019.
19. Andrews DM, Scalzo AA, Yokoyama WM, Smyth MJ, Degli-Esposti MA (2003) Functional interactions between dendritic cells and NK cells during viral infection. Nat Immunol 4: 175-181.
20. 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.
21. Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, et al. (2002) Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 195: 517-528.
22. Lucas M, Schachterle W, Oberle K, Aichele P, Diefenbach A (2007) Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
23. Degli-Esposti MA, Smyth MJ (2005) Close encounters of different kinds: dendritic cells and NK cells take centre stage. Nat Rev Immunol 5: 112-124.
24. bright subset. Blood 97: 3146-3151.
25. Cooper MA, Fehniger TA, Caligiuri MA (2001) The biology of human natural killer-cell subsets. Trends Immunol 22: 633-640.
26. bright Natural Killer Cells are Present in Human Lymph Nodes and are Activated by T cell Derived IL-2: a Potential New Link between Adaptive and Innate Immunity. Blood 12: 12.
27. Ferlazzo G, Münz C (2004) Natural killer cell compartments and their activation by dendritic cells. J Immunol 172: 1333-1339.
28. Ferlazzo G, Thomas D, Lin SL, Goodman K, Morandi B, et al. (2004) The abundant NK cells in human lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol 172: 1455-1462.
29. - natural killer cells is selectively responsible for both cell proliferation and interferon-gamma production upon interaction with dendritic cells. Eur J Immunol 34: 1715-1722.
30. Ferlazzo G, Thomas D, Pack M, Paludan C, Schmid D, et al. (2004) Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc Natl Acad Sci U S A 101: 16606-16611.
31. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, et al. (2004) Alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res 64: 5934-5937.
32. Münz C, Dao T, Ferlazzo G, De Cos MA, Goodman K, et al. (2005) Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood 105: 266-273.
33. Orange JS, Wang B, Terhorst C, Biron CA (1995) Requirement for natural killer cell-produced interferon gamma in defense against murine cytomegalovirus infection and enhancement of this defense pathway by interleukin 12 administration. J Exp Med 182: 1045-1056.
34. Kassim SH, Rajasagi NK, Zhao X, Chervenak R, Jennings SR (2006) In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses. J Virol 80: 3985-3993.
35. + NK helper cells. J Exp Med 202: 941-953.
36. Duff GW, Atkins E (1982) The inhibitory effect of polymyxin B on endotoxin-induced endogenous pyrogen production. J Immunol Methods 52: 333-340.
37. Moretta A (2002) Natural killer cells and dendritic cells: rendezvous in abused tissues. Nat Rev Immunol 2: 957-964.
38. Babcock JG, Hochberg D, Thorley-Lawson AD (2000) The expression pattern of Epstein-Barr virus latent genes in vivo is dependent upon the differentiation stage of the infected B cell. Immunity 13: 497-506.
39. McHeyzer-Williams LJ, McHeyzer-Williams MG (2005) Antigen-specific memory B cell development. Annu Rev Immunol 23: 487-513.
40. Bajenoff M, Breart B, Huang AY, Qi H, Cazareth J, et al. (2006) Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J Exp Med 203: 619-631.
41. Garrod KR, Wei SH, Parker I, Cahalan MD (2007) Natural killer cells actively patrol peripheral lymph nodes forming stable conjugates to eliminate MHC-mismatched targets. Proc Natl Acad Sci U S A 104: 12081-12086.
42. Banchereau J, Steinman RM (1998) Dendritic cells and the control of immunity. Nature 392: 245-252.
43. Iwasaki A, Medzhitov R (2004) Toll-like receptor control of the adaptive immune responses. Nat Immunol 5: 987-995.
44. Tabeta K, Georgel P, Janssen E, Du X, Hoebe K, et al. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc Natl Acad Sci U S A 101: 3516-3521.
45. Lim WH, Kireta S, Russ GR, Coates PT (2006) Human plasmacytoid dendritic cells regulate immune responses to Epstein-Barr virus (EBV) infection and delay EBV-related mortality in humanized NOD-SCID mice. Blood 109: 1043-1050.
46. Lagunoff M, Roizman B (1994) Expression of a herpes simplex virus 1 open reading frame antisense to the gamma(1)34.5 gene and transcribed by an RNA 3′ coterminal with the unspliced latency-associated transcript. J Virol 68: 6021-6028.
