Evolving role of 2B4/CD244 int and NK cell responses during virus infection

Frontiers in Immunology

Volumn 3, Issue DEC, 2012, Pages

  Waggoner, Stephen N ^a   Kumar, Vinay ^b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

2B4; NK cells; SLAM receptors; T cells; Virus infection; Xlp

Indexed keywords

EID: 84874268034     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00377     Document Type: Short Survey

References (93)

1. Ahlenstiel, G., Edlich, B., Hogdal, L. J., Rotman, Y., Noureddin, M., Feld, J. J., etal. (2011). Early changes in natural killer cell function indicate virologic response to interferon therapy for hepatitis C. Gastroenterology 141,1231-1239.
2. Aldy, K. N., Horton, N. C., Mathew, P. A., and Mathew, S. O. (2011). 2B4+ CD8+ T cells play an inhibitory role against constrained HIV epitopes. Biochem. Biophys. Res. Commun. 405, 503-507.
3. Altvater, B., Landmeier, S., Pscherer, S., Temme, J., Juergens, H., Pule, M. etal. (2009). 2B4 (CD244) signaling via chimeric receptors costimulates tumor-antigen specific proliferation and in vitro expansion of human T cells. Cancer Immunol. Immunother. 58,1991-2001.
4. Andrews, D. M., Estcourt, M. J., Ando-niou, C. E., Wikstrom, M. E., Khong, A., Voigt, V., etal. (2010). Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J. Exp. Med. 207, 1333-1343.
5. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B., and Lanier, L. L. (2002). Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323-1326.
6. Assarsson, E., Kambayashi, T., Schatzle, J. D., Cramer, S. O., von Bonin, A., Jensen, P. E., etal. (2004). NK cells stimulate proliferation of T and NK cells through 2B4/CD48 interactions. J. Immunol. 173,174-180.
7. Bengsch, B., Seigel, B., Ruhl, M., Timm, J., Kuntz, M., Blum, H. E., etal. (2010). Coexpres-sion of PD-1, 2B4, CD160 and KLRG1 on exhausted HCV-specific CD8+ T cells is linked to antigen recognition and T cell differentiation. PLoS Pathog. 6:e1000947. doi: 10.1371/journal.ppat.1000947
8. Biron, C. A., Byron, K. S., and Sullivan, J. L. (1989). Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 320,1731-1735.
9. Blackburn, S. D., Shin, H., Haining, W. N., Zou, T., Workman, C. J., Pol-ley, A., etal. (2009). Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10, 29-37.
10. Bottino, C., Falco, M., Parolini, S., Marcenaro, E., Augugliaro, R., Sivori, S., etal. (2001). NTB-A, a novel SH2D 1A-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.
11. Brown, M. G., Dokun, A. O., Heusel, J. W., Smith, H. R., Beckman, D. L., Blattenberger, E. A., etal. (2001). Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292, 934-937.
12. Brutkiewicz, R. R., and Welsh, R. M. (1995). Major histocompatibil-ity complex class I antigens and the control of viral infections by natural killer cells. J. Virol. 69, 3967-3971.
13. Bukowski, J. F., Woda, B. A., Habu, S., Okumura, K., and Welsh, R. M. (1983). Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 131,1531-1538.
14. Bukowski, J. F., Woda, B. A., and Welsh, R. M. (1984). Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice. J. Virol. 52, 119-128.
15. Cannons, J. L., Qi, H., Lu, K. T., Dutta, M., Gomez-Rodriguez, J., Cheng, J., etal. (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.
16. Cannons, J. L., Tangye, S. G., and Schwartzberg, P. L. (2011). SLAM family receptors and SAP adaptors in immunity. Annu. Rev. Immunol. 29, 665-705.
17. Chen, G., Tai, A. K., Lin, M., Chang, E, Terhorst, C., and Huber, B. T. (2005). Signaling lymphocyte activation molecule-associated protein is a negative regulator of the CD8 T cell response in mice. J. Immunol. 175, 2212-2218.
18. Chlewicki, L. K., Velikovsky, C. A., Bal-akrishnan, V., Mariuzza, R. A., and Kumar, V. (2008). Molecular basis of the dual functions of 2B4 (CD244). J. Immunol. 180,8159-8167.
19. Chung, B., Aoukaty, A., Dutz, J., Terhorst, C., and Tan, R. (2005). Signaling lymphocytic activation molecule-associated protein controls NKT cell functions. J. Immunol. 174,3153-3157.
