본문 바로가기
KERD
논문KCI 등재

The Multifaceted Roles of NK Cells in the Context of Murine Cytomegalovirus and Lymphocytic Choriomeningitis Virus Infections

2

조회

0

다운로드

0

인용

0

참고문헌

키워드

초록

NK cells belong to innate lymphoid cells and able to eliminate infected cells and tumor cells. NK cells play a valuable role in controlling viral infections. Also, they have the potential to shape the adaptive immunity via a unique crosstalk with the different immune cells. Murine models are important tools for delineating the immunological phenomena in viral infection. To decipher the immunological virus-host interactions, two major infection models are being investigated in mice regarding NK cell-mediated recognition: murine cytomegalovirus (MCMV) and lymphocytic choriomeningitis virus (LCMV). In this review, we recapitulate recent findings regarding the multifaceted role of NK cells in controlling LCMV and MCMV infections and outline the exquisite interplay between NK cells and other immune cells in these two settings. Considering that, infections with MCMV and LCMV recapitulates many physiopathological characteristics of human cytomegalovirus infection and chronic virus infections respectively, this study will extend our understanding of NK cells biology in interactions between the virus and its natural host.

Abstract

NK cells belong to innate lymphoid cells and able to eliminate infected cells and tumor cells. NK cells play a valuable role in controlling viral infections. Also, they have the potential to shape the adaptive immunity via a unique crosstalk with the different immune cells. Murine models are important tools for delineating the immunological phenomena in viral infection. To decipher the immunological virus-host interactions, two major infection models are being investigated in mice regarding NK cell-mediated recognition: murine cytomegalovirus (MCMV) and lymphocytic choriomeningitis virus (LCMV). In this review, we recapitulate recent findings regarding the multifaceted role of NK cells in controlling LCMV and MCMV infections and outline the exquisite interplay between NK cells and other immune cells in these two settings. Considering that, infections with MCMV and LCMV recapitulates many physiopathological characteristics of human cytomegalovirus infection and chronic virus infections respectively, this study will extend our understanding of NK cells biology in interactions between the virus and its natural host.

참고문헌 (163)

