Interferon type I responses in primary and secondary infections

Immunology and Cell Biology

Volumn 86, Issue 3, 2008, Pages 239-245

  Alsharifi, Mohammed ^a   Müllbacher, Arno ^a   Regner, Matthias ^a  

^a Biology and Environment   (Australia)

Author keywords

Immunoregulation; Type I interferon; Viral infections

Indexed keywords

ALPHA1 INTERFERON; BETA1 INTERFERON;

ANTIVIRAL ACTIVITY; B LYMPHOCYTE; CYTOKINE PRODUCTION; DENDRITIC CELL; HOST SUSCEPTIBILITY; IMMUNOREGULATION; LYMPHOCYTE ACTIVATION; MEMORY T LYMPHOCYTE; NONHUMAN; PROTEIN FUNCTION; REVIEW; T LYMPHOCYTE; VIRUS INFECTION;

ANIMALS; DENDRITIC CELLS; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNITY, ACTIVE; IMMUNITY, NATURAL; IMMUNOLOGIC MEMORY; INFECTION; INTERFERON TYPE I; LYMPHOCYTE ACTIVATION;

MAMMALIA; MUS; VERTEBRATA;

EID: 41149122141     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/sj.icb.7100159     Document Type: Review

References (125)

1. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond Biol Sci 1957; 147: 258-267.
2. Pestka S, Langer JA, Zoon KC, Samuel CE. Interferons and their actions. Annu Rev Biochem 1987; 56: 727-777.
3. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev 2001; 14: 778-809.
4. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 2003; 4: 63-68.
5. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003; 4: 69-77.
6. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 2006; 80: 4501-4509.
7. Ank N, West H, Paludan SR. IFN-lambda: novel antiviral cytokines. J Interferon Cytokine Res 2006; 26: 373-379.
8. Smith PL, Lombardi G, Foster GR. Type I interferons and the innate immune response - more than just antiviral cytokines. Mol Immunol 2005; 42: 869-877.
9. Pestka S, Krause CD, Walter MR. Interferons, interferon-like cytokines, and their receptors. Immunol Rev 2004; 202: 8-32.
10. Lefevre F, Guillomot M, D'Andrea S, Battegay S, La Bonnardiere C. Interferon-delta: the first member of a novel type I interferon family. Biochimie 1998; 80: 779-788.
11. Roberts RM, Cross JC, Leaman DW. Unique features of the trophoblast interferons. Pharmacol Ther 1991; 51: 329-345.
12. Hardy MP, Owczarek CM, Jermiin LS, Ejdeback M, Hertzog PJ. Characterization of the type I interferon locus and identification of novel genes. Genomics 2004; 84: 331-345.
13. LaFleur DW, Nardelli B, Tsareva T, Mather D, Feng P, Semenuk M et al. Interferon-kappa, a novel type I interferon expressed in human keratinocytes. J Biol Chem 2001; 276: 39765-39771.
14. Capon DJ, Shepard HM, Goeddel DV. Two distinct families of human and bovine interferon-alpha genes are coordinately expressed and encode functional polypeptides. Mol Cell Biol 1985; 5: 768-779.
15. Colamonici OR, Pfeffer LM, D'Alessandro F, Platanias LC, Gregory SA, Rosolen A et al. Multichain structure of the IFN-alpha receptor on hematopoietic cells. J Immunol 1992; 148: 2126-2132.
16. Novick D, Cohen B, Rubinstein M. The human interferon alpha/beta receptor: characterization and molecular cloning. Cell 1994; 77: 391-400.
17. Darnell Jr JE. STATs and gene regulation. Science 1997; 277: 1630-1635.
18. Darnell Jr JE, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994; 264: 1415-1421.
19. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM et al. Functional role of type I and type II interferons in antiviral defense. Science 1994; 264: 1918-1921.
20. Foster GR, Finter NB. Are all type I human interferons equivalent? J Viral Hepat 1998; 5: 143-152.
21. Walter MR, Bordens R, Nagabhushan TL, Williams BR, Herberman RB, Dinarello CA et al. Review of recent developments in the molecular characterization of recombinant alfa interferons on the 40th anniversary of the discovery of interferon. Cancer Biother Radiopharm 1998; 13: 143-154.
22. Schlaak JF, Hilkens CM, Costa-Pereira AP, Strobl B, Aberger F, Frischauf AM et al. Cell-type and donor-specific transcriptional responses to interferon-alpha. Use of customized gene arrays. J Biol Chem 2002; 277: 49428-49437.
23. De Maeyer E, De Maeyer-Guignard J. Type I interferons. Int Rev Immunol 1998; 17: 53-73.