20. Coffey, A. J., Brooksbank, R. A., Bran-dau, O., Oohashi, T., Howell, G. R., Bye, J. M., et al. (1998). Host response to EBV infection in X-linked lym-phoproliferative disease results from mutations in an SH2-domain encoding gene. Nat. Genet. 20, 129-135.
21. Crawford, A., and Wherry, E. J. (2009). The diversity of costimulatory and inhibitory receptor pathways and the regulation of antiviral T cell responses. Curr. Opin. Immunol. 21, 179-186.
22. Crotty, S., Kersh, E. N., Cannons, J., Schwartzberg, P. L., and Ahmed, R. (2003). SAP is required for generating long-term humoral immunity. Nature 421,282-287.
23. Crotty, S., McCausland, M. M., Aubert, R. D., Wherry, E. J., and Ahmed, R. (2006). Hypogammaglobulinemia and exacerbated CD8 T-cell-media-ted immunopathology in SAP-deficient mice with chronic LCMV infection mimics human XLP disease. Blood 108, 3085-3093.
24. Czar, M. J., Kersh, E. N., Mijares, L. A., Lanier, G., Lewis, J., Yap, G., etal. (2001). Altered lymphocyte responses and cytokine production in mice deficient in the X-linked lym-phoproliferative disease gene SH2D-1A/DSHP/SAP. Proc. Natl. Acad. Sci. U.S.A. 98,7449-7454.
25. Daniels, K. A., Devora, G., Lai, W. C., O'Donnell, C. L., Bennett, M., and Welsh, R. M. (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.
26. Dupre, L., Andolfi, G., Tangye, S. G., Clementi, R., Locatelli, F., Arico, M., etal. (2005). SAP controls the cytolytic activity of CD8+ T cells against EBV-infected cells. Blood 105, 4383-4389.
27. Engel, P., , N., Alba, M. M., Robertson, K., Ghazal, P., and Angulo, A. (2011). Human cytomegalovirus UL7, a homo-logue of the SLAM-family receptor CD229, impairs cytokine production. Immunol. Cell Biol. 89, 753-766.
28. Enose-Akahata, Y., Matsuura, E., Oh, U., and Jacobson, S. (2009). High expression of CD244 and SAP regulated CD8 T cell responses of patients with HTLV-I associated neurologic disease. PLoS Pathog. 5:e1000682. doi: 10.1371/journal.ppat.1000682
29. Griewank, K., Borowski, C., Riet-dijk, S., Wang, N., Julien, A., Wei, D. G., etal. (2007). Homotypic interactions mediated by Slamf 1 and Slamf6 receptors control NKT cell lineage development. Immunity 27, 751-762.
30. Hislop, A. D., Palendira, U., Leese, A. M., Arkwright, P. D., Rohrlich, P. S., Tangye, S. G., etal. (2010). Impaired Epstein-Barr virus-specific CD8+ T-cell function in X-linked lymphopro-liferative disease is restricted to SLAM family-positive B-cell targets. Blood 116,3249-3257.
31. Jennes, W., Verheyden, S., Demanet, C., Adje-Toure, C. A., Vuylsteke, B., Nkengasong, J. N., etal. (2006). Cutting edge: resistance to HIV-1 infection among African female sex workers is associated with inhibitory KIR in the absence of their HLA ligands.J. Immunol. 177,6588-6592.
32. Jost, S., Reardon, J., Peterson, E., Poole, D., Bosch, R., Alter, G., etal. (2011). Expansion of 2B4+ natural killer (NK) cells and decrease in NKp46+ NK cells in response to influenza. Immunology 132, 516-526.
33. Kageyama, R., Cannons, J. L., Zhao, F., Yusuf, I., Lao, C., Locci, M., etal. (2012). The receptor Ly108 functions as a SAP adaptor-dependent on-off switch for T cell help to B cells and NKT cell development. Immunity 36, 986-1002.
34. Kambayashi, T., Assarsson, E., Chambers, B. J., and Ljunggren, H. G. (2001). Cutting edge: regulation of CD8+ T cell proliferation by 2B4/CD48 interactions. J. Immunol. 167,6706-6710.
35. Khakoo, S. I., Thio, C. L., Martin, M. P., Brooks, C. R., Gao, X., Astemborski, J., etal. (2004). HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305, 872-874.
