Immunity to respiratory viruses

Annual Review of Immunology

Volumn 27, Issue , 2009, Pages 61-82

  Kohlmeier, Jacob E ^a   Woodland, David L ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

Influenza; Lung; Memory; T cell

Indexed keywords

ALPHA INTERFERON; B7 ANTIGEN; BETA INTERFERON; BETA1 INTEGRIN; CD27 ANTIGEN; CD4 ANTIGEN; CD40 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M; LEUKOSIALIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TOLL LIKE RECEPTOR; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VIRUS RNA;

ADAPTIVE IMMUNITY; AIRWAY; ANTIBODY PRODUCTION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL HETEROGENEITY; CELL INTERACTION; CELL MIGRATION; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOLYSIS; DENDRITIC CELL; EFFECTOR CELL; ERYTHROCYTE; HUMAN; IMMUNOSURVEILLANCE; INFLAMMATION; INFLUENZA; INNATE IMMUNITY; INTERFERON PRODUCTION; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; LUNG PARENCHYMA; LYMPHATIC DRAINAGE; LYMPHOCYTE SUBPOPULATION; LYMPHOID TISSUE; MACROPHAGE; MEMORY T LYMPHOCYTE; MOLECULAR RECOGNITION; MONOCYTE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PARAINFLUENZA VIRUS INFECTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RESPIRATORY SYSTEM; RESPIRATORY TRACT INFECTION; RESPIRATORY VIRUS; REVIEW; T LYMPHOCYTE; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS TITRATION;

ANIMALS; B-LYMPHOCYTES; CYTOKINES; HUMANS; IMMUNITY, ACTIVE; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; LUNG; RECEPTORS, PATTERN RECOGNITION; RESPIRATORY TRACT INFECTIONS; T-LYMPHOCYTE SUBSETS; VIRUSES;

EID: 67149140627     PISSN: 07320582     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.immunol.021908.132625     Document Type: Review

References (141)