24. Belardelli F, Gresser I. The neglected role of type I interferon in the T-cell response: implications for its clinical use. Immunol Today 1996; 17: 369-372.
25. Cella M, Jarrossay D, Facchetti F, Alebardi O, Nakajima H, Lanzavecchia A et al. Plasmacytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med 1999; 5: 919-923.
26. Eloranta ML, Sandberg K, Ricciardi-Castagnoli P, Lindahl M, Alm GV. Production of interferon-alpha/beta by murine dendritic cell lines stimulated by virus and bacteria. Scand J Immunol 1997; 46: 235-241.
27. Rodel J, Groh A, Vogelsang H, Lehmann M, Hartmann M, Straube E. Beta interferon is produced by Chlamydia trachomatis-infected fibroblast-like synoviocytes and inhibits gamma interferon-induced HLA-DR expression. Infect Immun 1998; 66: 4491-4495.
28. Sing A, Merlin T, Knopf HP, Nielsen PJ, Loppnow H, Galanos C et al. Bacterial induction of beta interferon in mice is a function of the lipopolysaccharide component. Infect Immun 2000; 68: 1600-1607.
29. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, Dezutter-Dambuyant C et al. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat Immunol 2001; 2: 1144-1150.
30. Siegal FP, Kadowaki N, Shodell M, Fitzgerald-Bocarsly PA, Shah K, Ho S et al. The nature of the principal type 1 interferon-producing cells in human blood. Science 1999; 284: 1835-1837.
31. Cella M, Salio M, Sakakibara Y, Langen H, Julkunen I, Lanzavecchia A. Maturation, activation, and protection of dendritic cells induced by double-stranded RNA. J Exp Med 1999; 189: 821-829.
32. Le Bon A, Tough DF. Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 2002; 14: 432-436.
33. Diebold SS, Montoya M, Unger H, Alexopoulou L, Roy P, Haswell LE et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003; 424: 324-328.
34. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006; 25: 373-381.
35. Muzio M, Bosisio D, Polentarutti N, D'Amico G, Stoppacciaro A, Mancinelli R et al. Differential expression and regulation of Toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 2000; 164: 5998-6004.
36. Uematsu S, Akira S. Toll-like Receptors and type I Interferons. J Biol Chem 2007; 282: 15319-15323.
37. Carpenter S, O'Neill L A. How important are Toll-like receptors for antimicrobial responses? Cell Microbiol 2007; 9: 1891-1901.
38. Levy DE, Marie I, Smith E, Prakash A. Enhancement and diversification of IFN induction by IRF-7-mediated positive feedback. J Interferon Cytokine Res 2002; 22: 87-93.
39. Miettinen M, Sareneva T, Julkunen I, Matikainen S. IFNs activate Toll-like receptor gene expression in viral infections. Genes Immun 2001; 2: 349-355.
40. Heinz S, Haehnel V, Karaghiosoff M, Schwarzfischer L, Muller M, Krause SW et al. Species-specific regulation of Toll-like receptor 3 genes in men and mice. J Biol Chem 2003; 278: 21502-21509.
41. Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, Briere F et al. Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 2002; 195: 517-528.
42. Deonarain R, Alcami A, Alexiou M, Dallman MJ, Gewert DR, Porter AC. Impaired antiviral response and alpha/beta interferon induction in mice lacking beta interferon. J Virol 2000; 74: 3404-3409.
43. Sen GC, Ransohoff RM. Interferon-induced antiviral actions and their regulation. Adv Virus Res 1993; 42: 57-102.
44. van den Broek MF, Muller U, Huang S, Zinkernagel RM, Aguet M. Immune defence in mice lacking type I and/or type II interferon receptors. Immunol Rev 1995; 148: 5-18.
45. Zhou A, Paranjape J, Brown TL, Nie H, Naik S, Dong B et al. Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J 1997; 16: 6355-6363.
46. Leib DA, Machalek MA, Williams BR, Silverman RH, Virgin HW. Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci USA 2000; 97: 6097-6101.
47. Bergmann M, Garcia-Sastre A, Carnero E, Pehamberger H, Wolff K, Palese P et al. Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J Virol 2000; 74: 6203-6206.
48. Levy DE, Garcia-Sastre A. The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev 2001; 12: 143-156.