36. Kubin, M. Z., Parshley, D. L., Din, W., Waugh, J. Y., Davis-Smith, T., Smith, C. A., et al. (1999). Molecular cloning and biological characterization of NK cell activation-inducing ligand, a counterstructure for CD48. Eur. J. Immunol. 29, 3466-3477.
37. Lang, P. A., Lang, K. S., Xu, H. C., Grusdat, M., Parish, I. A., Recher, M., etal. (2012). Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl. Acad. Sci. U.S.A. 109, 1210-1215.
38. Lee, K. M., Bhawan, S., Majima, T., Wei, H., Nishimura, M. I., Yagita, H., etal. (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.
39. Lee, K. M., McNerney, M. E., Stepp, S. E., Mathew, P. A., Schatzle, J. D., Bennett, M., etal. (2004). 2B4 acts as anon-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J. Exp. Med. 199,1245-1254.
40. Lee, S. H., Girard, S., Macina, D., Busa, M., Zafer, A., Belouchi, A., etal. (2001). Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28,42-45.
41. Lee, S. H., Kim, K. S., Fodil-Cornu, N., Vidal, S. M., and Biron, C. A. (2009). Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 206, 2235-2251.
42. Ma, C. S., Hare, N. J., Nichols, K. E., Dupre, L., Andolfi, G., Roncar-olo, M. G., etal. (2005). Impaired humoral immunity in X-linked lym-phoproliferative disease is associated with defective IL-10 production by CD4+ T cells. J. Clin. Invest. 115, 1049-1059.
43. Malbran, A., Belmonte, L., Ruibal-Ares, B., Bare, P., Massud, I., Parodi, C., etal. (2004). 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 103,1625-1631.
44. Marcoe, J. P., Lim, J. R., Schaubert, K. L., Fodil-Cornu, N., Matka, M., McCub-brey, A. L., etal. (2012). TGF-beta is responsible for NK cell immaturity during ontogeny and increased susceptibility to infection during mouse infancy. Nat. Immunol. 13, 843-850.
45. Martin, M. P., Qi, Y., Gao, X., Yamada, E., Martin, J. N., Pereyra, F., etal. (2007). Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat. Genet. 39, 733-740.
46. Mathew, S. O., Rao, K. K., Kim, J. R., Bambard, N. D., and Mathew, P. A. (2009). Functional role of human NK cell receptor 2B4 (CD244) isoforms. Eur. J. Immunol. 39, 1632-1641.
47. McNerney, M. E., Guzior, D., and Kumar, V (2005a). 2B4 (CD244)-CD48 interactions provide a novel MHC class I-independent system for NK-cell self-tolerance in mice. Blood 106, 1337-1340.
48. McNerney, M. E., Lee, K. M., and Kumar, V (2005b). 2B4 (CD244) is a non-MHC binding receptor with multiple functions on natural killer cells and CD8+ T cells. Mol. Immunol. 42,489-494.
49. Mitrovic, M., Arapovic, J., Jordan, S., Fodil-Cornu, N., Ebert, S., Vidal, S. M., etal. (2012). The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8+ T-cell response. J. Virol. 86,2165-2175.
50. Mooney, J. M., Klem, J., Wulfing, C., Mijares, L. A., Schwartzberg, P. L., Bennett, M., etal. (2004). The murine NK receptor 2B4 (CD244) exhibits inhibitory function independent of signaling lymphocytic activation molecule-associated protein expression. J. Immunol. 173, 3953- 3961.
51. Nakajima, H., Cella, M., Bouchon, A., Grierson, H. L., Lewis, J., Duck-ett, C. S., etal. (2000). Patients with X-linked lymphoproliferative disease have a defect in 2B4 receptor-mediated NK cell cytotoxicity. Eur. J. Immunol. 30,3309-3318.
52. Narni-Mancinelli, E., Jaeger, B. N., Bernat, C., Fenis, A., Kung, S., De Gassart, A., etal. (2012). Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 335, 344-348.
53. Nichols, K. E., Hom, J., Gong, S. Y., Ganguly, A., Ma, C.S., Cannons, J. L., et al. (2005). Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 11, 340-345.
54. Ostrowski, S. R., Ullum, H., Pedersen, B. K., Gerstoft, J., and Katzenstein, T. L. (2005). 2B4 expression on natural killer cells increases in HIV-1 infected patients followed prospec-tively during highly active antiretro-viral therapy. Clin. Exp. Immunol. 141,526-533.