1. Horimoto T, Kawaoka Y. 2001. Pandemic threat posed by avian influenza A viruses. Clin. Microbiol. Rev. 14:129-49
2. Holt PG, Strickland DH, Wikstrom ME, Jahnsen FL. 2008. Regulation of immunological homeostasis in the respiratory tract. Nat. Rev. Immunol. 8:142-52
3. Iwasaki A, Medzhitov R. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5:987-95
4. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413:732-38
5. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303:1529-31
6. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, et al. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101:5598-603
7. Lund J, Sato A, Akira S, Medzhitov R, Iwasaki A. 2003. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198:513-20
8. Kurt-Jones EA, Popova L, Kwinn L, Haynes LM, Jones LP, et al. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1:398-401
9. Heil F, Ahmad-Nejad P, Hemmi H, Hochrein H, Ampenberger F, et al. 2003. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur. J. Immunol. 33:2987-97
10. Matsumoto M, Funami K, Tanabe M, Oshiumi H, Shingai M, et al. 2003. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 171:3154-62
11. Wang JP, Kurt-Jones EA, Finberg RW. 2007. Innate immunity to respiratory viruses. Cell. Microbiol. 9:1641-46
12. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. 2006. 5′-triphosphate RNA is the ligand for RIG-I. Science 314:994-97
13. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, et al. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314:997-1001
14. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-37
15. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. 2005. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23:19-28
16. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-5
17. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, et al. 2007. Cutting edge: Influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J. Immunol. 178:3368-72
18. Asselin-Paturel C, Boonstra A, Dalod M, Durand I, Yessaad N, et al. 2001. Mouse type I IFN-producing cells are immature APCs with plasmacytoid morphology. Nat. Immunol. 2:1144-50
19. Kumagai Y, Takeuchi O, Kato H, Kumar H, Matsui K, et al. 2007. Alveolar macrophages are the primary interferon-α producer in pulmonary infection with RNA viruses. Immunity 27:240-52
20. Pribul PK, Harker J, Wang B, Wang H, Tregoning JS, et al. 2008. Alveolar macrophages are a major determinant of early responses to viral lung infection but do not influence subsequent disease development. J. Virol. 82:4441-48
21. Pirhonen J, Sareneva T, Kurimoto M, Julkunen I, Matikainen S. 1999. Virus infection activates IL-1βand IL-18 production in human macrophages by a caspase-1-dependent pathway. J. Immunol. 162:7322-29
22. Chan MC, Cheung CY, Chui WH, Tsao SW, Nicholls JM, et al. 2005. Proinflammatory cytokine responses induced by influenza A (H5N1) viruses in primary human alveolar and bronchial epithelial cells. Respir. Res. 6:135
23. Piqueras B, Connolly J, Freitas H, Palucka AK, Banchereau J. 2006. Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107:2613-18
24. Herold S, von Wulffen W, Steinmueller M, Pleschka S, Kuziel WA, et al. 2006. Alveolar epithelial cells direct monocyte transepithelial migration upon influenza virus infection: impact of chemokines and adhesion molecules. J. Immunol. 177:1817-24
25. -/- mice. J. Leukoc. Biol. 81:793-801
26. Wareing MD, Shea AL, Inglis CA, Dias PB, Sarawar SR. 2007. CXCR2 is required for neutrophil recruitment to the lung during influenza virus infection, but is not essential for viral clearance. Viral Immunol. 20:369-78
27. Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, et al. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409:1055-60
28. Siren J, Sareneva T, Pirhonen J, Strengell M, Veckman V, et al. 2004. Cytokine and contact-dependent activation of natural killer cells by influenza A or Sendai virus-infected macrophages. J. Gen. Virol. 85:2357-64
29. He XS, Draghi M, Mahmood K, Holmes TH, Kemble GW, et al. 2004. T cell-dependent production of IFN-γ by NK cells in response to influenza A virus. J. Clin. Invest. 114:1812-19
30. Draghi M, Pashine A, Sanjanwala B, Gendzekhadze K, Cantoni C, et al. 2007. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J. Immunol. 178:2688-98
31. Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, et al. 2006. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7:517-23
32. Hintzen G, Ohl L, del Rio ML, Rodriguez-Barbosa JI, Pabst O, et al. 2006. Induction of tolerance to innocuous inhaled antigen relies on a CCR7-dependent dendritic cell-mediated antigen transport to the bronchial lymph node. J. Immunol. 177:7346-54
33. Legge KL, Braciale TJ. 2003. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18:265-77
34. Belz GT, Smith CM, Kleinert L, Reading P, Brooks A, et al. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101:8670-75
