Molecular pathogenesis of EBV susceptibility in XLP as revealed by analysis of female carriers with heterozygous expression of SAP

PLoS Biology

Volumn 9, Issue 11, 2011, Pages

  Palendira, Umaimainthan ^a,b   Low, Carol ^a   Chan, Anna ^a   Hislop, Andrew D ^c   Ho, Edwin ^a   Phan, Tri Giang ^a,b   Deenick, Elissa ^a,b   Cook, Matthew C ^d,e,f   Riminton, D Sean ^g   Choo, Sharon ^h   Loh, Richard ⁱ   Alvaro, Frank ^j   Booth, Claire ^k   Gaspar, H Bobby ^k   Moretta, Alessandro ^l   Khanna, Rajiv ^m   Rickinson, Alan B ^c   Tangye, Stuart G ^a,b  

^a GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d The Australian National University   (Australia)

^e Biology and Environment   (Australia)

^f CANBERRA HOSPITAL   (Australia)

^g Department of Microbiology and Infectious Diseases   (Australia)

^h ROYAL CHILDREN'S HOSPITAL   (Australia)

ⁱ PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^j JOHN HUNTER HOSPITAL   (Australia)

^k UNIVERSITY COLLEGE LONDON   (United Kingdom)

^l UNIVERSITY OF GENOA   (Italy)

^m QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN NTB 2B4; PROTEIN NTB A; RECEPTOR; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; CD150 ANTIGEN; CD244 PROTEIN, HUMAN; CD48 ANTIGEN; CELL SURFACE RECEPTOR; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIGEN; SH2D1A PROTEIN, HUMAN; SIGNAL PEPTIDE;

ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; BONE MARROW; CD8+ T LYMPHOCYTE; CELL CLONE; CELL SPECIFICITY; CONTROLLED STUDY; CYTOTOXICITY; EPSTEIN BARR VIRUS INFECTION; FIBROBLAST; GENE EXPRESSION; HETEROZYGOTE; HUMAN; HUMAN CELL; INFECTION SENSITIVITY; LYMPHOPROLIFERATIVE DISEASE; MEMORY T LYMPHOCYTE; MOLECULAR PATHOLOGY; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; VIRAL TROPISM; X CHROMOSOME INACTIVATION; X CHROMOSOME LINKED DISORDER; X LINKED LYMPHOPROLIFERATIVE DISEASE; DENDRITIC CELL; EPSTEIN BARR VIRUS; FEMALE; GENE REARRANGEMENT; GENETICS; GENOTYPE; IMMUNOLOGY; INFLUENZA; MONONUCLEAR CELL; ORTHOMYXOVIRUS; PATHOGENICITY; PATHOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

ANTIGENS, CD; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; EPSTEIN-BARR VIRUS INFECTIONS; FEMALE; GENOTYPE; HERPESVIRUS 4, HUMAN; HUMANS; IMMUNOGLOBULIN CLASS SWITCHING; INFLUENZA, HUMAN; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEUKOCYTES, MONONUCLEAR; LYMPHOPROLIFERATIVE DISORDERS; ORTHOMYXOVIRIDAE; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; X CHROMOSOME INACTIVATION;

EID: 82455175808     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001187     Document Type: Article

References (75)