  1. Vivier E, "Functions of natural killer cells", Nat Immunol, 9, pp.503~510 (2008)
  2. Min-Oo G, "Natural killer cells : walking three paths down memory lane", Trends Immunol, 34, pp.251~258 (2013)
  3. Hammer Q, "Natural killer cell specificity for viral infections", Nat Immunol, 19, pp.800~808 (2018)
  4. Biron CA, "Natural killer cells in antiviral defense : function and regulation by innate cytokines", Annu Rev Immunol, 17, pp.189~220 (1999)
  5. Sandu I, "T-cell heterogeneity, progenitor-progeny relationships, and function during latent and chronic viral infections", Immunol Rev, 316, pp.136~159 (2023)
  6. Agnellini P, "Impaired NFAT nuclear translocation results in split exhaustion of virus-specific CD8+ T cell functions during chronic viral infection", Proc Natl Acad Sci U S A, 104, pp.4565~4570 (2007)
  7. Mueller SN, "High antigen levels are the cause of T cell exhaustion during chronic viral infection", Proc Natl Acad Sci U S A, 106, pp.8623~8628 (2009)
  8. Goodier MR, "CMV and natural killer cells : shaping the response to vaccination", Eur J Immunol, 48, pp.50~65 (2018)
  9. Krmpotic A, "Pathogenesis of murine cytomegalovirus infection", Microbes Infect, 5, pp.1263~1277 (2003)
  10. Mitrović M, "The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8(+)T-cell response", J Virol, 86, pp.2165~2175 (2012)
  11. Zangger N, "CD4 T cell-mediated immune control of cytomegalovirus infection in murine salivary glands", Pathogens, 10, pp.1531~ (2021)
  12. Studstill CJ, "Chronic LCMV infection is fortified with versatile tactics to suppress host t cell immunity and establish viral persistence", Viruses, 13, pp.1951~ (2021)
  13. Caron L, "Armstrong strain lymphocytic choriomeningitis virus infection after accidental laboratory exposure", Virol J, 20, pp.294~ (2023)
  14. Welsh RM, "NK cells controlling virus-specific T cells : Rheostats for acute vs. persistent infections", Virology, 435, pp.37~45 (2013)
  15. Gatherer D, "ICTV virus taxonomy profile : Herpesviridae 2021", J Gen Virol, 102, pp.001673~ (2021)
  16. Hudson JB, "The murine cytomegalovirus as a model for the study of viral pathogenesis and persistent infections", Arch Virol, 62, pp.1~29 (1979)
  17. Tang Q, "Mouse cytomegalovirus crosses the species barrier with help from a few human cytomegalovirus proteins", J Virol, 80, pp.7510~7521 (2006)
  18. Brune W, "A mouse model for cytomegalovirus infection", Curr Protoc Immunol, Chapter 19, pp.Unit 19.7~ (2001)
  19. Rawlinson WD, "Analysis of the complete DNA sequence of murine cytomegalovirus", J Virol, 70, pp.8833~8849 (1996)
  20. Sitnik KM, "Fibroblasts are a site of murine cytomegalovirus lytic replication and Stat1-dependent latent persistence in vivo", Nat Commun, 14, pp.3087~ (2023)
  21. McNab F, "Type I interferons in infectious disease", Nat Rev Immunol, 15, pp.87~103 (2015)
  22. Presti RM, "Interferon gamma regulates acute and latent murine cytomegalovirus infection and chronic disease of the great vessels", J Exp Med, 188, pp.577~588 (1998)
  23. Gil MP, "Biologic consequences of Stat1-independent IFN signaling", Proc Natl Acad Sci U S A, 98, pp.6680~6685 (2001)
  24. Hoffmann HH, "Interferons and viruses : an evolutionary arms race of molecular interactions", Trends Immunol, 36, pp.124~138 (2015)
  25. Lazear HM, "Interferon-λ : immune functions at barrier surfaces and beyond", Immunity, 43, pp.15~28 (2015)
  26. Billiau A, "Interferon-gamma : a historical perspective", Cytokine Growth Factor Rev, 20, pp.97~113 (2009)
  27. McKenzie AN, "Innate lymphoid cells in inflammation and immunity", Immunity, 41, pp.366~374 (2014)
  28. Schroder K, "Interferon-gamma : an overview of signals, mechanisms and functions", J Leukoc Biol, 75, pp.163~189 (2004)