55. Palendira, U., Low, C., Chan, A., Hislop, A. D., Ho, E., Phan, T. G., etal. (2011). Molecular pathogene-sis of EBV susceptibility in XLP as revealed by analysis of female carriers with heterozygous expression of SAP. PLoS Biol. 9:e1001187. doi: 10.1371/journal.pbio.1001187
56. Parolini, S., Bottino, C., Falco, M., Augugliaro, R., Giliani, S., Frances-chini, R., etal. (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.
57. Pasquier, B., Yin, L., Fondaneche, M. C., Relouzat, F., Bloch-Queyrat, C., Lambert, N., etal. (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.
58. Qi, H., Cannons, J. L., Klauschen, F., Schwartzberg, P. L., and Germain, R. N. (2008). SAP-controlled T-B cell interactions underlie germinal centre formation. Nature 455, 764-769.
59. Rabinovich, B. A., Li, J., Shannon, J., Hurren, R., Chalupny, J., Cosman, D., etal. (2003). Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J. Immunol. 170, 3572-3576.
60. Raulet, D. H. (2003). Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3, 781-790.
61. Raziorrouh, B., Schraut, W., Gerlach, T., Nowack, D., Gruner, N. H., Ulsenheimer, A., etal. (2010). The immunoregulatory role of CD244 in chronic hepatitis B infection and its inhibitory potential on virus-specific CD8+ T-cell function. Hepatology 52, 1934-1947.
62. Robbins, S. H., Bessou, G., Cornil-lon, A., Zucchini, N., Rupp, B., Ruzsics, Z., etal. (2007). Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 3:e123. doi: 10.1371/ journal.ppat.0030123
63. Schatzle, J. D., Sheu, S., Stepp, S. E., Mathew, P. A., Bennett, M., and Kumar, V. (1999). Characterization of inhibitory and stimulatory forms of the murine natural killer cell receptor 2B4. Proc. Natl. Acad. Sci. U.S.A. 96,3870-3875.
64. Schlaphoff, V., Lunemann, S., Suneetha, P. V., Jaroszewicz, J., Grabowski, J., Dietz, J., etal. (2011). Dual function of the NK cell receptor 2B4 (CD244) in the regulation of HCV-specific CD8+ T cells. PLoS Pathog. 7:e1002045. doi: 10.1371/journal.ppat.1002045
65. Shah, A. H., Sowrirajan, B., Davis, Z. B., Ward, J. P., Campbell, E. M., Planelles, V., etal. (2010). Degranu-lation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 8, 397-409.
66. Sharifi, R., Sinclair, J. C., Gilmour, K. C., Arkwright, P. D., Kinnon, C., Thrasher, A. J., etal. (2004). SAP mediates specific cytotoxic T-cell functions in X-linked lymphoproliferative disease. Blood 103, 3821-3827.
67. Shin, H., and Wherry, E. J. (2007). CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19,408-415.
68. Smith, H. R., Heusel, J. W., Mehta, I. K., Kim, S., Dorner, B. G., Naidenko, O. V., etal. (2002). Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. U.S.A. 99, 8826-8831.
69. Soderquest, K., Walzer, T., Zafirova, B., Klavinskis, L. S., Polic, B., Vivier, E., etal. (2011). Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 186,3304-3308.
70. Stadnisky, M. D., Xie, X., Coats, E. R., Bullock, T. N., and Brown, M. G. (2011). Self MHC class I-licensed NK cells enhance adaptive CD8 T-cell viral immunity. Blood 117, 5133- 5141.
71. Stepp, S. E., Schatzle, J. D., Bennett, M., Kumar, V., and Mathew, P. A. (1999). Gene structure of the murine NK cell receptor 2B4: presence of two alternatively spliced isoforms with distinct cytoplasmic domains. Eur. J. Immunol. 29, 2392-2399.
72. Su, H. C., Nguyen, K. B., Salazar-Mather, T. P., Ruzek, M. C., Dalod, M. Y., and Biron, C. A. (2001). NK cell functions restrain T cell responses during viral infections. Eur. J. Immunol. 31, 3048-3055.