49. Jaramillo ML, Abraham N, Bell JC. The interferon system: a review with emphasis on the role of PKR in growth control. Cancer Invest 1995; 13: 327-338.
50. Ryman KD, Klimstra WB, Nguyen KB, Biron CA, Johnston RE. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J Virol 2000; 74: 3366-3378.
51. White LJ, Wang JG, Davis NL, Johnston RE. Role of alpha/beta interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5′ untranslated region. J Virol 2001; 75: 3706-3718.
52. Lobigs M, Mullbacher A, Wang Y, Pavy M, Lee E. Role of type I and type II interferon responses in recovery from infection with an encephalitic flavivirus. J Gen Virol 2003; 84: 567-572.
53. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu Rev Immunol 1999; 17: 189-220.
54. Jewett A, Bonavida B. Interferon-alpha activates cytotoxic function but inhibits interleukin-2-mediated proliferation and tumor necrosis factor-alpha secretion by immature human natural killer cells. J Clin Immunol 1995; 15: 35-44.
55. Becknell B, Caligiuri MA. Interleukin-2, interleukin-15, and their roles in human natural killer cells. Adv Immunol 2005; 86: 209-239.
56. Waldmann TA, Tagaya Y. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol 1999; 17: 19-49.
57. Nguyen KB, Cousens LP, Doughty LA, Pien GC, Durbin JE, Biron CA. Interferon alpha/ beta-mediated inhibition and promotion of interferon gamma: STAT1 resolves a paradox. Nat Immunol 2000; 1: 70-76.
58. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 1997; 15: 323-350.
59. Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature 1974; 248: 701-702.
60. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-gamma. Annu Rev Immunol 1997; 15: 749-795.
61. Luft T, Pang KC, Thomas E, Hertzog P, Hart DN, Trapani J et al. Type I IFNs enhance the terminal differentiation of dendritic cells. J Immunol 1998; 161: 1947-1953.
62. Gallucci S, Lolkema M, Matzinger P. Natural adjuvants: endogenous activators of dendritic cells. Nat Med 1999; 5: 1249-1255.
63. Mattei F, Schiavoni G, Belardelli F, Tough DF. IL-15 is expressed by dendritic cells in response to type I IFN, double-stranded RNA, or lipopolysaccharide and promotes dendritic cell activation. J Immunol 2001; 167: 1179-1187.
64. Jinushi M, Takehara T, Tatsumi T, Kanto T, Groh V, Spies T et al. Autocrine/paracrine IL-15 that is required for type I IFN-mediated dendritic cell expression of MHC class I-related chain A and B is impaired in hepatitis C virus infection. J Immunol 2003; 171: 5423-5429.
65. Asselin-Paturel C, Brizard G, Chemin K, Boonstra A, O'Garra A, Vicari A et al. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J Exp Med 2005; 201: 1157-1167.
66. Paquette RL, Hsu N, Said J, Mohammed M, Rao NP, Shih G et al. Interferon-alpha induces dendritic cell differentiation of CML mononuclear cells in vitro and in vivo. Leukemia 2002; 16: 1484-1489.
67. + T cell response. J Immunol 2003; 170: 5195-5202.
68. Honda K, Sakaguchi S, Nakajima C, Watanabe A, Yanai H, Matsumoto M et al. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc Natl Acad Sci USA 2003; 100: 10872-10877.
69. Kadowaki N, Antonenko S, Lau JY, Liu YJ. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med 2000; 192: 219-226.
70. Hahm B, Trifilo MJ, Zuniga EI, Oldstone MB. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 2005; 22: 247-257.
71. Schlender J, Hornung V, Finke S, Gunthner-Biller M, Marozin S, Brzozka K et al. Inhibition of Toll-like receptor 7- and 9-mediated alpha/beta interferon production in human plasmacytoid dendritic cells by respiratory syncytial virus and measles virus. J Virol 2005; 79: 5507-5515.
72. Ramaswamy M, Shi L, Monick MM, Hunninghake GW, Look DC. Specific inhibition of type I interferon signal transduction by respiratory syncytial virus. Am J Respir Cell Mol Biol 2004; 30: 893-900.
73. Gautier G, Humbert M, Deauvieau F, Scuiller M, Hiscott J, Bates EE et al. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J Exp Med 2005; 201: 1435-1446.