1. Coffey A. J, Brooksbank R. A, Brandau O, Oohashi T, Howell G. R, et al. (1998) Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat Genet 20: 129-135.
2. Sayos J, Wu C, Morra M, Wang N, Zhang X, et al. (1998) The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395: 462-469.
3. Nichols K. E, Harkin D. P, Levitz S, Krainer M, Kolquist K. A, et al. (1998) Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc Natl Acad Sci U S A 95: 13765-13770.
4. Schwartzberg P. L, Mueller K. L, Qi H, Cannons J. L, (2009) SLAM receptors and SAP influence lymphocyte interactions, development and function. Nat Rev Immunol 9: 39-46.
5. Veillette A, (2006) Immune regulation by SLAM family receptors and SAP-related adaptors. Nat Rev Immunol 6: 56-66.
6. Veillette A, Dong Z, Perez-Quintero L. A, Zhong M. C, Cruz-Munoz M. E, (2009) Importance and mechanism of 'switch' function of SAP family adapters. Immunol Rev 232: 229-239.
7. Ma C. S, Nichols K. E, Tangye S. G, (2007) Regulation of cellular and humoral immune responses by the SLAM and SAP families of molecules. Annu Rev Immunol 25: 337-379.
8. Filipovich A. H, Zhang K, Snow A. L, Marsh R. A, (2010) X-linked lymphoproliferative syndromes: brothers or distant cousins? Blood 116: 3398-3408.
9. Nichols K. E, Ma C. S, Cannons J. L, Schwartzberg P. L, Tangye S. G, (2005) Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol Rev 203: 180-199.
10. Fischer A, (2007) Human primary immunodeficiency diseases. Immunity 27: 835-845.
11. Nichols K. E, Hom J, Gong S. Y, Ganguly A, Ma C. S, et al. (2005) Regulation of NKT cell development by SAP, the protein defective in XLP. Nat Med 11: 340-345.
12. Pasquier B, Yin L, Fondaneche M. C, Relouzat F, Bloch-Queyrat C, et al. (2005) Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J Exp Med 201: 695-701.
13. Cannons J. L, Yu L. J, Jankovic D, Crotty S, Horai R, et al. (2006) SAP regulates T cell-mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J Exp Med 203: 1551-1565.
14. Crotty S, Kersh E. N, Cannons J, Schwartzberg P. L, Ahmed R, (2003) SAP is required for generating long-term humoral immunity. Nature 421: 282-287.
15. Ma C. S, Pittaluga S, Avery D. T, Hare N. J, Maric I, et al. (2006) Selective generation of functional somatically mutated IgM+CD27+, but not Ig isotype-switched, memory B cells in X-linked lymphoproliferative disease. J Clin Invest 116: 322-333.
16. Ma C. S, Hare N. J, Nichols K. E, Dupre L, Andolfi G, et al. (2005) Impaired humoral immunity in X-linked lymphoproliferative disease is associated with defective IL-10 production by CD4+ T cells. J Clin Invest 115: 1049-1059.
17. Qi H, Cannons J. L, Klauschen F, Schwartzberg P. L, Germain R. N, (2008) SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455: 764-769.
18. Deenick E. K, Chan A, Ma C. S, Gatto D, Schwartzberg P. L, et al. (2010) Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity 33: 241-253.
19. Dupre L, Andolfi G, Tangye S. G, Clementi R, Locatelli F, et al. (2005) SAP controls the cytolytic activity of CD8+ T cells against EBV-infected cells. Blood 105: 4383-4389.
20. Sharifi R, Sinclair J. C, Gilmour K. C, Arkwright P. D, Kinnon C, et al. (2004) SAP mediates specific cytotoxic T-cell functions in X-linked lymphoproliferative disease. Blood 103: 3821-3827.
21. Argov S, Johnson D. R, Collins M, Koren H. S, Lipscomb H, et al. (1986) Defective natural killing activity but retention of lymphocyte-mediated antibody-dependent cellular cytotoxicity in patients with the X-linked lymphoproliferative syndrome. Cell Immunol 100: 1-9.
22. Bottino C, Falco M, Parolini S, Marcenaro E, Augugliaro R, et al. (2001) NTB-A, a novel SH2D1A-associated 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 194: 235-246.
23. Harada S, Sakamoto K, Seeley J. K, Lindsten T, Bechtold T, et al. (1982) Immune deficiency in the X-linked lymphoproliferative syndrome. I. Epstein-Barr virus-specific defects. J Immunol 129: 2532-2535.
24. 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.
25. Sullivan J. L, Byron K. S, Brewster F. E, Purtilo D. T, (1980) Deficient natural killer cell activity in X-linked lymphoproliferative syndrome. Science 210: 543-545.
26. Tangye S. G, Phillips J. H, Lanier L. L, Nichols K. E, (2000) Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J Immunol 165: 2932-2936.
27. Nakajima H, Cella M, Bouchon A, Grierson H. L, Lewis J, et al. (2000) Patients with X-linked lymphoproliferative disease have a defect in 2B4 receptor-mediated NK cell cytotoxicity. Eur J Immunol 30: 3309-3318.