73. Sun, C., Fu, B., Gao, Y., Liao, X., Sun, R., Tian, Z., etal. (2012). TGF-β1 down-regulation of NKG2D/DAP10 and 2B4/SAP expression on human NK cells contributes to HBV persistence. PLoS Pathog. 8:e1002594. doi: 10.1371/journal.ppat.1002594
74. Tangye, S. G., Cherwinski, H., Lanier, L. L., and Phillips, J. H. (2000a). 2B4-mediated activation of human natural killer cells. Mol. Immunol. 37, 493-501.
75. Tangye, S. G., Phillips, J. H., Lanier, L. L., and Nichols, K. E. (2000b). 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.
76. Taniguchi, R. T., Guzior, D., and Kumar, V. (2007). 2B4 inhibits NK-cell fratricide. Blood 110, 2020-2023.
77. Tatsuo, H., Ono, N., Tanaka, K., and Yanagi, Y. (2000). SLAM (CDw150) is a cellular receptor for measles virus. Nature 406, 893-897.
78. Thorley-Lawson, D. A., Schooley, R. T., Bhan, A. K., and 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.
79. Tomescu, C., Duh, R M., Hoh, R., Viviani, A., Harvill, K., Martin, M. P., etal. (2012). Impact of protective KIR/HLA genotypes on NK cell and T cell function in HIV-1 infected controllers. AIDS 26, 1869-1878.
80. Vaidya, S. V., Stepp, S. E., McNerney, M. E., Lee, J. K., Bennett, M., Lee, K. M., etal. (2005). Targeted disruption of the 2B4 gene in mice reveals an in vivo role of 2B4 (CD244) in the rejection of B16 melanoma cells. J. Immunol. 174, 800-807.
81. Veillette, A. (2006). NK cell regulation by SLAM family receptors and SAP-related adapters. Immunol. Rev. 214, 22-34.
82. Veillette, A., Dong, Z., Perez-Quintero, L. A., Zhong, M. C., and Cruz-Munoz, M. E. (2009). Importance and mechanism of 'switch' function of SAP family adapters. Immunol. Rev. 232, 229-239.
83. Vivier, E., and Anfossi, N. (2004). Inhibitory NK-cell receptors on T cells: witness of the past, actors of the future. Nat. Rev. Immunol. 4, 190-198.
84. Waggoner, S. N., Cornberg, M., Selin, L. K., and Welsh, R. M. (2012). Natural killer cells act as rheostats modulating antiviral T cells. Nature 481, 394-398.
85. Waggoner, S. N., Taniguchi, R. T., Mathew, P. A., Kumar, V., and Welsh, R. M. (2010). Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J. Clin. Invest. 120,1925-1938.
86. Ward, J., Bonaparte, M., Sacks, J., Guterman, J., Fogli, M., Mavilio, D., etal. (2007). HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts. Blood 110, 1207-1214.
87. Welsh, R. M., Brubaker, J. O., Vargas-Cortes, M., and O'Donnell, C. L. (1991). Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J. Exp. Med. 173,1053-1063.
88. West, E. E., Youngblood, B., Tan, W. G., Jin, H. T., Araki, K., Alexe, G., etal. (2011). Tight regulation of memory CD8+ T cells limits their effectiveness during sustained high viral load. Immunity 35, 285-298.
89. Wherry, E. J., Ha, S. J., Kaech, S. M., Haining, W. N., Sarkar, S., Kalia, V., etal. (2007). Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27, 670-684.
90. Wu, C., Nguyen, K. B., Pien, G. C., Wang, N., Gullo, C., Howie, D., etal. (2001). SAP controls T cell responses to virus and terminal differentiation of TH2 cells. Nat. Immunol. 2, 410-414.
91. Yin, L., Al-Alem, U., Liang, J., Tong, W. M., Li, C., Badiali, M., etal. (2003). Mice deficient in the X-linked lymphoproliferative disease gene sap exhibit increased susceptibility to murine gammaherpesvirus-68 and hypo-gammaglobulinemia. J. Med. Virol. 71,446-455.
92. Yusuf, I., Kageyama, R., Monticelli, L., Johnston, R. J., Ditoro, D., Hansen, K., etal. (2010). Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 185, 190-202.
93. Zinkernagel, R. M., and Welsh, R. M. (1976). H-2 compatibility requirement for virus-specific T cell-mediated effector functions in vivo. I. Specificity of T cells conferring antiviral protection against lymphocytic choriomeningitis virus is associated with H-2K and H-2D. J. Immunol. 117,1495-1502