  29. Kang S, "Direct antiviral mechanisms of interferon-gamma", Immune Netw, 18, pp.e33~ (2018)
  30. Kropp KA, "Reversible inhibition of murine cytomegalovirus replication by gamma interferon(IFN-γ)in primary macrophages involves a primed type I IFN-signaling subnetwork for full establishment of an immediate-early antiviral state", J Virol, 85, pp.10286~10299 (2011)
  31. Heise MT, "The T-cell-independent role of gamma interferon and tumor necrosis factor alpha in macrophage activation during murine cytomegalovirus and herpes simplex virus infections", J Virol, 69, pp.904~909 (1995)
  32. Gribaudo G, "Interferons inhibit onset of murine cytomegalovirus immediate-early gene transcription", Virology, 197, pp.303~311 (1993)
  33. Lucin P, "Late phase inhibition of murine cytomegalovirus replication by synergistic action of interferon-gamma and tumour necrosis factor", J Gen Virol, 75, pp.101~110 (1994)
  34. Senik A, "Enhancement of mouse natural killer cell activity by type II interferon", Ann Immunol (Paris), 131C, pp.349~361 (1980)
  35. Nathan CF, "Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity", J Exp Med, 158, pp.670~689 (1983)
  36. Leibson HJ, "Role of gamma-interferon in antibody-producing responses", Nature, 309, pp.799~801 (1984)
  37. Gajewski TF, "Anti-proliferative effect of IFN-gamma in immune regulation. I. IFN-gamma inhibits the proliferation of Th2 but not Th1 murine helper T lymphocyte clones", J Immunol, 140, pp.4245~4252 (1988)
  38. Hengel H, "Restoration of cytomegalovirus antigen presentation by gamma interferon combats viral escape", J Virol, 68, pp.289~297 (1994)
  39. Brown MG, "Vital involvement of a natural killer cell activation receptor in resistance to viral infection", Science, 292, pp.934~937 (2001)
  40. Scalzo AA, "The interplay between host and viral factors in shaping the outcome of cytomegalovirus infection", Immunol Cell Biol, 85, pp.46~54 (2007)
  41. Lee SH, "Keeping NK cells in highly regulated antiviral warfare", Trends Immunol, 28, pp.252~259 (2007)
  42. Arase H, "Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors", Science, 296, pp.1323~1326 (2002)
  43. Bubić I, "Gain of virulence caused by loss of a gene in murine cytomegalovirus", J Virol, 78, pp.7536~7544 (2004)
  44. Lanier LL, "DAP10-and DAP12-associated receptors in innate immunity", Immunol Rev, 227, pp.150~160 (2009)
  45. Nabekura T, "Antigen-specific expansion and differentiation of natural killer cells by alloantigen stimulation", J Exp Med, 211, pp.2455~2465 (2014)
  46. Orr MT, "Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection", J Exp Med, 206, pp.807~817 (2009)
  47. Sun JC, "Adaptive immune features of natural killer cells", Nature, 457, pp.557~561 (2009)
  48. Dokun AO, "Specific and nonspecific NK cell activation during virus infection", Nat Immunol, 2, pp.951~956 (2001)
  49. Terrén I, "Cytokine-induced memory-like NK cells : from the basics to clinical applications", Front Immunol, 13, pp.884648~ (2022)
  50. Sun JC, "Cutting edge : IL-15-independent NK cell response to mouse cytomegalovirus infection", J Immunol, 183, pp.2911~2914 (2009)
  51. Trinchieri G, "Interleukin-12 and the regulation of innate resistance and adaptive immunity", Nat Rev Immunol, 3, pp.133~146 (2003)
  52. Sun JC, "Proinflammatory cytokine signaling required for the generation of natural killer cell memory", J Exp Med, 209, pp.947~954 (2012)
  53. Zeleznjak J, "Mouse cytomegalovirus encoded immunoevasins and evolution of Ly49 receptors-sidekicks or enemies?", Immunol Lett, 189, pp.40~47 (2017)
  54. Corbett AJ, "Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation", J Immunol, 186, pp.1713~1722 (2011)
  55. Robbins SH, "Natural killer cells promote early CD8 T cell responses against cytomegalovirus", PLoS Pathog, 3, pp.e123~ (2007)