28. Orange J. S, (2002) Human natural killer cell deficiencies and susceptibility to infection. Microbes Infect 4: 1545-1558.
29. Fulcher D. A, Avery D. T, Fewings N. L, Berglund L. J, Wong S, et al. (2009) Invariant natural killer (iNK) T cell deficiency in patients with common variable immunodeficiency. Clin Exp Immunol 157: 365-369.
30. Locci M, Draghici E, Marangoni F, Bosticardo M, Catucci M, et al. (2009) The Wiskott-Aldrich syndrome protein is required for iNKT cell maturation and function. J Exp Med 206: 735-742.
31. Matangkasombut P, Pichavant M, Saez D. E, Giliani S, Mazzolari E, et al. (2008) Lack of iNKT cells in patients with combined immune deficiency due to hypomorphic RAG mutations. Blood 111: 271-274.
32. Hislop A. D, Palendira U, Leese A. M, Arkwright P. D, Rohrlich P. S, et al. (2010) Impaired Epstein-Barr virus-specific CD8+ T-cell function in X-linked lymphoproliferative disease is restricted to SLAM family-positive B-cell targets. Blood 116: 3249-3257.
33. Lee K. M, Bhawan S, Majima T, Wei H, Nishimura M. I, et al. (2003) Cutting edge: the NK cell receptor 2B4 augments antigen-specific T cell cytotoxicity through CD48 ligation on neighboring T cells. J Immunol 170: 4881-4885.
34. Hermans I. F, Silk J. D, 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.
35. Moreno M, Molling J. W, von Mensdorff-Pouilly S, Verheijen R. H, Hooijberg E, et al. (2008) IFN-gamma-producing human invariant NKT cells promote tumor-associated antigen-specific cytotoxic T cell responses. J Immunol 181: 2446-2454.
36. Stober D, Jomantaite I, Schirmbeck R, Reimann J, (2003) NKT cells provide help for dendritic cell-dependent priming of MHC class I-restricted CD8+ T cells in vivo. J Immunol 170: 2540-2548.
37. Rickinson A, Kieff E, (2007) Epstein-Barr virus. Fields Virology. 5th ed Philadelphia Lippincott, Williams & Wilkins.
38. Hamilton J. K, Paquin L. A, Sullivan J. L, Maurer H. S, Cruzi F. G, et al. (1980) X-linked lymphoproliferative syndrome registry report. J Pediatr 96: 669-673.
39. Sakamoto K, Seeley J. K, Lindsten T, Sexton J, Yetz J, et al. (1982) Abnormal anti-Epstein Barr virus antibodies in carriers of the X-linked lymphoproliferative syndrome and in females at risk. J Immunol 128: 904-907.
40. Chen G, Tai A. K, Lin M, Chang F, Terhorst C, et al. (2005) Signaling lymphocyte activation molecule-associated protein is a negative regulator of the CD8 T cell response in mice. J Immunol 175: 2212-2218.
41. Chen G, Tai A. K, Lin M, Chang F, Terhorst C, et al. (2007) Increased proliferation of CD8+ T cells in SAP-deficient mice is associated with impaired activation-induced cell death. Eur J Immunol 37: 663-674.
42. Snow A. L, Marsh R. A, Krummey S. M, Roehrs P, Young L. R, et al. (2009) Restimulation-induced apoptosis of T cells is impaired in patients with X-linked lymphoproliferative disease caused by SAP deficiency. J Clin Invest 119: 2976-2989.
43. Nagy N, Matskova L, Kis L. L, Hellman U, Klein G, et al. (2009) The proapoptotic function of SAP provides a clue to the clinical picture of X-linked lymphoproliferative disease. Proc Natl Acad Sci U S A 106: 11966-11971.
44. Betts M. R, Brenchley J. M, Price D. A, De Rosa S. C, Douek D. C, et al. (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281: 65-78.
45. Aktas E, Kucuksezer U. C, Bilgic S, Erten G, Deniz G, (2009) Relationship between CD107a expression and cytotoxic activity. Cell Immunol 254: 149-154.
46. Hare N. J, Ma C. S, Alvaro F, Nichols K. E, Tangye S. G, (2006) Missense mutations in SH2D1A identified in patients with X-linked lymphoproliferative disease differentially affect the expression and function of SAP. Int Immunol 18: 1055-1065.
47. Roda-Navarro P, Mittelbrunn M, Ortega M, Howie D, Terhorst C, et al. (2004) Dynamic redistribution of the activating 2B4/SAP complex at the cytotoxic NK cell immune synapse. J Immunol 173: 3640-3646.
48. Bouchon A, Cella M, Grierson H. L, Cohen J. I, Colonna M, (2001) Activation of NK cell-mediated cytotoxicity by a SAP-independent receptor of the CD2 family. J Immunol 167: 5517-5521.
49. Henning G, Kraft M. S, Derfuss T, Pirzer R, de Saint-Basile G, et al. (2001) Signaling lymphocytic activation molecule (SLAM) regulates T cellular cytotoxicity. Eur J Immunol 31: 2741-2750.
50. Thorley-Lawson D. A, Schooley R. T, Bhan A. K, Nadler L. M, (1982) Epstein-Barr virus superinduces a new human B cell differentiation antigen (B-LAST 1) expressed on transformed lymphoblasts. Cell 30: 415-425.