35. Diacovo TG, Blasius AL, Mak TW, Cella M, Colonna M. 2005. Adhesive mechanisms governing interferon-producing cell recruitment into lymph nodes. J. Exp. Med. 202:687-96
36. Grayson MH, Ramos MS, Rohlfing MM, Kitchens R, Wang HD, et al. 2007. Controls for lung dendritic cell maturation and migration during respiratory viral infection. J. Immunol. 179:1438-48
37. Zuercher AW, Coffin SE, Thurnheer MC, Fundova P, Cebra JJ. 2002. Nasal-associated lymphoid tissue is a mucosal inductive site for virus-specific humoral and cellular immune responses. J. Immunol. 168:1796-803
38. Rangel-Moreno J, Moyron-Quiroz J, Kusser K, Hartson L, Nakano H, Randall TD. 2005. Role of CXC chemokine ligand 13, CC chemokine ligand (CCL) 19, and CCL21 in the organization and function of nasal-associated lymphoid tissue. J. Immunol. 175:4904-13
39. Moyron-Quiroz JE, Rangel-Moreno J, Kusser K, Hartson L, Sprague F, et al. 2004. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10:927-34
40. Miller MJ, Wei SH, Parker I, Cahalan MD. 2002. Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296:1869-73
41. Stoll S, Delon J, Brotz TM, Germain RN. 2002. Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296:1873-76
42. + T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27:203-13
43. + T cell precursor frequency regulates primary and memory responses to infection. Immunity 28:859-69
44. Yager EJ, Ahmed M, Lanzer K, Randall TD, Woodland DL, Blackman MA. 2008. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205:711-23
45. Hugues S, Fetler L, Bonifaz L, Helft J, Amblard F, Amigorena S. 2004. Distinct T cell dynamics in lymph nodes during the induction of tolerance and immunity. Nat. Immunol. 5:1235-42
46. + T cell behavior in mucosal and systemic lymphoid tissues during the induction of oral priming and tolerance. J. Exp. Med. 201:1815-23
47. + T cells during pulmonary influenza virus infection. J. Immunol. 173:1209-18
48. + T cell effector population size. J. Immunol. 173:2923-27
49. Roman E, Miller E, Harmsen A, Wiley J, Von Andrian UH, et al. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196:957-68
50. + T cell responses through regulated FasL expression. Immunity 23:649-59
51. Sallusto F, Kremmer E, Palermo B, Hoy A, Ponath P, et al. 1999. Switch in chemokine receptor expression upon TCR stimulation reveals novel homing potential for recently activated T cells. Eur. J. Immunol. 29:2037-45
52. + memory T cells and their capacity for secondary expansion. J. Immunol. 175:1665-76
53. + T cell responses: correlation of cytokine profile and TCR avidity. J. Immunol. 172:5553-60
54. Schaller MA, Neupane R, Rudd BD, Kunkel SL, Kallal LE, et al. 2007. Notch ligand Delta-like 4 regulates disease pathogenesis during respiratory viral infections by modulating Th2 cytokines. J. Exp. Med. 204:2925-34
55. Constantin G, Majeed M, Giagulli C, Piccio L, Kim JY, et al. 2000. Chemokines trigger immediate β2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity 13:759-69
56. Thatte J, Dabak V, Williams MB, Braciale TJ, Ley K. 2003. LFA-1 is required for retention of effector CD8 T cells in mouse lungs. Blood 101:4916-22
57. Curtis JL, Sonstein J, Craig RA, Todt JC, Knibbs RN, et al. 2002. Subset-specific reductions in lung lymphocyte accumulation following intratracheal antigen challenge in endothelial selectin-deficient mice. J. Immunol. 169:2570-79
58. Clark JG, Mandac-Dy JB, Dixon AE, Madtes DK, Burkhart KM, et al. 2004. Trafficking of Th1 cells to lung: a role for selectins and a P-selectin glycoprotein-1-independent ligand. Am. J. Respir. Cell Mol. Biol. 30:220-27
59. Richter M, Ray SJ, Chapman TJ, Austin SJ, Rebhahn J, et al. 2007. Collagen distribution and expression of collagen-binding α1β1 (VLA-1) and α2β1 (VLA-2) integrins on CD4 and CD8 T cells during influenza infection. J. Immunol. 178:4506-16
60. Wareing MD, Lyon AB, Lu B, Gerard C, Sarawar SR. 2004. Chemokine expression during the development and resolution of a pulmonary leukocyte response to influenza A virus infection in mice. J. Leukoc. Biol. 76:886-95
61. Monick MM, Powers LS, Hassan I, Groskreutz D, Yarovinsky TO, et al. 2007. Respiratory syncytial virus synergizes with Th2 cytokines to induce optimal levels of TARC/CCL17. J. Immunol. 179:1648-58
62. + T cell-mediated inflammation in the central nervous system of virus-infected mice. J. Immunol. 175:1767-75
63. Galkina E, Thatte J, Dabak V, Williams MB, Ley K, Braciale TJ. 2005. Preferential migration of effector CD8 T cells into the interstitium of the normal lung. J. Clin. Invest. 115:3473-83
64. Thomas SY, Banerji A, Medoff BD, Lilly CM, Luster AD. 2007. Multiple chemokine receptors, including CCR6 and CXCR3, regulate antigen-induced T cell homing to the human asthmatic airway. J. Immunol. 179:1901-12
65. + T cell responses. J. Immunol. 176:1600-8
66. + T cells specific for influenza A virus M1 display broad expression of maturation-associated phenotypic markers and chemokine receptors. Immunology 115:239-45