  56. Asselin-Paturel C, "Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody", J Immunol, 171, pp.6466~6477 (2003)
  57. Shibuya A, "DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes", Immunity, 4, pp.573~581 (1996)
  58. Nabekura T, "Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection", Immunity, 40, pp.225~234 (2014)
  59. Wu J, "An activating immunoreceptor complex formed by NKG2D and DAP10", Science, 285, pp.730~732 (1999)
  60. Champsaur M, "Effect of NKG2D ligand expression on host immune responses", Immunol Rev, 235, pp.267~285 (2010)
  61. Jamieson AM, "The role of the NKG2D immunoreceptor in immune cell activation and natural killing", Immunity, 17, pp.19~29 (2002)
  62. Raulet DH, "Roles of the NKG2D immunoreceptor and its ligands", Nat Rev Immunol, 3, pp.781~790 (2003)
  63. Diefenbach A, "Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D", Nat Immunol, 3, pp.1142~1149 (2002)
  64. Gilfillan S, "NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation", Nat Immunol, 3, pp.1150~1155 (2002)
  65. Billadeau DD, "NKG2D-DAP10 triggers human NK cell-mediated killing via a Syk-independent regulatory pathway", Nat Immunol, 4, pp.557~564 (2003)
  66. Zompi S, "NKG2D triggers cytotoxicity in mouse NK cells lacking DAP12 or Syk family kinases", Nat Immunol, 4, pp.565~572 (2003)
  67. Nabekura T, "Cutting edge : NKG2D signaling enhances NK cell responses but alone is insufficient to drive expansion during mouse cytomegalovirus infection", J Immunol, 199, pp.1567~1571 (2017)
  68. Zafirova B, "Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice", Immunity, 31, pp.270~282 (2009)
  69. French AR, "DAP12 signaling directly augments proproliferative cytokine stimulation of NK cells during viral infections", J Immunol, 177, pp.4981~4990 (2006)
  70. Ho EL, "Costimulation of multiple NK cell activation receptors by NKG2D", J Immunol, 169, pp.3667~3675 (2002)
  71. Jelenčić V, "NK cell receptor NKG2D sets activation threshold for the NCR1 receptor early in NK cell development", Nat Immunol, 19, pp.1083~1092 (2018)
  72. Khan AU, "The TNFα", TNFR2 axis mediates natural killer cell proliferation by promoting aerobic glycolysis, 2023, pp.20, 1140~1155
  73. Huntington ND, "Ironman training for NK cells", Nat Immunol, 24, pp.1599~1601 (2023)
  74. Sheppard S, "The murine natural cytotoxic receptor NKp46", NCR1 controls TRAIL protein expression in NK cells and ILC1s, 2018, pp.22, 3385~3392
  75. Pessino A, "Molecular cloning of NKp46 : a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity", J Exp Med, 188, pp.953~960 (1998)
  76. Biassoni R, "The murine homologue of the human NKp46, a triggering receptor involved in the induction of natural cytotoxicity", Eur J Immunol, 29, pp.1014~1020 (1999)
  77. Narni-Mancinelli E, "Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses", Science, 335, pp.344~348 (2012)
  78. Walton SM, "Absence of cross-presenting cells in the salivary gland and viral immune evasion confine cytomegalovirus immune control to effector CD4 T cells", PLoS Pathog, 7, pp.e1002214~ (2011)
  79. Campbell AE, "The salivary glands as a privileged site of cytomegalovirus immune evasion and persistence", Med Microbiol Immunol(Berl), 197, pp.205~213 (2008)
  80. Nabekura T, "IL-33 receptor ST2 amplifies the expansion of NK cells and enhances host defense during mouse cytomegalovirus infection", J Immunol, 194, pp.5948~5952 (2015)
  81. Madera S, "Cutting edge : stage-specific requirement of IL-18 for antiviral NK cell expansion", J Immunol, 194, pp.1408~1412 (2015)
  82. French AR, "Natural killer cells and viral infections", Curr Opin Immunol, 15, pp.45~51 (2003)
  83. Hangartner L, "Antiviral antibody responses : the two extremes of a wide spectrum", Nat Rev Immunol, 6, pp.231~243 (2006)
