The role of invariant natural killer T cells in microbial immunity

Journal of Infection and Chemotherapy

Volumn 19, Issue 4, 2013, Pages 560-570

  Kinjo, Yuki ^a   Kitano, Naoki ^a   Kronenberg, Mitchell ^a,b  

^a NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Bacteria; CD1d; Glycolipid; Invariant; NKT cell

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; BACTERIAL ANTIGEN; CD1D ANTIGEN; CHICKENPOX VACCINE; GAMMA INTERFERON; GLYCOLIPID; INACTIVATED VIRUS VACCINE; INFLUENZA VACCINE; INTERLEUKIN 13; INTERLEUKIN 4; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; X LINKED INHIBITOR OF APOPTOSIS;

ANTIBODY TITER; ANTIGEN RECOGNITION; BACTERIAL INFECTION; CHLAMYDIASIS; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; EPSTEIN BARR VIRUS INFECTION; HOST RESISTANCE; HUMAN; INFECTION; INFLAMMATION; INFLUENZA; INNATE IMMUNITY; INTESTINE FLORA; INVARIANT NATURAL KILLER T CELL; LYMPHOPROLIFERATIVE DISEASE; MICROBIAL IMMUNITY; MYCOSIS; NATURAL KILLER T CELL; NONHUMAN; PROTOZOAL INFECTION; REVIEW; STREPTOCOCCUS PNEUMONIAE; T LYMPHOCYTE ACTIVATION; VIRUS INFECTION;

ANIMALS; ANTIGENS; COMMUNICABLE DISEASES; CYTOKINES; HUMANS; NATURAL KILLER T-CELLS; SIGNAL TRANSDUCTION;

EID: 84882249534     PISSN: 1341321X     EISSN: 14377780     Source Type: Journal    
DOI: 10.1007/s10156-013-0638-1     Document Type: Review

References (89)

