Hypogammaglobulinemia and exacerbated CD8 T-cell-mediated immunopathology in SAP-deficient mice with chronic LCMV infection mimics human XLP disease

Blood

Volumn 108, Issue 9, 2006, Pages 3085-3093

  Crotty, Shane ^a   McCausland, Megan M ^b   Aubert, Rachael D ^b   Wherry, E John ^b   Ahmed, Rafi ^b  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; GERMINAL CENTER; HYPOGAMMAGLOBULINEMIA; IMMUNOPATHOLOGY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; LYMPHOPROLIFERATIVE DISEASE; MALE; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; WEIGHT REDUCTION; X LINKED LYMPHOPROLIFERATIVE DISEASE;

EID: 33750385770     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-04-018929     Document Type: Article

References (85)

1. Coffey AJ, Brooksbank RA, Brandau O, et al. Host response to EBV infection in X-linked lymphoproliferative disease results from mutations in an SH2-domain encoding gene. Nat Genet. 1998;20:129-135.
2. Nichols KE, Harkin DP, Levitz S, et al. Inactivating mutations in an SH2 domain-encoding gene in X-linked lymphoproliferative syndrome. Proc Natl Acad Sci U S A. 1998;95:13765-13770.
3. Sayos J, Wu C, Morra M, et al. The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature. 1998;395:462-469.
4. Nichols KE, Hom J, Gong SY, et al. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat Med. 2005;11:340-345.
5. Feldhahn N, Schwering I, Lee S, et al. Silencing of B cell receptor signals in human naive B cells. J Exp Med. 2002;196:1291-1305.
6. Shlapatska LM, Mikhalap SV, Berdova AG, et al. CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J Immunol. 2001;166:5480-5487.
7. Nichols KE, Ma CS, Cannons JL, Schwartzberg PL, Tangye SG. Molecular and cellular pathogenesis of X-linked lymphoproliferative disease. Immunol Rev. 2005;203:180-199.
8. Engel P, Eck MJ, Terhorst C. The SAP and SLAM families in immune responses and X-linked lymphoproliferative disease. Nat Rev Immunol. 2003;3:813-821.
9. Latour S, Veillette A. Molecular and immunological basis of X-linked lymphoproliferative disease. Immunol Rev. 2003;192:212-224.
10. Czar MJ, Kersh EN, Mijares LA, et al. Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lymphoproliferative disease gene SH2D1A/DSHP/SAP. Proc Natl Acad Sci U S A. 2001;98:7449-7454.
11. Wu C, Nguyen KB, Pien GC, et al. SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat Immunol. 2001;2:410-414.
12. Crotty S, Kersh EN, Cannons J, Schwartzberg PL, Ahmed R. SAP is required for generating long-term humoral immunity. Nature. 2003;421:282-287.
13. Yin L, Al-Alem U, Liang J, et al. Mice deficient in the X-linked lymphoproliferative disease gene sap exhibit increased susceptibility to murine gammaherpesvirus-68 and hypo-gammaglobulinemia. J Med Virol. 2003;71:446-455.
14. Latour S, Gish G, Helgason CD, Humphries RK, Pawson T, Veillette A. Regulation of SLAM-mediated signal transduction by SAP, the X-linked lymphoproliferative gene product. Nat Immunol. 2001;2:681-690.
15. Howie D, Okamoto S, Rietdijk S, et al. The role of SAP in murine CD150 (SLAM)-mediated T-cell proliferation and interferon gamma production. Blood. 2002;100:2899-2907.
16. Cannons JL, Yu LJ, Hill B, et al. SAP regulates T(H)2 differentiation and PKC-theta-mediated activation of NF-kappaB1. Immunity. 2004;21:693-706.
17. Davidson D, Shi X, Zhang S, et al. Genetic evidence linking SAP, the X-linked lymphoproliferative gene product, to Src-related kinase FynT in T(H)2 cytokine regulation. Immunity. 2004;21:707-717.
18. Tangye SG, Phillips JH, Lanier LL, Nichols KE. Functional requirement for SAP in 2B4-mediated activation of human natural killer cells as revealed by the X-linked lymphoproliferative syndrome. J Immunol. 2000;165:2932-2936.
19. 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;192:337-346.
20. Bottino C, Falco M, Parolini S, et al. NTB-A [correction of GNTB-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. 2001;194:235-246.