  84. Bukowski JF, "Pathogenesis of murine cytomegalovirus infection in natural killer cell-depleted mice", J Virol, 52, pp.119~128 (1984)
  85. Halenius A, "Classical and non-classical MHC I molecule manipulation by human cytomegalovirus : so many targets—but how many arrows in the quiver?", Cell Mol Immunol, 12, pp.139~153 (2015)
  86. Lisnić B, "NK cell interplay with cytomegaloviruses", Curr Opin Virol, 15, pp.9~18 (2015)
  87. Babić M, "Cytomegalovirus immunoevasin reveals the physiological role of"missing self"recognition in natural killer cell dependent virus control in vivo", J Exp Med, 207, pp.2663~2673 (2010)
  88. Kavanagh DG, "The multiple immune-evasion genes of murine cytomegalovirus are not redundant : m4 and m152 inhibit antigen presentation in a complementary and cooperative fashion", J Exp Med, 194, pp.967~978 (2001)
  89. Arapović J, "Promiscuity of MCMV immunoevasin of NKG2D : m138", fcr-1 down-modulates RAE-1epsilon in addition to MULT-1 and H60, 2009, pp.47, 114~122
  90. Lis N, "The murine cytomegalovirus immunoevasin gp40", m152 inhibits NKG2D receptor RAE-1γ by intracellular retention and cell surface masking, 2021, pp.134, jcs257428~
  91. Jonjić S, "Immune evasion of natural killer cells by viruses", Curr Opin Immunol, 20, pp.30~38 (2008)
  92. Arnon TI, "Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus", Nat Immunol, 6, pp.515~523 (2005)
  93. Sylwester AW, "Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects", J Exp Med, 202, pp.673~685 (2005)
  94. Blees A, "Structure of the human MHC-I peptide-loading complex", Nature, 551, pp.525~528 (2017)
  95. Manandhar T, "Battle between host immune cellular responses and HCMV immune evasion", Int J Mol Sci, 20, pp.3626~ (2019)
  96. Biron CA, "Severe herpesvirus infections in an adolescent without natural killer cells", N Engl J Med, 320, pp.1731~1735 (1989)
  97. Orange JS, "Natural killer cell deficiency", J Allergy Clin Immunol, 132, pp.515~525 (2013)
  98. Oldstone MB, "Virus and immune responses : lymphocytic choriomeningitis virus as a prototype model of viral pathogenesis", Br Med Bull, 41, pp.70~74 (1985)
  99. Bonthius DJ, "Lymphocytic choriomeningitis virus : an underrecognized cause of neurologic disease in the fetus, child, and adult", Semin Pediatr Neurol, 19, pp.89~95 (2012)
  100. Biggar RJ, "Lymphocytic choriomeningitis outbreak associated with pet hamsters. Fifty-seven cases from New York State", JAMA, 232, pp.494~500 (1975)
  101. Zhou X, "Role of lymphocytic choriomeningitis virus(LCMV)in understanding viral immunology : past, present and future", Viruses, 4, pp.2650~2669 (2012)
  102. Welsh RM, "Lymphocytic choriomeningitis virus(LCMV) : propagation, quantitation, and storage", Curr Protoc Microbiol, Chapter 15, pp.Unit 15A.1~ (2008)
  103. Emonet SF, "Arenavirus genetic diversity and its biological implications", Infect Genet Evol, 9, pp.417~429 (2009)
  104. Lee KJ, "NP and L proteins of lymphocytic choriomeningitis virus(LCMV)are sufficient for efficient transcription and replication of LCMV genomic RNA analogs", J Virol, 74, pp.3470~3477 (2000)
  105. Vilibic-Cavlek T, "Lymphocytic choriomeningitis-emerging trends of a neglected virus : a narrative review", Trop Med Infect Dis, 6, pp.88~ (2021)
  106. Norris BA, "Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity", Immunity, 38, pp.309~321 (2013)
  107. Cao W, "Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus", Science, 282, pp.2079~2081 (1998)
  108. Meyer BJ, "Arenaviruses : genomic RNAs, transcription, and replication", Curr Top Microbiol Immunol, 262, pp.139~157 (2002)
  109. Takagi T, "Genomic analysis and pathogenic characteristics of lymphocytic choriomeningitis virus strains isolated in Japan", Comp Med, 62, pp.185~192 (2012)
