Natural killer cells regulate diverse T cell responses

Trends in Immunology

Volumn 34, Issue 7, 2013, Pages 342-349

  Crome, Sarah Q ^a   Lang, Philipp A ^b   Lang, Karl S ^c   Ohashi, Pamela S ^a,d  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b Department of Gastroenterology Hepatology and Infectious Diseases ^*  (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

autoimmunity; chronic infection; immune regulation; natural killer cells; T cells; transplantation

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 4; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; ANTIGEN PRESENTATION; AUTOIMMUNITY; BONE MARROW TRANSPLANTATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOKINE PRODUCTION; CYTOTOXICITY; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HISTOCOMPATIBILITY; HUMAN; HYPERTRANSAMINASEMIA; IMMUNOPATHOLOGY; JUVENILE RHEUMATOID ARTHRITIS; MEMORY T LYMPHOCYTE; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; UPREGULATION; VIRAL CLEARANCE; VIRUS INFECTION;

ANIMALS; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; IMMUNOMODULATION; KILLER CELLS, NATURAL; LYMPHOCYTE SUBSETS; MICE; T-LYMPHOCYTES;

EID: 84880799474     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2013.03.002     Document Type: Review

References (87)

1. Lee S.H., et al. Keeping NK cells in highly regulated antiviral warfare. Trends Immunol. 2007, 28:252-259.
2. Smyth M.J., et al. New aspects of natural-killer-cell surveillance and therapy of cancer. Nat. Rev. Cancer 2002, 2:850-861.
3. Orange J.S. Human natural killer cell deficiencies. Curr. Opin. Allergy Clin. Immunol. 2006, 6:399-409.
4. Vossen M.T., et al. Absence of circulating natural killer and primed CD8+ cells in life-threatening varicella. J. Infect. Dis. 2005, 191:198-206.
5. Biron C.A., et al. Severe herpesvirus infections in an adolescent without natural killer cells. N. Engl. J. Med. 1989, 320:1731-1735.
6. Sun J.C., et al. Adaptive immune features of natural killer cells. Nature 2009, 457:557-561.
7. Vivier E., et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011, 331:44-49.
8. Paust S., et al. Adaptive immune responses mediated by natural killer cells. Immunol. Rev. 2010, 235:286-296.
9. Lunemann A., et al. Regulatory NK-cell functions in inflammation and autoimmunity. Mol. Med. 2009, 15:352-358.
10. Smeltz R.B., et al. Inhibition of autoimmune T cell responses in the DA rat by bone marrow-derived NK cells in vitro: implications for autoimmunity. J. Immunol. 1999, 163:1390-1397.
11. Zhang B., et al. Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J. Exp. Med. 1997, 186:1677-1687.
12. Su H.C., et al. NK cell functions restrain T cell responses during viral infections. Eur. J. Immunol. 2001, 31:3048-3055.
13. Lanier L.L. Evolutionary struggles between NK cells and viruses. Nat. Rev. Immunol. 2008, 8:259-268.
14. Moretta A., et al. Early liaisons between cells of the innate immune system in inflamed peripheral tissues. Trends Immunol. 2005, 26:668-675.
15. Walzer T., et al. Natural-killer cells and dendritic cells: "l'union fait la force". Blood 2005, 106:2252-2258.
16. Fort M.M., et al. A role for NK cells as regulators of CD4+ T cells in a transfer model of colitis. J. Immunol. 1998, 161:3256-3261.
17. Vankayalapati R., et al. NK cells regulate CD8+ T cell effector function in response to an intracellular pathogen. J. Immunol. 2004, 172:130-137.
18. Fodil-Cornu N., et al. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 2008, 181:6394-6405.
19. Lee S.H., et al. Activating receptors promote NK cell expansion for maintenance, IL-10 production, and CD8 T cell regulation during viral infection. J. Exp. Med. 2009, 206:2235-2251.
20. Brooks D.G., et al. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 2006, 12:1301-1309.
21. Andrews D.M., et al. Innate immunity defines the capacity of antiviral T cells to limit persistent infection. J. Exp. Med. 2010, 207:1333-1343.
22. Narni-Mancinelli E., et al. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 2012, 335:344-348.
23. Mitrovic M., et al. The NK cell response to mouse cytomegalovirus infection affects the level and kinetics of the early CD8(+) T-cell response. J. Virol. 2012, 86:2165-2175.
24. Shin H., Wherry E.J. CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 2007, 19:408-415.
25. Wherry E.J., et al. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007, 27:670-684.
26. Lang P.A., et al. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:1210-1215.