21. Sharifi R, Sinclair JC, Gilmour KC, et al. SAP mediates specific cytotoxic T-cell functions in X-linked lymphoproliferative disease. Blood. 2004;103:3821-3827.
22. Chen G, Tai AK, Lin M, Chang F, Terhorst C, Huber BT. Signaling lymphocyte activation molecule-associated protein is a negative regulator of the CD8 T cell response in mice. J Immunol. 2005;175:2212-2218.
23. Dupre L, Andolfi G, Tangye SG, et al. SAP controls the cytolytic activity of CD8+ T cells against EBV-infected cells. Blood. 2005;105:4383-4389.
24. Chung B, Aoukaty A, Dutz J, Terhorst C, Tan R. Signaling lymphocytic activation molecule-associated protein controls NKT cell functions. J Immunol. 2005;174:3153-3157.
25. Pasquier B, Yin L, Fondaneche 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;201:695-701.
26. Malbran A, Belmonte L, Ruibal-Ares B, et al. Loss of circulating CD27+ memory B cells and CCR4+ T cells occurring in association with elevated EBV loads in XLP patients surviving primary EBV infection. Blood. 2004;103:1625-1631.
27. Ma CS, Hare NJ, Nichols KE, et al. Impaired humoral immunity in X-linked lymphoproliferative disease is associated with defective IL-10 production by CD4+ T cells. J Clin Invest. 2005;115:1049-1059.
28. Sumegi J, Huang D, Lanyi A, et al. Correlation of mutations of the SH2D1A gene and Epstein-Barr virus infection with clinical phenotype and outcome in X-linked lymphoproliferative disease. Blood. 2000;96:3118-3125.
29. Seemayer TA, Gross TG, Egeler RM, et al. X-linked lymphoproliferative disease: twenty-five years after the discovery. Pediatr Res. 1995;38:471-478.
30. Purtilo DT, Grierson HL, Davis JR, Okano M. The X-linked lymphoproliferative disease: from autopsy toward cloning the gene 1975-1990. Pediatr Pathol. 1991;11:685-710.
31. Sullivan JL, Byron KS, Brewster FE, Baker SM, Ochs HD. X-linked lymphoproliferative syndrome. Natural history of the immunodeficiency. J Clin Invest. 1983;71:1765-1778.
32. Purtilo DT, Sakamoto K, Barnabei V, et al. Epstein-Barr virus-induced diseases in boys with the X-linked lymphoproliferative syndrome (XLP): update on studies of the registry. Am J Med. 1982;73:49-56.
33. Grierson HL, Skare J, Hawk J, Pauza M, Purtilo DT. Immunoglobulin class and subclass deficiencies prior to Epstein-Barr virus infection in males with X-linked lymphoproliferative disease. Am J Med Genet. 1991;40:294-297.
34. Brandau O, Schuster V, Weiss M, et al. Epstein-Barr virus-negative boys with non-Hodgkin lymphoma are mutated in the SH2D1A gene, as are patients with X-linked lymphoproliferative disease (XLP). Hum Mol Genet. 1999;8:2407-2413.
35. Sumazaki R, Kanegane H, Osaki M, et al. SH2D1A mutations in Japanese males with severe Epstein-Barr virus-associated illnesses. Blood. 2001;98:1268-1270.
36. Hugle B, Suchowerskyj P, Hellebrand H, et al. Persistent hypogammaglobulinemia following mononucleosis in boys is highly suggestive of X-linked lymphoproliferative disease - report of three cases. J Clin Immunol. 2004;24:515-522.
37. Sayos J, Martin M, Chen A, et al. Cell surface receptors Ly-9 and CD84 recruit the X-linked lymphoproliferative disease gene product SAP. Blood. 2001;97:3867-3874.
38. Tangye SG, Lazetic S, Woollatt E, Sutherland GR, Lanier LL, Phillips JH. Cutting edge: human 2B4, an activating NK cell receptor, recruits the protein tyrosine phosphatase SHP-2 and the adaptor signaling protein SAP. J Immunol. 1999;162:6981-6985.
39. Sidorenko SP, Clark EA. The dual-function CD150 receptor subfamily: the viral attraction. Nat Immunol. 2003;4:19-24.
40. Veillette A, Latour S. The SLAM family of immune-cell receptors. Curr Opin Immunol. 2003;15:277-285.
41. Veillette A, Latour S, Davidson D. Negative regulation of immunoreceptor signaling. Annu Rev Immunol. 2002;20:669-707.
