Innate immune control of EBV-infected B cells by invariant natural killer T cells

Blood

Volumn 122, Issue 15, 2013, Pages 2600-2608

  Chung, Brian K ^a   Tsai, Kevin ^a   Allan, Lenka L ^a   Zheng, Dong Jun ^a   Nie, Johnny C ^a   Biggs, Catherine M ^a   Hasan, Mohammad R ^a   Kozak, Frederick K ^b   Van Den Elzen, Peter ^a   Priatel, John J ^a   Tan, Rusung ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BC CHILDREN S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; CD1D ANTIGEN; GAMMA INTERFERON; LYMPHOID ENHANCER FACTOR 1; CD1D PROTEIN, HUMAN; LEF1 PROTEIN, HUMAN;

ANTIGEN RECOGNITION; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; EPSTEIN BARR VIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; LYMPHOBLASTOID CELL LINE; NATURAL KILLER T CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; T CELL DEPLETION; UPREGULATION; CELL COMMUNICATION; CELL TRANSFORMATION; COMPLICATION; EPSTEIN BARR VIRUS; IMMUNOLOGY; LYMPHOPROLIFERATIVE DISEASE; METABOLISM; PALATINE TONSIL; VIROLOGY;

ANTIGENS, CD1D; B-LYMPHOCYTES; CELL COMMUNICATION; CELL TRANSFORMATION, NEOPLASTIC; EPSTEIN-BARR VIRUS INFECTIONS; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNITY, INNATE; LYMPHOID ENHANCER-BINDING FACTOR 1; LYMPHOPROLIFERATIVE DISORDERS; NATURAL KILLER T-CELLS; PALATINE TONSIL;

EID: 84891550264     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-01-480665     Document Type: Article

References (53)