74. Curtsinger JM, Lins DC, Mescher MF. Signal 3 determines tolerance versus full activation of naive CD8T cells: dissociating proliferation and development of effector function. J Exp Med 2003; 197: 1141-1151.
75. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med 1999; 189: 521-530.
76. Pilling D, Akbar AN, Girdlestone J, Orteu CH, Borthwick NJ, Amft N et al. Interferon-beta mediates stromal cell rescue of T cells from apoptosis. Eur J Immunol 1999; 29: 1041-1050.
77. + T cells stimulated by virus-induced type I interferon. Nat Immunol 2003; 4: 1009-1015.
78. + T cell response during cross-priming. J Immunol 2006; 176: 4682-4689.
79. Nguyen KB, Watford WT, Salomon R, Hofmann SR, Pien GC, Morinobu A et al. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 2002; 297: 2063-2066.
80. Pien GC, Nguyen KB, Malmgaard L, Satoskar AR, Biron CA. A unique mechanism for innate cytokine promotion of T cell responses to viral infections. J Immunol 2002; 169: 5827-5837.
81. Cousens LP, Peterson R, Hsu S, Dorner A, Altman JD, Ahmed R et al. Two roads diverged: interferon alpha/beta- and interleukin 12-mediated pathways in promoting T cell interferon gamma responses during viral infection. J Exp Med 1999; 189: 1315-1328.
82. + T cells during primary and secondary viral infections. J Immunol 2005; 174: 5936-5940.
83. Sun S, Zhang X, Tough DF, Sprent J. Type I interferon-mediated stimulation of T cells by CpG DNA. J Exp Med 1998; 188: 2335-2342.
84. Sun S, Zhang X, Tough D, Sprent J. Multiple effects of immunostimulatory DNA on T cells and the role of type I interferons. Springer Semin Immunopathol 2000; 22: 77-84.
85. Sprent J, Zhang X, Sun S, Tough D. T-cell proliferation in vivo and the role of cytokines. Philos Trans R Soc Lond B Biol Sci 2000; 355: 317-322.
86. Jiang J, Lau LL, Shen H. Selective depletion of nonspecific T cells during the early stage of immune responses to infection. J Immunol 2003; 171: 4352-4358.
87. McNally JM, Zarozinski CC, Lin MY, Brehm MA, Chen HD, Welsh RM. Attrition of bystander CD8 T cells during virus-induced T-cell and interferon responses. J Virol 2001; 75: 5965-5976.
88. Dunlop MB, Blanden RV. Mechanisms of suppression of cytotoxic T-cell responses in murine lymphocytic choriomeningitis virus infection. J Exp Med 1977; 145: 1131-1143.
89. Hanon E, Stinchcombe JC, Saito M, Asquith BE, Taylor GP, Tanaka Y et al. Fratricide among CD8(+) T lymphocytes naturally infected with human T cell lymphotropic virus type I. Immunity 2000; 13: 657-664.
90. Alsharifi M, Lobigs M, Simon MM, Kersten A, Muller K, Koskinen A et al. NK cell-mediated immunopathology during an acute viral infection of the CNS. Eur J Immunol 2006; 36: 887-896.
91. Bogdan C, Mattner J, Schleicher U. The role of type I interferons in non-viral infections. Immunol Rev 2004; 202: 33-48.
92. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998; 67: 227-264.
93. Le Bon A, Schiavoni G, D'Agostino G, Gresser I, Belardelli F, Tough DF. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 2001; 14: 461-470.
94. Demeure CE, Wu CY, Shu U, Schneider PV, Heusser C, Yssel H et al. In vitro maturation of human neonatal CD4 T lymphocytes. II. Cytokines present at priming modulate the development of lymphokine production. J Immunol 1994; 152: 4775-4782.
95. + T cells. J Exp Med 1993; 178: 1655-1663.
96. Sinigaglia F, D'Ambrosio D, Rogge L. Type I interferons and the Th1/Th2 paradigm. Dev Comp Immunol 1999; 23: 657-663.
97. Estes DM, Tuo W, Brown WC, Goin J. Effects of type I/type II interferons and transforming growth factor-beta on B-cell differentiation and proliferation. Definition of costimulation and cytokine requirements for immunoglobulin synthesis and expression. Immunology 1998; 95: 604-611.
98. Alsharifi M, Lobigs M, Regner M, Lee E, Koskinen A, Mullbacher A. Type-I interferons, in response to viral infection, trigger systemic, partial, lymphocyte activation. J Immunol 2005; 175: 4635-4640.
99. Braun D, Caramalho I, Demengeot J. IFN-alpha/beta enhances BCR-dependent B cell responses. Int Immunol 2002; 14: 411-419.