42. Latour S, Roncagalli R, Chen R, et al. Binding of SAP SH2 domain to FynT SH3 domain reveals a novel mechanism of receptor signalling in immune regulation. Nat Cell Biol. 2003;5:149-154.
43. Chan B, Lanyi A, Song HK, et al. SAP couples Fyn to SLAM immune receptors. Nat Cell Biol. 2003;5:155-160.
44. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J Exp Med. 1984;160:521-540.
45. Lee KJ, Perez M, Pinschewer DD, de la Torre JC. Identification of the lymphocytic choriomeningitis virus (LCMV) proteins required to rescue LCMV RNA analogs into LCMV-like particles. J Virol. 2002;76:6393-6397.
46. Graham DB, Bell MP, McCausland MM, et al. Ly9 (CD229)-deficient mice exhibit T cell defects yet do not share several phenotypic characteristics associated with SLAM- and SAP-deficient mice. J Immunol. 2006;176:291-300.
47. Wright KE, Buchmeier MJ. Antiviral antibodies attenuate T-cell-mediated immunopathology following acute lymphocytic choriomeningitis virus infection. J Virol. 1991;65:3001-3006.
48. Ahmed R, Jamieson BD, Porter DD. Immune therapy of a persistent and disseminated viral infection. J Virol. 1987;61:3920-3929.
49. Buchmeier MJ, Zajac A. Lymphocytic choriomeningitis virus. In: Ahmed R, Chen I, eds. Persistent Viral Infections. New York, NY: John Wiley and Sons; 1999:575-605.
50. Fuller MJ, Khanolkar A, Tebo AE, Zajac AJ. Maintenance, loss, and resurgence of T cell responses during acute, protracted, and chronic viral infections. J Immunol. 2004;172:4204-4214.
51. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol. 2003;77:4911-4927.
52. Fuller MJ, Zajac AJ. Ablation of CD8 and CD4 T cell responses by high viral loads. J Immunol. 2003;170:477-486.
53. Morra M, Barrington RA, Abadia-Molina AC, et al. Defective B cell responses in the absence of SH2D1A. Proc Natl Acad Sci U S A. 2005;102:4819-4823.
54. Cannons JL, Yu LJ, Jankovic D, et al. SAP regulates T cell-mediated help for humoral immunity by a mechanism distinct from cytokine regulation. J Exp Med. 2006;203:1551-1565.
55. Smith KG, Hewitson TD, Nossal GJ, Tarlinton DM. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur J Immunol. 1996;26:444-448.
56. Tarlinton DM, Hodgkin PD. Targeting plasma cells in autoimmune diseases. J Exp Med. 2004;199:1451-1454.
57. Jamieson BD, Butler LD, Ahmed R. Effective clearance of a persistent viral infection requires cooperation between virus-specific Lyt2+ T cells and nonspecific bone marrow-derived cells. J Virol. 1987;61:3930-3937.
58. Homann D, Tishon A, Berger DP, Weigle WO, von Herrath MG, Oldstone MB. Evidence for an underlying CD4 helper and CD8 T-cell defect in B-cell-deficient mice: failure to clear persistent virus infection after adoptive immunotherapy with virus-specific memory cells from muMT/muMT mice. J Virol. 1998;72:9208-9216.
59. Matloubian M, Concepcion RJ, Ahmed R. CD4+ T cells are required to sustain CD8+ cytotoxic T-cell responses during chronic viral infection. J Virol. 1994;68:8056-8063.
60. Volkert M, Larsen JH, Pfau C. Studies on immunological tolerance to LCM virus. 4. The question of immunity in adoptively immunized virus carriers. Acta Pathol Microbiol Scand. 1964;61:268-282.
61. Baldridge JR, McGraw TS, Paoletti A, Buchmeier MJ. Antibody prevents the establishment of persistent arenavirus infection in synergy with endogenous T cells. J Virol. 1997;71:755-758.
62. Planz O, Ehl S, Furrer E, et al. A critical role for neutralizing- antibody-producing B cells, CD4(+) T cells, and interferons in persistent and acute infections of mice with lymphocytic choriomeningitis virus: implications for adoptive immunotherapy of virus carriers. Proc Natl Acad Sci U S A. 1997;94:6874-6879.