  110. Dangi T, "Interrogating adaptive immunity using LCMV", Curr Protoc Immunol, 130, pp.e99~ (2020)
  111. Sevilla N, "Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells", J Exp Med, 192, pp.1249~1260 (2000)
  112. Cook KD, "NK cells and their ability to modulate T cells during virus infections", Crit Rev Immunol, 34, pp.359~388 (2014)
  113. Mempel TR, "T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases", Nature, 427, pp.154~159 (2004)
  114. Walzer T, "Natural-killer cells and dendritic cells : "l’union fait la force"", Blood, 106, pp.2252~2258 (2005)
  115. Sivori S, "CpG and double-stranded RNA trigger human NK cells by Toll-like receptors : induction of cytokine release and cytotoxicity against tumors and dendritic cells", Proc Natl Acad Sci U S A, 101, pp.10116~10121 (2004)
  116. Biron CA, "Innate immune responses to LCMV infections : natural killer cells and cytokines", Curr Top Microbiol Immunol, 263, pp.7~27 (2002)
  117. Vivier E, "Natural killer cell signaling pathways", Science, 306, pp.1517~1519 (2004)
  118. Bukowski JF, "Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo", J Immunol, 131, pp.1531~1538 (1983)
  119. Welsh RM, "Antiviral activity of NK 1. 1+ natural killer cells in C57BL", 6 scid mice infected with murine cytomegalovirus, 1994, pp.13, 239~245
  120. Waggoner SN, "Roles of natural killer cells in antiviral immunity", Curr Opin Virol, 16, pp.15~23 (2016)
  121. Zhou J, "Liver-resident NK cells control antiviral activity of hepatic T cells via the PD-1-PD-L1 axis", Immunity, 50, pp.403~417 (2019)
  122. Lang PA, "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, pp.1210~1215 (2012)
  123. Hamdan TA, "The diverse functions of the ubiquitous Fcγ receptors and their unique constituent, FcRγ subunit", Pathogens, 9, pp.140~ (2020)
  124. Duhan V, "NK cell-intrinsic FcεRIγ limits CD8+ T-cell expansion and thereby turns an acute into a chronic viral infection", PLoS Pathog, 15, pp.e1007797~ (2019)
  125. Pallmer K, "NK cells negatively regulate CD8 T cells via natural cytotoxicity receptor(NCR)1 during LCMV infection", PLoS Pathog, 15, pp.e1007725~ (2019)
  126. Waggoner SN, "Natural killer cells act as rheostats modulating antiviral T cells", Nature, 481, pp.394~398 (2011)
  127. Waggoner SN, "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, pp.1925~1938 (2010)
  128. Cook KD, "The depletion of NK cells prevents T cell exhaustion to efficiently control disseminating virus infection", J Immunol, 190, pp.641~649 (2013)
  129. Cook KD, "NK cells inhibit humoral immunity by reducing the abundance of CD4+ T follicular helper cells during a chronic virus infection", J Leukoc Biol, 98, pp.153~162 (2015)
  130. Mack EA, "Type 1 interferon induction of natural killer cell gamma interferon production for defense during lymphocytic choriomeningitis virus infection", MBio, 2, pp.e00169-11~ (2011)
  131. Madera S, "Type I IFN promotes NK cell expansion during viral infection by protecting NK cells against fratricide", J Exp Med, 213, pp.225~233 (2016)
  132. Crouse J, "Type I interferons protect T cells against NK cell attack mediated by the activating receptor NCR1", Immunity, 40, pp.961~973 (2014)
  133. Xu HC, "Type I interferon protects antiviral CD8+ T cells from NK cell cytotoxicity", Immunity, 40, pp.949~960 (2014)
  134. Huang Z, "IFNAR1 signaling in NK cells promotes persistent virus infection", Sci Adv, 7, pp.eabb8087~ (2021)
  135. Rydyznski C, "Generation of cellular immune memory and B-cell immunity is impaired by natural killer cells", Nat Commun, 6, pp.6375~ (2015)
  136. Cardoso Alves L, "Non-apoptotic TRAIL function modulates NK cell activity during viral infection", EMBO Rep, 21, pp.e48789~ (2020)