51. Cruz-Munoz M. E, Dong Z, Shi X, Zhang S, Veillette A, (2009) Influence of CRACC, a SLAM family receptor coupled to the adaptor EAT-2, on natural killer cell function. Nat Immunol 10: 297-305.
52. Tangye S. G, Cherwinski H, Lanier L. L, Phillips J. H, (2000) 2B4-mediated activation of human natural killer cells. Mol Immunol 37: 493-501.
53. Valiante N. M, Trinchieri G, (1993) Identification of a novel signal transduction surface molecule on human cytotoxic lymphocytes. J Exp Med 178: 1397-1406.
54. Yokoyama S, Staunton D, Fisher R, Amiot M, Fortin J. J, et al. (1991) Expression of the Blast-1 activation/adhesion molecule and its identification as CD48. J Immunol 146: 2192-2200.
55. Cunningham-Rundles C, Ponda P. P, (2005) Molecular defects in T- and B-cell primary immunodeficiency diseases. Nat Rev Immunol 5: 880-892.
56. Fearon E. R, Winkelstein J. A, Civin C. I, Pardoll D. M, Vogelstein B, (1987) Carrier detection in X-linked agammaglobulinemia by analysis of X-chromosome inactivation. N Engl J Med 316: 427-431.
57. Prchal J. T, Carroll A. J, Prchal J. F, Crist W. M, Skalka H. W, et al. (1980) Wiskott-Aldrich syndrome: cellular impairments and their implication for carrier detection. Blood 56: 1048-1054.
58. Puck J. M, Nussbaum R. L, Conley M. E, (1987) Carrier detection in X-linked severe combined immunodeficiency based on patterns of X chromosome inactivation. J Clin Invest 79: 1395-1400.
59. Plunkett F. J, Franzese O, Belaramani L. L, Fletcher J. M, Gilmour K. C, et al. (2005) The impact of telomere erosion on memory CD8+ T cells in patients with X-linked lymphoproliferative syndrome. Mech Ageing Dev 126: 855-865.
60. Taylor-Wiedeman J, Sissons J. G, Borysiewicz L. K, Sinclair J. H, (1991) Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J Gen Virol 72 (Pt 9): 2059-2064.
61. Randall T. D, (2010) Pulmonary dendritic cells: thinking globally, acting locally. J Exp Med 207: 451-454.
62. Hislop A. D, Taylor G. S, Sauce D, Rickinson A. B, (2007) Cellular responses to viral infection in humans: lessons from Epstein-Barr virus. Annu Rev Immunol 25: 587-617.
63. Hislop A. D, Taylor G. S, Sauce D, Rickinson B. A, (2007) Cellular responses to viral infection in humans: lessons from Epstein-Barr Virus. Annu Rev Immunol 25: 587-617.
64. Rickinson A. B, Kieff E, (2006) Epstein-Barr virus. In: Knipe D. M, Howley P. M, Griffin D. E, editors. Fields virology. 5th ed Philadelphia Lippincott Williams & Wilkins pp. 2655-2700.
65. Dong Z, Cruz-Munoz M. E, Zhong M. C, Chen R, Latour S, et al. (2009) Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat Immunol 10: 973-980.
66. Eissmann P, Beauchamp L, Wooters J, Tilton J. C, Long E. O, et al. (2005) Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood 105: 4722-4729.
67. Sivori S, Falco M, Marcenaro E, Parolini S, Biassoni R, et al. (2002) Early expression of triggering receptors and regulatory role of 2B4 in human natural killer cell precursors undergoing in vitro differentiation. Proc Natl Acad Sci U S A 99: 4526-4531.
68. Vacca P, Pietra G, Falco M, Romeo E, Bottino C, et al. (2006) Analysis of natural killer cells isolated from human decidua: evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK-cell function. Blood 108: 4078-4085.
69. Roncagalli R, Taylor J. E, Zhang S, Shi X, Chen R, et al. (2005) Negative regulation of natural killer cell function by EAT-2, a SAP-related adaptor. Nat Immunol 6: 1002-1010.
70. Eissmann P, Watzl C, (2006) Molecular analysis of NTB-A signaling: a role for EAT-2 in NTB-A-mediated activation of human NK cells. J Immunol 177: 3170-3177.
71. Cannons J. L, Qi H, Lu K. T, Dutta M, Gomez-Rodriguez J, et al. (2010) Optimal germinal center responses require a multistage T cell:B cell adhesion process involving integrins, SLAM-associated protein, and CD84. Immunity 32: 253-265.
72. Tassi I, Colonna M, (2005) The cytotoxicity receptor CRACC (CS-1) recruits EAT-2 and activates the PI3K and phospholipase Cgamma signaling pathways in human NK cells. J Immunol 175: 7996-8002.
73. Rigaud S, Fondaneche M. C, Lambert N, Pasquier B, Mateo V, et al. (2006) XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature 444: 110-114.
74. Hislop A. D, Annels N. E, Gudgeon N. H, Leese A. M, Rickinson A. B, (2002) Epitope-specific evolution of human CD8(+) T cell responses from primary to persistent phases of Epstein-Barr virus infection. J Exp Med 195: 893-905.
75. Steven N. M, Leese A. M, Annels N. E, Lee S. P, Rickinson A. B, (1996) Epitope focusing in the primary cytotoxic T cell response to Epstein-Barr virus and its relationship to T cell memory. J Exp Med 184: 1801-1813.