67. Roberts AD, Ely KH, Woodland DL. 2005. Differential contributions of central and effector memory T cells to recall responses. J. Exp. Med. 202:123-33
68. + T cells in primary and secondary influenza pneumonia. Immunity 8:683-91
69. Carding SR, Allan W, McMickle A, Doherty PC. 1993. Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J. Exp. Med. 177:475-82
70. Mayer KD, Mohrs K, Crowe SR, Johnson LL, Rhyne P, et al. 2005. The functional heterogeneity of type 1 effector T cells in response to infection is related to the potential for IFN-γ production. J. Immunol. 174:7732-39
71. + T cells. J. Immunol. 173:721-25
72. + effector T cell responses in the lung allograft predominate over the blood during human primary infection. J. Immunol. 181:546-56
73. + T cells requires direct targeting to virus-infected epithelium. Eur. J. Immunol. 25:111-16
74. + T cells clear influenza virus by perforin or Fasdependent processes. J. Immunol. 159:5197-200
75. + T cells. J. Exp. Med. 174:875-80
76. + T cells. J. Immunol. 149:1319-25
77. Gerhard W. 2001. The role of the antibody response in influenza virus infection. Curr. Top. Microbiol. Immunol. 260:171-90
78. Graham MB, Braciale TJ. 1997. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med. 186:2063-68
79. Lee BO, Rangel-Moreno J, Moyron-Quiroz JE, Hartson L, Makris M, et al. 2005. CD4 T cell-independent antibody response promotes resolution of primary influenza infection and helps to prevent reinfection. J. Immunol. 175:5827-38
80. Baumgarth N, Herman OC, Jager GC, Brown LE, Herzenberg LA, Chen J. 2000. B-1 and B-2 cell-derived immunoglobulin M antibodies are nonredundant components of the protective response to influenza virus infection. J. Exp. Med. 192:271-80
81. Kopf M, Brombacher F, Bachmann MF. 2002. Role of IgM antibodies versus B cells in influenza virus-specific immunity. Eur. J. Immunol. 32:2229-36
82. Harada Y, Muramatsu M, Shibata T, Honjo T, Kuroda K. 2003. Unmutated immunoglobulin M can protect mice from death by influenza virus infection. J. Exp. Med. 197:1779-85
83. Palladino G, Mozdzanowska K, Washko G, Gerhard W. 1995. Virus-neutralizing antibodies of immunoglobulin G (IgG) but not of IgM or IgA isotypes can cure influenza virus pneumonia in SCID mice. J. Virol. 69:2075-81
84. Bishop GA, Hostager BS. 2001. B lymphocyte activation by contact-mediated interactions with T lymphocytes. Curr. Opin. Immunol. 13:278-85
85. + T cell-dependent immunoglobulin A response to influenza infection in the absence of key cognate T-B interactions. J. Exp. Med. 198:1011-21
86. + T cell contraction is controlled by early inflammation. Nat. Immunol. 5:809-17
87. + T-cell memory and prime-boost after dendritic-cell vaccination. Nat. Med. 11:748-56
88. McKinstry KK, Golech S, Lee WH, Huston G, Weng NP, Swain SL. 2007. Rapid default transition of CD4 T cell effectors to functional memory cells. J. Exp. Med. 204:2199-211
89. + T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-95
90. + T cells. Proc. Nat. Acad. Sci. USA 98:6313-18
91. + memory T cells in nonlymphoid tissues express a highly activated phenotype. J. Immunol. 169:6655-58
92. Masopust D, Vezys V, Usherwood EJ, Cauley LS, Olson S, et al. 2004. Activated primary and memory CD8 T cells migrate to nonlymphoid tissues regardless of site of activation or tissue of origin. J. Immunol. 172:4875-82
93. + T cells specific for respiratory viruses in the human lung. J. Exp. Med. 202:1433-42
94. + T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166:1813-22
95. Liang S, Mozdzanowska K, Palladino G, Gerhard W. 1994. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152:1653-61
96. Jelley-Gibbs DM, Brown DM, Dibble JP, Haynes L, Eaton SM, Swain SL. 2005. Unexpected prolonged presentation of influenza antigens promotes CD4 T cell memory generation. J. Exp. Med. 202:697-706
97. Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. 2006. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24:439-49
98. + T cells. Proc. Natl. Acad. Sci. USA 101:6116-21
99. + T cells in the lung airways. J. Immunol. 178:4721-25
100. Ely KH, Cookenham T, Roberts AD, Woodland DL. 2006. Memory T cell populations in the lung airways are maintained by continual recruitment. J. Immunol. 176:537-43
101. Sallusto F, Lenig D, Forster R, Lipp M, Lanzavecchia A. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401:708-12
102. Masopust D, Vezys V, Marzo AL, Lefrancois L. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291:2413-17
103. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, et al. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 3:225-34
104. + T cells. Immunity 22:259-70
105. Becker TC, Coley SM, Wherry EJ, Ahmed R. 2005. Bone marrow is a preferred site for homeostatic proliferation of memory CD8 T cells. J. Immunol. 174:1269-73
106. + T cell lineage commitment. Nat. Immunol. 6:793-99
107. Moulton VR, Bushar ND, Leeser DB, Patke DS, Farber DL. 2006. Divergent generation of heterogeneous memory CD4 T cells. J. Immunol. 177:869-76