1. Gaspar HB, Sharifi R, Gilmour KC, Thrasher AJ. X-linked lymphoproliferative disease: clinical, diagnostic and molecular perspective. Br J Haematol. 2002;119(3):585-595.
2. Cannons JL, Tangye SG, Schwartzberg PL. SLAM family receptors and SAP adaptors in immunity. Annu Rev Immunol. 2011;29: 665-705.
3. Chung B, Aoukaty A, Dutz J, Terhorst C, Tan R. Signaling lymphocytic activation moleculeassociated protein controls NKT cell functions. J Immunol. 2005;174(6):3153-3157.
4. Nichols KE, Hom J, Gong SY, et al. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat Med. 2005;11(3): 340-345.
5. Pasquier B, Yin L, Fondanèche MC, et al. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J Exp Med. 2005;201(5):695-701.
6. Banovic T, Yanilla M, Simmons R, et al. Disseminated varicella infection caused by varicella vaccine strain in a child with low invariant natural killer T cells and diminished CD1d expression. J Infect Dis. 2011;204(12):1893-1901.
7. Levy O, Orange JS, Hibberd P, et al. Disseminated varicella infection due to the vaccine strain of varicella-zoster virus, in a patient with a novel deficiency in natural killer T cells. J Infect Dis. 2003;188(7):948-953.
8. Huck K, Feyen O, Niehues T, et al. Girls homozygous for an IL-2-inducible T cell kinase mutation that leads to protein deficiency develop fatal EBV-associated lymphoproliferation. J Clin Invest. 2009;119(5):1350-1358.
9. Rigaud S, Fondanèche MC, Lambert N, et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature. 2006; 444(7115):110-114.
10. Sanchez DJ, Gumperz JE, Ganem D. Regulation of CD1d expression and function by a herpesvirus infection. J Clin Invest. 2005;115(5):1369-1378.
11. Yuan W, Dasgupta A, Cresswell P. Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling. Nat Immunol. 2006;7(8):835-842.
12. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol. 2004;22: 817-890.
13. Rossjohn J, Pellicci DG, Patel O, Gapin L, Godfrey DI. Recognition of CD1d-restricted antigens by natural killer T cells. Nat Rev Immunol. 2012;12(12):845-857.
14. Juno JA, Keynan Y, Fowke KR. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog. 2012;8(8):e1002838.
15. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol. 2007;25:297-336.
16. Barton E, Mandal P, Speck SH. Pathogenesis and host control of gammaherpesviruses: lessons from the mouse. Annu Rev Immunol. 2011;29: 351-397.
17. Hislop AD, Taylor GS, Sauce D, Rickinson AB. Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu Rev Immunol. 2007;25:587-617.
18. Szatmari I, Pap A, Rühl R, et al. PPARgamma controls CD1d expression by turning on retinoic acid synthesis in developing human dendritic cells. J Exp Med. 2006;203(10):2351-2362.
19. Chen Q, Mosovsky KL, Ross AC. Retinoic acid and α-galactosylceramide differentially regulate B cell activation in vitro and augment antibody production in vivo. Clin Vaccine Immunol. 2011; 18(6):1015-1020.
20. Allan LL, Stax AM, Zheng DJ, et al. CD1d and CD1c expression in human B cells is regulated by activation and retinoic acid receptor signaling. J Immunol. 2011;186(9):5261-5272.
21. Miller G, Lipman M. Release of infectious Epstein-Barr virus by transformed marmoset leukocytes. Proc Natl Acad Sci USA. 1973;70(1):190-194.
22. Speck P, Kline KA, Cheresh P, Longnecker R. Epstein-Barr virus lacking latent membrane protein 2 immortalizes B cells with efficiency indistinguishable from that of wild-type virus. J Gen Virol. 1999;80(Pt 8):2193-2203.
23. Allan LL, Hoefl K, Zheng DJ, et al. Apolipoprotein-mediated lipid antigen presentation in B cells provides a pathway for innate help by NKT cells. Blood. 2009;114(12):2411-2416.
24. Exley M, Garcia J, Balk SP, Porcelli S. Requirements for CD1d recognition by human invariant Valpha241 CD4-CD8-T cells. J Exp Med. 1997;186(1):109-120.
25. Storkus WJ, Howell DN, Salter RD, Dawson JR, Cresswell P. NK susceptibility varies inversely with target cell class I HLA antigen expression. J Immunol. 1987;138(6):1657-1659.
26. Kenna T, O'Brien M, Hogan AE, et al. CD1 expression and CD1-restricted T cell activity in normal and tumour-bearing human liver. Cancer Immunol Immunother. 2007;56(4):563-572.
27. Braaten D, Luban J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. J EMBO. 2001;20(6):1300-1309.
28. Brigl M, van den Elzen P, Chen X, et al. Conserved and heterogeneous lipid antigen specificities of CD1d-restricted NKT cell receptors. J Immunol. 2006;176(6):3625-3634.
29. Behrens J, von Kries JP, Kühl M, et al. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature. 1996;382(6592):638-642.
30. Chen QY, Zhang T, Pincus SH, et al. Human CD1D gene expression is regulated by LEF-1 through distal promoter regulatory elements. J Immunol. 2010;184(9):5047-5054.
31. Easwaran V, Pishvaian M, Salimuddin, Byers S. Cross-regulation of beta-catenin-LEF/TCF and retinoid signaling pathways. Curr Biol. 1999;9(23): 1415-1418.
32. Strowig T, Brilot F, Arrey F, et al. Tonsilar NK cells restrict B cell transformation by the Epstein-Barr virus via IFN-gamma. PLoS Pathog. 2008;4(2): e27.
33. Callan MF, Steven N, Krausa P, et al. Large clonal expansions of CD81 T cells in acute infectious mononucleosis. Nat Med. 1996;2(8):906-911.
34. Heslop HE, Slobod KS, Pule MA, et al. Long-term outcome of EBV-specific T-cell infusions to prevent or treat EBV-related lymphoproliferative disease in transplant recipients. Blood. 2010; 115(5):925-935.
35. Bottino C, Falco M, Parolini S, et al. NTB-A [correction of GNTB-A], a novel SH2D1Aassociated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative disease. J Exp Med. 2001; 194(3):235-246.
36. Dupré L, Andolfi G, Tangye SG, et al. SAP controls the cytolytic activity of CD81 T cells against EBV-infected cells. Blood. 2005;105(11): 4383-4389.
37. Parolini S, Bottino C, Falco M, et al. 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. 2000;192(3):337-346.
38. Hislop AD, Palendira U, Leese AM, et al. Impaired Epstein-Barr virus-specific CD81 T-cell function in X-linked lymphoproliferative disease is restricted to SLAM family-positive B-cell targets. Blood. 2010;116(17):3249-3257.
39. Ho LP, Urban BC, Jones L, Ogg GS, McMichael AJ. CD4(-)CD8alphaalpha subset of CD1drestricted NKT cells controls T cell expansion. J Immunol. 2004;172(12):7350-7358.
40. Matsuda JL, Naidenko OV, Gapin L, et al. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J Exp Med. 2000;192(5):741-754.
41. Vincent MS, Leslie DS, Gumperz JE, Xiong X, Grant EP, Brenner MB. CD1-dependent dendritic cell instruction. Nat Immunol. 2002;3(12): 1163-1168.
42. Carnaud C, Lee D, Donnars O, et al. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells. J Immunol. 1999;163(9):4647-4650.
43. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med. 2003;198(2):267-279.
44. Long HM, Taylor GS, Rickinson AB. Immune defence against EBV and EBV-associated disease. Curr Opin Immunol. 2011;23(2):258-264.
45. Wolf H, Werner J, zur Hausen H. EBV DNA in nonlymphoid cells of nasopharyngeal carcinomas and in a malignant lymphoma obtained after inoculation of EBV into cottontop marmosets. Cold Spring Harb Symp Quant Biol. 1975; 39(Pt 2):791-796.
46. Lockridge JL, Chen X, Zhou Y, et al. Analysis of the CD1 antigen presenting system in humanized SCID mice. PLoS ONE. 2011;6(6):e21701.
47. Bosma A, Abdel-Gadir A, Isenberg DA, Jury EC, Mauri C. Lipid-antigen presentation by CD1d(1) B cells is essential for the maintenance of invariant natural killer T cells. Immunity. 2012; 36(3):477-490.
48. Ohno R, Asou N, Ohnishi K. Treatment of acute promyelocytic leukemia: strategy toward further increase of cure rate. Leukemia. 2003;17(8): 1454-1463.
49. Dezube BJ. New therapies for the treatment of AIDS-related Kaposi sarcoma. Curr Opin Oncol. 2000;12(5):445-449.
50. Reya T, O'Riordan M, Okamura R, et al. Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity. 2000;13(1):15-24.
51. Pang MF, Lin KW, Peh SC. The signaling pathways of Epstein-Barr virus-encoded latent membrane protein 2A (LMP2A) in latency and cancer. Cell Mol Biol Lett. 2009;14(2):222-247.
52. Morrison JA, Klingelhutz AJ, Raab-Traub N. Epstein-Barr virus latent membrane protein 2A activates beta-catenin signaling in epithelial cells. J Virol. 2003;77(22):12276-12284.
53. Morrison JA, Gulley ML, Pathmanathan R, Raab-Traub N. Differential signaling pathways are activated in the Epstein-Barr virus-associated malignancies nasopharyngeal carcinoma and Hodgkin lymphoma. Cancer Res. 2004;64(15): 5251-5260.