47. Sample J, Liebowitz D, Kieff E (1989) Two related Epstein-Barr virus membrane proteins are encoded by separate genes. J Virol 63: 933-937.
48. Jacquemont B, Roizman B (1975) RNA synthesis in cells infected with herpes simplex virus. X. Properties of viral symmetric transcripts and of double-stranded RNA prepared from them. J Virol 15: 707-713.
49. Schulz O, Diebold SS, Chen M, Naslund TI, Nolte MA, et al. (2005) Toll-like receptor 3 promotes cross-priming of virus-infected cells. Nature 433: 887-892.
50. Gitlin L, Barchet W, Gilfillan S, Cella M, Beutler B, et al. (2006) Essential role of mda-5 in type I IFN responses to polyriboinosinic: polyribocytidylic acid and encephalomyocarditis picornavirus. Proc Natl Acad Sci U S A 103: 8459-8464.
51. Bickham K, Goodman K, Paludan C, Nikiforow S, Tsang ML, et al. (2003) Dendritic cells initiate immune control of Epstein-Barr virus transformation of B lymphocytes in vitro. J Exp Med 198: 1653-1663.
52. Borg C, Abdelali J, Laderach D, Maruyama K, Wakasugi H, et al. (2004) NK Cell Activation by Dendritic Cells (DC) Require The Formation of a Synapse leading to IL-12 Polarization in DC. Blood 104: 3267-3275.
53. Ferlazzo G, Tsang ML, Moretta L, Melioli G, Steinman RM, et al. (2002) Human dendritic cells activate resting NK cells and are recognized via the NKp30 receptor by activated NK cells. J Exp Med 195: 343-351.
54. Moretta A, Comoli P, Montagna D, Gasparoni A, Percivalle E, et al. (1997) High frequency of Epstein-Barr virus (EBV) lymphoblastoid cell linereactive lymphocytes in cord blood: evaluation of cytolytic activity and IL-2 production. Clin Exp Immunol 107: 312-320.
55. Lotz M, Tsoukas CD, Fong S, Carson DA, Vaughan JH (1985) Regulation of Epstein-Barr virus infection by recombinant interferons. Selected sensitivity to interferon-gamma. Eur J Immunol 15: 520-525.
56. + T cells that poorly kill EBV-infected cells. Viral Immunol 15: 213-225.
57. Lee SP, Brooks JM, Al-Jarrah H, Thomas WA, Haigh TA, et al. (2004) CD8 T cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J Exp Med 199: 1409-1420.
58. Laouar Y, Sutterwala FS, Gorelik L, Flavell RA (2005) Transforming growth factor-beta controls T helper type 1 cell development through regulation of natural killer cell interferon-gamma. Nat Immunol 6: 600-607.
59. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, et al. (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5: 1260-1265.
60. Morandi B, Bougras G, Muller WA, Ferlazzo G, Münz C (2006) NK cells of human secondary lymphoid tissues enhance T cell polarization via IFNgamma secretion. Eur J Immunol 36: 2394-2400.
61. + T cells in healthy carriers of Epstein-Barr virus are primarily Th1 in function. J Clin Invest 107: 121-130.
62. Kulwichit W, Edwards RH, Davenport EM, Baskar JF, Godfrey V, et al. (1998) Expression of the Epstein-Barr virus latent membrane protein 1 induces B cell lymphoma in transgenic mice. Proc Natl Acad Sci U S A 95: 11963-11968.
63. Dawson CW, Rickinson AB, Young LS (1990) Epstein-Barr virus latent membrane protein inhibits human epithelial cell differentiation. Nature 344: 777-780.
64. Fahraeus R, Rymo L, Rhim JS, Klein G (1990) Morphological transformation of human keratinocytes expressing the LMP gene of Epstein-Barr virus. Nature 345: 447-449.
65. Presti RM, Popkin DL, Connick M, Paetzold S, Virgin HWt (2001) Novel cell type-specific antiviral mechanism of interferon gamma action in macrophages. J Exp Med 193: 483-496.
66. Borza CM, Hutt-Fletcher LM (2002) Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat Med 8: 594-599.