108. Bachmann MF, Kundig TM, Odermatt B, Hengartner H, Zinkernagel RM. 1994. Free recirculation of memory B cells versus antigen-dependent differentiation to antibody-forming cells. J. Immunol. 153:3386-97
109. Slifka MK, Antia R, Whitmire JK, Ahmed R. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8:363-72
110. Noelle RJ, Roy M, Shepherd DM, Stamenkovic I, Ledbetter JA, Aruffo A. 1992. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl. Acad. Sci. USA 89:6550-54
111. Lee BO, Moyron-Quiroz J, Rangel-Moreno J, Kusser KL, Hartson L, et al. 2003. CD40, but not CD154, expression on B cells is necessary for optimal primary B cell responses. J. Immunol. 171:5707-17
112. Galli G, Pittoni P, Tonti E, Malzone C, Uematsu Y, et al. 2007. Invariant NKT cells sustain specific B cell responses and memory. Proc. Nat. Acad. Sci. USA 104:3984-89
113. Liang B, Hyland L, Hou S. 2001. Nasal-associated lymphoid tissue is a site of long-term virus-specific antibody production following respiratory virus infection of mice. J. Virol. 75:5416-20
114. Joo HM, He Y, Sangster MY. 2008. Broad dispersion and lung localization of virus-specific memory B cells induced by influenza pneumonia. Proc. Nat. Acad. Sci. USA 105:3485-90
115. Stamboulian D, Bonvehi PE, Nacinovich FM, Cox N. 2000. Influenza. Infect. Dis. Clin. N. Am. 14:141-66
116. Rangel-Moreno J, Carragher DM, Misra RS, Kusser K, Hartson L, et al. 2008. B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J. Immunol. 180:454-63
117. Goulding J, Snelgrove R, Saldana J, Didierlaurent A, Cavanagh M, et al. 2007. Respiratory infections: Do we ever recover? Proc. Am. Thorac. Soc. 4:618-25
118. Kim EY, Battaile JT, Patel AC, You Y, Agapov E, et al. 2008. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat. Med. 14:633-40
119. Moyron-Quiroz JE, Rangel-Moreno J, Hartson L, Kusser K, Tighe MP, et al. 2006. Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 25:643-54
120. Walzl G, Tafuro S, Moss P, Openshaw PJ, Hussell T. 2000. Influenza virus lung infection protects from respiratory syncytial virus-induced immunopathology. J. Exp. Med. 192:1317-26
121. Chen HD, Fraire AE, Joris I, Welsh RM, Selin LK. 2003. Specific history of heterologous virus infections determines antiviral immunity and immunopathology in the lung. Am. J. Pathol. 163:1341-55
122. Williams AE, Edwards L, Humphreys IR, Snelgrove R, Rae A, et al. 2004. Innate imprinting by the modified heat-labile toxin of Escherichia coli (LTK63) provides generic protection against lung infectious disease. J. Immunol. 173:7435-43
123. Cerwenka A, Morgan TM, Dutton RW. 1999. Naive, effector, and memory CD8 T cells in protection against pulmonary influenza virus infection: homing properties rather than initial frequencies are crucial. J. Immunol. 163:5535-43
124. + T cells that persist in the lungs. J. Exp. Med. 193:981-86
125. Ostler T, Hussell T, Surh CD, Openshaw P, Ehl S. 2001. Long-term persistence and reactivation of T cell memory in the lung of mice infected with respiratory syncytial virus. Eur. J. Immunol. 31:2574-82
126. + T cells persist in the upper respiratory tract following influenza virus infection. J. Immunol. 167:3293-99
127. Vallbracht S, Unsold H, Ehl S. 2006. Functional impairment of cytotoxic T cells in the lung airways following respiratory virus infections. Eur. J. Immunol. 36:1434-42
128. + T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2:1067-76
129. + T cells to the lung during influenza pneumonia. J. Immunol. 167:6983-90
130. + T cells to the lung airways during respiratory virus infections. J. Immunol. 170:1423-29
131. + T cell response to respiratory virus infections. Immunity 29:101-13
132. + effector and memory T cell generation. Nat. Immunol. 4:835-42
133. Hammarlund E, Lewis MW, Hansen SG, Strelow LI, Nelson JA, et al. 2003. Duration of antiviral immunity after smallpox vaccination. Nat. Med. 9:1131-37
134. Zammit DJ, Cauley LS, Pham QM, Lefrancois L. 2005. Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22:561-70
135. Castiglioni P, Hall de S, Jacovetty EL, Ingulli E, Zanetti M. 2008. Protection against influenza A virus by memory CD8 T cells requires reactivation by bone marrow-derived dendritic cells. J. Immunol. 180:4956-64
136. + T cells play a prominent role in recall responses to secondary viral infection in the lung. J. Immunol. 172:6533-37
137. + central memory T cells in protection from simian AIDS. J. Immunol. 175:3502-7
138. + T cells and antiviral protection. J. Immunol. 175:4677-85
139. Stock AT, Jones CM, Heath WR, Carbone FR. 2006. Cutting edge: central memory T cells do not show accelerated proliferation or tissue infiltration in response to localized herpes simplex virus-1 infection. J. Immunol. 177:1411-15
140. Klonowski KD, Marzo AL, Williams KJ, Lee SJ, Pham QM, Lefrancois L. 2006. CD8 T cell recall responses are regulated by the tissue tropism of the memory cell and pathogen. J. Immunol. 177:6738-46
141. + T cells. J. Exp. Med. 204:1625-36