  137. Pratumchai I, "B cell-derived IL-27 promotes control of persistent LCMV infection", Proc Natl Acad Sci U S A, 119, pp.e2116741119~ (2022)
  138. Butz EA, "Massive expansion of antigen-specific CD8+ T cells during an acute virus infection", Immunity, 8, pp.167~175 (1998)
  139. Wherry EJ, "Lineage relationship and protective immunity of memory CD8 T cell subsets", Nat Immunol, 4, pp.225~234 (2003)
  140. Wherry EJ, "Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment", J Virol, 77, pp.4911~4927 (2003)
  141. Cornberg M, "Clonal exhaustion as a mechanism to protect against severe immunopathology and death from an overwhelming CD8 T cell response", Front Immunol, 4, pp.475~ (2013)
  142. Moskophidis D, "Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells", Nature, 362, pp.758~761 (1993)
  143. Wherry EJ, "T cell exhaustion", Nat Immunol, 12, pp.492~499 (2011)
  144. Lee SH, "Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection", J Exp Med, 206, pp.2235~2251 (2009)
  145. Su HC, "IL-2-dependent NK cell responses discovered in virus-infected beta 2-microglobulin-deficient mice", J Immunol, 153, pp.5674~5681 (1994)
  146. Whitmire JK, "Direct interferon-gamma signaling dramatically enhances CD4+ and CD8+ T cell memory", J Immunol, 179, pp.1190~1197 (2007)
  147. Whitmire JK, "Interferon-gamma acts directly on CD8+ T cells to increase their abundance during virus infection", J Exp Med, 201, pp.1053~1059 (2005)
  148. Whitmire JK, "Cutting edge : early IFN-gamma signaling directly enhances primary antiviral CD4+ T cell responses", J Immunol, 175, pp.5624~5628 (2005)
  149. Gerosa F, "Reciprocal activating interaction between natural killer cells and dendritic cells", J Exp Med, 195, pp.327~333 (2002)
  150. Mocikat R, "Natural killer cells activated by MHC class I(low)targets prime dendritic cells to induce protective CD8 T cell responses", Immunity, 19, pp.561~569 (2003)
  151. Adam C, "DC-NK cell cross talk as a novel CD4+ T-cell-independent pathway for antitumor CTL induction", Blood, 106, pp.338~344 (2005)
  152. Andrews DM, "Infection of dendritic cells by murine cytomegalovirus induces functional paralysis", Nat Immunol, 2, pp.1077~1084 (2001)
  153. Andrews DM, "Innate immunity defines the capacity of antiviral T cells to limit persistent infection", J Exp Med, 207, pp.1333~1343 (2010)
  154. Lee SH, "Cutting edge : a novel mechanism bridging innate and adaptive immunity : IL-12 induction of CD25 to form high-affinity IL-2 receptors on NK cells", J Immunol, 189, pp.2712~2716 (2012)
  155. Su HC, "NK cell functions restrain T cell responses during viral infections", Eur J Immunol, 31, pp.3048~3055 (2001)
  156. Chambers BJ, "Triggering of natural killer cells by the costimulatory molecule CD80(B7-1)", Immunity, 5, pp.311~317 (1996)
  157. Carbone E, "Recognition of autologous dendritic cells by human NK cells", Eur J Immunol, 29, pp.4022~4029 (1999)
  158. Schuster IS, "TRAIL+ NK cells control CD4+ T cell responses during chronic viral infection to limit autoimmunity", Immunity, 41, pp.646~656 (2014)
  159. Crouse J, "NK cells regulating T cell responses : mechanisms and outcome", Trends Immunol, 36, pp.49~58 (2015)
  160. Rabinovich BA, "Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells", J Immunol, 170, pp.3572~3576 (2003)
  161. Cerboni C, "Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM", ATR-dependent mechanism and become susceptible to autologous NK-cell lysis, 2007, pp.110, 606~615
  162. Xu HC, "Lymphocytes negatively regulate nk cell activity via Qa-1b following viral infection", Cell Reports, 21, pp.2528~2540 (2017)
  163. Xu HC, "Slow viral propagation during initial phase of infection leads to viral persistence in mice", Commun Biol, 4, pp.508~ (2021)

이 간행물의 다른 논문 (6건)