63. Thomsen AR, Johansen J, Marker O, Christensen JP. Exhaustion of CTL memory and recrudescence of viremia in lymphocytic choriomeningitis virus-infected MHC class II-deficient mice and B cell-deficient mice. J Immunol. 1996;157:3074-3080.
64. Recher M, Lang KS, Hunziker L, et al. Deliberate removal of T cell help improves virus-neutralizing antibody production. Nat Immunol. 2004;5:934-942.
65. Wherry EJ, Ahmed R. Memory CD8 T-cell differentiation during viral infection. J Virol. 2004;78:5535-5545.
66. Kagi D, Ledermann B, Burki K, Zinkernagel RM, Hengartner H. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu Rev Immunol. 1996;14:207-232.
67. Zajac AJ, Blattman JN, Murali-Krishna K, et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med. 1998;188:2205-2213.
68. Welsh RM, Selin LK, Szomolanyi-Tsuda E. Immunological memory to viral infections. Annu Rev Immunol. 2004;22:711-743.
69. Wherry EJ, Barber DL, Kaech SM, Blattman JN, Ahmed R. Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A. 2004;101:16004-16009.
70. Oldstone MB, Blount P, Southern PJ, Lampert PW. Cytoimmunotherapy for persistent virus infection reveals a unique clearance pattern from the central nervous system. Nature. 1986;321:239-243.
71. Moskophidis D, Lechner F, Pircher H, Zinkernagel RM. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 1993;362:758-761.
72. Odermatt B, Eppler M, Leist TP, Hengartner H, Zinkernagel RM. Virus-triggered acquired immunodeficiency by cytotoxic T-cell-dependent destruction of antigen-presenting cells and lymph follicle structure. Proc Natl Acad Sci U S A. 1991;88:8252-8256.
73. Whitmire JK, Slifka MK, Grewal IS, Flavell RA, Ahmed R. CD40 ligand-deficient mice generate a normal primary cytotoxic T- lymphocyte response but a defective humoral response to a viral infection. J Virol. 1996;70:8375-8381.
74. Thorley-Lawson DA. Epstein-Barr virus: exploiting the immune system. Nat Rev Immunol. 2001;1:75-82.
75. Nistala K, Gilmour KC, Cranston T, et al. X-linked lymphoproliferative disease: three atypical cases. Clin Exp Immunol. 2001;126:126-130.
76. Morra M, Howie D, Grande MS, et al. X-linked lymphoproliferative disease: a progressive immunodeficiency. Annu Rev Immunol. 2001;19:657-682.
77. Purtilo DT, Cassel CK, Yang JP, Harper R. X-linked recessive progressive combined variable immunodeficiency (Duncan's disease). Lancet. 1975;1:935-940.
78. Matloubian M, Suresh M, Glass A, et al. A role for perforin in downregulating T-cell responses during chronic viral infection. J Virol. 1999;73:2527-2536.
79. Walsh CM, Matloubian M, Liu CC, et al. Immune function in mice lacking the perforin gene. Proc Natl Acad Sci U S A. 1994;91:10854-10858.
80. Storm P, Bartholdy C, Sorensen MR, Christensen JP, Thomsen AR. Perforin-deficient CD8+ T cells mediate fatal lymphocytic choriomeningitis despite impaired cytokine production. J Virol. 2006;80:1222-1230.
81. Puglielli MT, Browning JL, Brewer AW, et al. Reversal of virus-induced systemic shock and respiratory failure by blockade of the lymphotoxin pathway. Nat Med. 1999;5:1370-1374.
82. Binder D, van den Broek MF, Kagi D, et al. Aplastic anemia rescued by exhaustion of cytokine-secreting CD8+ T cells in persistent infection with lymphocytic choriomeningitis virus. J Exp Med. 1998;187:1903-1920.
83. Zajac AJ, Muller D, Pederson K, Frelinger JA, Quinn DG. Natural killer cell activity in lymphocytic choriomeningitis virus-infected beta 2-microglobulin-deficient mice. Int Immunol. 1995;7:1545-1556.
84. Su HC, Nguyen KB, Salazar-Mather TP, Ruzek MC, Dalod MY, Biron CA. NK cell functions restrain T cell responses during viral infections. Eur J Immunol. 2001;31:3048-3055.
85. Tay CH, Welsh RM, Brutkiewicz RR. NK cell response to viral infections in beta 2-microglobulin-deficient mice. J Immunol. 1995;154:780-789.