27. Waggoner S.N., et al. Natural killer cells act as rheostats modulating antiviral T cells. Nature 2012, 481:394-398.
28. Waggoner S.N., et al. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J. Clin. Immunol. 2010, 120:1925-1938.
29. Soderquest K., et al. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 2011, 186:3304-3308.
30. McNerney M.E., et al. Role of natural killer cell subsets in cardiac allograft rejection. Am. J. Transplant. 2006, 6:505-513.
31. Beilke J.N., et al. NK cells promote islet allograft tolerance via a perforin-dependent mechanism. Nat. Med. 2005, 11:1059-1065.
32. Bose A., et al. Cutting edge: perforin down-regulates CD4 and CD8 T cell-mediated immune responses to a transplanted organ. J. Immunol. 2003, 170:1611-1614.
33. Noval Rivas M., et al. NK cell regulation of CD4 T cell-mediated graft-versus-host disease. J. Immunol. 2010, 184:6790-6798.
34. Takeda K., Dennert G. The development of autoimmunity in C57BL/6 lpr mice correlates with the disappearance of natural killer type 1-positive cells: evidence for their suppressive action on bone marrow stem cell proliferation, B cell immunoglobulin secretion, and autoimmune symptoms. J. Exp. Med. 1993, 177:155-164.
35. Lu L., et al. Regulation of activated CD4+ T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity 2007, 26:593-604.
36. Lu L., et al. Regulation of CD8+ regulatory T cells: Interruption of the NKG2A-Qa-1 interaction allows robust suppressive activity and resolution of autoimmune disease. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:19420-19425.
37. Reittie J.E., et al. Endogenously generated activated killer cells circulate after autologous and allogeneic marrow transplantation but not after chemotherapy. Blood 1989, 73:1351-1358.
38. Lowdell M.W. Natural killer cells in haematopoietic stem cell transplantation. Transfus. Med. 2003, 13:399-404.
39. Larghero J., et al. Association of bone marrow natural killer cell dose with neutrophil recovery and chronic graft-versus-host disease after HLA identical sibling bone marrow transplants. Br. J. Haematol. 2007, 138:101-109.
40. Bielekova B., et al. Regulatory CD56(bright) natural killer cells mediate immunomodulatory effects of IL-2Ralpha-targeted therapy (daclizumab) in multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5941-5946.
41. Villanueva J., et al. Natural killer cell dysfunction is a distinguishing feature of systemic onset juvenile rheumatoid arthritis and macrophage activation syndrome. Arthritis Res. Ther. 2005, 7:R30-R37.
42. Yoon J.C., et al. Natural killer cell function is intact after direct exposure to infectious hepatitis C virions. Hepatology 2009, 49:12-21.
43. Ahlenstiel G., et al. Effects of the CCR5-Delta32 mutation on hepatitis C virus-specific immune responses in patients with haemophilia. Immunol. Invest. 2009, 38:284-296.
44. Amadei B., et al. Activation of natural killer cells during acute infection with hepatitis C virus. Gastroenterology 2010, 138:1536-1545.
45. Khakoo S.I., et al. HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 2004, 305:872-874.
46. Paladino N., et al. Increased frequencies of activating natural killer receptors are associated with liver injury in individuals who do not eliminate hepatitis C virus. Tissue Antigens 2007, 69(Suppl. 1):109-111.
47. Dring M.M., et al. Innate immune genes synergize to predict increased risk of chronic disease in hepatitis C virus infection. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:5736-5741.
48. Ahlenstiel G., et al. Early changes in natural killer cell function indicate virologic response to interferon therapy for hepatitis C. Gastroenterology 2011, 141:1231-1239. 1239 e1231-1232.
49. Pembroke T., et al. Rapid early innate control of hepatitis C virus during IFN-alpha treatment compromises adaptive CD4(+) T-cell immunity. Eur. J. Immunol. 2012, 42:2383-2394.
50. Robbins S.H., et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 2007, 3:e123.
51. Krebs P., et al. NK-cell-mediated killing of target cells triggers robust antigen-specific T-cell-mediated and humoral responses. Blood 2009, 113:6593-6602.
52. Sun J.C., Lanier L.L. NK cell development, homeostasis and function: parallels with CD8(+) T cells. Nat. Rev. Immunol. 2011, 11:645-657.
53. De Rose V., et al. IFN-gamma inhibits the proliferation of allergen-activated T lymphocytes from atopic, asthmatic patients by inducing Fas/FasL-mediated apoptosis. J. Leukoc. Biol. 2004, 76:423-432.
54. Ivanov I.I., et al. Transcriptional regulation of Th17 cell differentiation. Semin. Immunol. 2007, 19:409-417.