100. Tough DF, Borrow P, Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 1996; 272: 1947-1950.
101. Jeannin P, Herbault N, Delneste Y, Magistrelli G, Lecoanet-Henchoz S, Caron G et al. Human effector memory T cells express CD86: a functional role in naive T cell priming. J Immunol 1999; 162: 2044-2048.
102. Nakada M, Nishizaki K, Yoshino T, Okano M, Yamamoto T, Masuda Y et al. CD80 (B7-1) and CD86 (B7-2) antigens on house dust mite-specific T cells in atopic disease function through T-T cell interactions. J Allergy Clin Immunol 1999; 104: 222-227.
103. Hattori H, Okano M, Yoshino T, Akagi T, Nakayama E, Saito C et al. Expression of costimulatory CD80/CD86-CD28/CD152 molecules in nasal mucosa of patients with perennial allergic rhinitis. Clin Exp Allergy 2001; 31: 1242-1249.
104. + tumour-infiltrating lymphocytes (TIL) from patients with ovarian and other types of peritoneal carcinomatosis. Clin Exp Immunol 2000; 119: 19-27.
105. + regulatory T cells. Eur J Immunol 2002; 32: 2888-2896.
106. Takahashi T, Hirano N, Takahashi T, Chiba S, Yazaki Y, Hirai H. Immunogene therapy against mouse leukemia using B7 molecules. Cancer Gene Ther 2000; 7: 144-150.
107. Zheng Y, Manzotti CN, Liu M, Burke F, Mead KI, Sansom DM. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol 2004; 172: 2778-2784.
108. Testi R, D'Ambrosio D, De Maria R, Santoni A. The CD69 receptor: a multipurpose cell-surface trigger for hematopoietic cells. Immunol Today 1994; 15: 479-483.
109. Sancho D, Gomez M, Sanchez-Madrid F. CD69 is an immunoregulatory molecule induced following activation. Trends Immunol 2005; 26: 136-140.
110. Matloubian M, Lo CG, Cinamon G, Lesneski MJ, Xu Y, Brinkmann V et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 2004; 427: 355-360.
111. Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL et al. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 2006; 440: 540-544.
112. Lowenthal JW, Tougne C, MacDonald HR, Smith KA, Nabholz M. Antigenic stimulation regulates the expression of IL 2 receptors in a cytolytic T lymphocyte clone. J Immunol 1985; 134: 931-939.
113. Baechler EC, Gregersen PK, Behrens TW. The emerging role of interferon in human systemic lupus erythematosus. Curr Opin Immunol 2004; 16: 801-807.
114. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 2005; 202: 637-650.
115. Thompson LJ, Kolumam GA, Thomas S, Murali-Krishna K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J Immunol 2006; 177: 1746-1754.
116. Selin LK, Vergilis K, Welsh RM, Nahill SR. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J Exp Med 1996; 183: 2489-2499.
117. Selin LK, Lin MY, Kraemer KA, Pardoll DM, Schneck JP, Varga SM et al. Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 1999; 11: 733-742.
118. + T cells during reconstitution of lymphopenic environments. J Immunol 2003; 171: 655-663.
119. Tompkins MB, Nelson PD, English RV, Novotney C. Early events in the immunopathogenesis of feline retrovirus infections. J Am Vet Med Assoc 1991; 199: 1311-1315.
120. Alsharifi M, Regner M, Blanden R, Lobigs M, Lee E, Koskinen A et al. Exhaustion of type I interferon response following an acute viral infection. J Immunol 2006; 177: 3235-3241.
121. Carrero JA, Calderon B, Unanue ER. Listeriolysin O from Listeria monocytogenes is a lymphocyte apoptogenic molecule. J Immunol 2004; 172: 4866-4874.
122. Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, Smyth MJ et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 2004; 172: 123-129.
123. Della Chiesa M, Vitale M, Carlomagno S, Ferlazzo G, Moretta L, Moretta A. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 2003; 33: 1657-1666.
124. Bjorck P. Dendritic cells exposed to herpes simplex virus in vivo do not produce IFN-alpha after rechallenge with virus in vitro and exhibit decreased T cell alloreactivity. J Immunol 2004; 172: 5396-5404.
125. Andrews DM, Andoniou CE, Granucci F, Ricciardi-Castagnoli P, Degli-Esposti MA. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat Immunol 2001; 2: 1077-1084.