55. Manetti R., et al. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune responses and inhibits the development of IL-4-producing Th cells. J. Exp. Med. 1993, 177:1199-1204.
56. Crome S.Q., et al. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin. Exp. Immunol. 2010, 159:109-119.
57. Zhu J., Paul W.E. CD4 T cells: fates, functions, and faults. Blood 2008, 112:1557-1569.
58. Morandi B., et al. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-gamma secretion. Eur. J. Immunol. 2006, 36:2394-2400.
59. Deniz G., et al. Regulatory NK cells suppress antigen-specific T cell responses. J. Immunol. 2008, 180:850-857.
60. Cerboni C., et al. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK- cell lysis. Blood 2007, 110:606-615.
61. Rabinovich B.A., et al. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J. Immunol. 2003, 170:3572-3576.
62. Kagi D., et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 1994, 369:31-37.
63. Roy S., et al. NK cells lyse T regulatory cells that expand in response to an intracellular pathogen. J. Immunol. 2008, 180:1729-1736.
64. Thornton A.M., et al. Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 2010, 184:3433-3441.
65. Dovat S., et al. Transgenic expression of Helios in B lineage cells alters B cell properties and promotes lymphomagenesis. J. Immunol. 2005, 175:3508-3515.
66. Naganuma H., et al. Increased susceptibility of IFN-gamma-treated neuroblastoma cells to lysis by lymphokine-activated killer cells: participation of ICAM-1 induction on target cells. Int. J. Cancer 1991, 47:527-532.
67. Barber D.F., et al. LFA-1 contributes an early signal for NK cell cytotoxicity. J. Immunol. 2004, 173:3653-3659.
68. Jiang W., et al. Unexpected role for granzyme K in CD56bright NK cell-mediated immunoregulation of multiple sclerosis. J. Immunol. 2011, 187:781-790.
69. Nielsen N., et al. Cytotoxicity of CD56(bright) NK cells towards autologous activated CD4+ T cells is mediated through NKG2D, LFA-1 and TRAIL and dampened via CD94/NKG2A. PLoS ONE 2012, 7:e31959.
70. Peppa D., et al. Up-regulation of a death receptor renders antiviral T cells susceptible to NK cell-mediated deletion. J. Exp. Med. 2013, 210:99-114.
71. Allan S.E., et al. CD4+ T-regulatory cells: toward therapy for human diseases. Immunol. Rev. 2008, 223:391-421.
72. Lanier L.L. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008, 9:495-502.
73. Hayakawa Y., Smyth M.J. CD27 dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J. Immunol. 2006, 176:1517-1524.
74. Huntington N.D., et al. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 2007, 7:703-714.
75. Robbins S.H., et al. Cutting edge: inhibitory functions of the killer cell lectin-like receptor G1 molecule during the activation of mouse NK cells. J. Immunol. 2002, 168:2585-2589.
76. Sun J.C., et al. NK cells and immune "memory". J. Immunol. 2011, 186:1891-1897.
77. Di Santo J.P. Functionally distinct NK-cell subsets: developmental origins and biological implications. Eur. J. Immunol. 2008, 38:2948-2951.
78. De Maria A., et al. Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:728-732.
79. Strowig T., et al. Noncytotoxic functions of NK cells: direct pathogen restriction and assistance to adaptive immunity. J. Immunol. 2008, 180:7785-7791.
80. Ferlazzo G., et al. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J. Immunol. 2004, 172:1455-1462.
81. Ferlazzo G., Munz C. NK cell compartments and their activation by dendritic cells. J. Immunol. 2004, 172:1333-1339.
82. Dalbeth N., et al. CD56bright NK cells are enriched at inflammatory sites and can engage with monocytes in a reciprocal program of activation. J. Immunol. 2004, 173:6418-6426.
83. Ottaviani C., et al. CD56brightCD16(-) NK cells accumulate in psoriatic skin in response to CXCL10 and CCL5 and exacerbate skin inflammation. Eur. J. Immunol. 2006, 36:118-128.
84. Carrega P., et al. Natural killer cells infiltrating human nonsmall-cell lung cancer are enriched in CD56 bright CD16(-) cells and display an impaired capability to kill tumor cells. Cancer 2008, 112:863-875.
85. Jacobs R., et al. CD56bright cells differ in their KIR repertoire and cytotoxic features from CD56dim NK cells. Eur. J. Immunol. 2001, 31:3121-3127.
86. Chen S., et al. Suppression of tumor formation in lymph nodes by L-selectin-mediated natural killer cell recruitment. J. Exp. Med. 2005, 202:1679-1689.
87. Mailliard R.B., et al. IL-18-induced CD83+CCR7+ NK helper cells. J. Exp. Med. 2005, 202:941-953.