1. Tupin E, Kinjo Y, Kronenberg M. The unique role of natural killer T cells in the response to microorganisms. Nat Rev Microbiol. 2007;5:405-17.
2. Taniguchi M, Tashiro T, Dashtsoodol N, Hongo N, Watarai H. The specialized iNKT cell system recognizes glycolipid antigens and bridges the innate and acquired immune systems with potential applications for cancer therapy. Int Immunol. 2010;22:1-6.
3. Brigl M, Brenner MB. How invariant natural killer T cells respond to infection by recognizing microbial or endogenous lipid antigens. Semin Immunol. 2010;22:79-86.
4. Pei B, Vela JL, Zajonc D, Kronenberg M. Interplay between carbohydrate and lipid in recognition of glycolipid antigens by natural killer T cells. Ann N Y Acad Sci. 2012;1253:68-79.
5. Rossjohn J, Pellicci DG, Patel O, Gapin L, Godfrey DI. Recognition of CD1d-restricted antigens by natural killer T cells. Nat Rev Immunol. 2012;12:845-57.
6. Zajonc DM, Kronenberg M. Carbohydrate specificity of the recognition of diverse glycolipids by natural killer T cells. Immunol Rev. 2009;230:188-200.
7. Godfrey DI, MacDonald HR, Kronenberg M, Smyth MJ, Van Kaer L. NKT cells: what's in a name? Nat Rev Immunol. 2004;4:231-7.
8. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, et al. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 1997;278:1626-9.
9. Brossay L, Chioda M, Burdin N, Koezuka Y, Casorati G, Dellabona P, et al. CD1d-mediated recognition of an alpha-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J Exp Med. 1998;188:1521-8.
10. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, Kumar V. Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide. J Exp Med. 2004;199:947-57.
11. Terabe M, Swann J, Ambrosino E, Sinha P, Takaku S, Hayakawa Y, et al. A nonclassical non-V alpha14J alpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med. 2005;202:1627-33.
12. Rhost S, Lofbom L, Rynmark BM, Pei B, Mansson JE, Teneberg S, et al. Identification of novel glycolipid ligands activating a sulfatide-reactive, CD1d-restricted, type II natural killer T lymphocyte. Eur J Immunol. 2012;42:2851-60.
13. Tatituri RV, Watts GF, Bhowruth V, Barton N, Rothchild A, Hsu FF, et al. Recognition of microbial and mammalian phospholipid antigens by NKT cells with diverse TCRs. Proc Natl Acad Sci USA. 2013;110:1827-32.
14. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, et al. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science. 1997;278:1623-6.
15. Kawakami K, Yamamoto N, Kinjo Y, Miyagi K, Nakasone C, Uezu K, et al. Critical role of Valpha14+ natural killer T cells in the innate phase of host protection against Streptococcus pneumoniae infection. Eur J Immunol. 2003;33:3322-30.
16. Nakamatsu M, Yamamoto N, Hatta M, Nakasone C, Kinjo T, Miyagi K, et al. Role of interferon-gamma in Valpha14+ natural killer T cell-mediated host defense against Streptococcus pneumoniae infection in murine lungs. Microbes Infect. 2007;9:364-74.
17. Bedel R, Matsuda JL, Brigl M, White J, Kappler J, Marrack P, et al. Lower TCR repertoire diversity in Traj18-deficient mice. Nat Immunol. 2012;13:705-6.
18. Kinjo Y, Illarionov P, Vela JL, Pei B, Girardi E, Li X, et al. Invariant natural killer T cells recognize glycolipids from pathogenic gram-positive bacteria. Nat Immunol. 2011;12:966-74.
19. Joyee AG, Qiu H, Wang S, Fan Y, Bilenki L, Yang X. Distinct NKT cell subsets are induced by different Chlamydia species leading to differential adaptive immunity and host resistance to the infections. J Immunol. 2007;178:1048-58.
20. Joyee AG, Uzonna J, Yang X. Invariant NKT cells preferentially modulate the function of CD8 alpha+ dendritic cell subset in inducing type 1 immunity against infection. J Immunol. 2010;184:2095-106.
21. Peng Y, Zhao L, Shekhar S, Liu L, Wang H, Chen Q, et al. The glycolipid exoantigen derived from Chlamydia muridarum activates invariant natural killer T cells. Cell Mol Immunol. 2012;9:361-6.
22. Jiang J, Karimi O, Ouburg S, Champion CI, Khurana A, Liu G, et al. Interruption of CXCL13-CXCR5 axis increases upper genital tract pathology and activation of NKT cells following chlamydial genital infection. PLoS ONE. 2012;7:e47487.
23. Kawana K, Quayle AJ, Ficarra M, Ibana JA, Shen L, Kawana Y, et al. CD1d degradation in Chlamydia trachomatis-infected epithelial cells is the result of both cellular and chlamydial proteasomal activity. J Biol Chem. 2007;282:7368-75.
24. Wong CH, Jenne CN, Lee WY, Leger C, Kubes P. Functional innervation of hepatic iNKT cells is immunosuppressive following stroke. Science. 2011;334:101-5.
25. Kawakami K, Kinjo Y, Uezu K, Yara S, Miyagi K, Koguchi Y, et al. Monocyte chemoattractant protein-1-dependent increase of V alpha 14 NKT cells in lungs and their roles in Th1 response and host defense in cryptococcal infection. J Immunol. 2001;167:6525-32.
26. Cohen NR, Tatituri RV, Rivera A, Watts GF, Kim EY, Chiba A, et al. Innate recognition of cell wall beta-glucans drives invariant natural killer T cell responses against fungi. Cell Host Microbe. 2011;10:437-50.
27. Ishikawa H, Hisaeda H, Taniguchi M, Nakayama T, Sakai T, Maekawa Y, et al. CD4(+) v(alpha)14 NKT cells play a crucial role in an early stage of protective immunity against infection with Leishmania major. Int Immunol. 2000;12:1267-74.
28. Mattner J, Donhauser N, Werner-Felmayer G, Bogdan C. NKT cells mediate organ-specific resistance against Leishmania major infection. Microbes Infect. 2006;8:354-62.
29. Amprey JL, Im JS, Turco SJ, Murray HW, Illarionov PA, Besra GS, et al. A subset of liver NK T cells is activated during Leishmania donovani infection by CD1d-bound lipophosphoglycan. J Exp Med. 2004;200:895-904.
30. Duthie MS, Kahn M, White M, Kapur RP, Kahn SJ. Critical proinflammatory and anti-inflammatory functions of different subsets of CD1d-restricted natural killer T cells during Trypanosoma cruzi infection. Infect Immun. 2005;73:181-92.
31. Tyznik AJ, Tupin E, Nagarajan NA, Her MJ, Benedict CA, Kronenberg M. Cutting edge: the mechanism of invariant NKT cell responses to viral danger signals. J Immunol. 2008;181:4452-6.
32. Wesley JD, Tessmer MS, Chaukos D, Brossay L. NK cell-like behavior of Valpha14i NK T cells during MCMV infection. PLoS Pathog. 2008;4:e1000106.
33. Lee SH, Girard S, Macina D, Busa M, Zafer A, Belouchi A, et al. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat Genet. 2001;28:42-5.
34. Daniels KA, Devora G, Lai WC, O'Donnell CL, Bennett M, Welsh RM. Murine cytomegalovirus is regulated by a discrete subset of natural killer cells reactive with monoclonal antibody to Ly49H. J Exp Med. 2001;194:29-44.
35. Ashkar AA, Rosenthal KL. Interleukin-15 and natural killer and NKT cells play a critical role in innate protection against genital herpes simplex virus type 2 infection. J Virol. 2003;77:10168-71.
36. Grubor-Bauk B, Simmons A, Mayrhofer G, Speck PG. Impaired clearance of herpes simplex virus type 1 from mice lacking CD1d or NKT cells expressing the semivariant V alpha 14-J alpha 281 TCR. J Immunol. 2003;170:1430-4.
37. Cornish AL, Keating R, Kyparissoudis K, Smyth MJ, Carbone FR, Godfrey DI. NKT cells are not critical for HSV-1 disease resolution. Immunol Cell Biol. 2006;84:13-9.
38. Nieuwenhuis EE, Matsumoto T, Exley M, Schleipman RA, Glickman J, Bailey DT, et al. CD1d-dependent macrophage-mediated clearance of Pseudomonas aeruginosa from lung. Nat Med. 2002;8:588-93.
39. Kinjo T, Nakamatsu M, Nakasone C, Yamamoto N, Kinjo Y, Miyagi K, et al. NKT cells play a limited role in the neutrophilic inflammatory responses and host defense to pulmonary infection with Pseudomonas aeruginosa. Microbes Infect. 2006;8:2679-85.
40. Mannoor MK, Weerasinghe A, Halder RC, Reza S, Morshed M, Ariyasinghe A, et al. Resistance to malarial infection is achieved by the cooperation of NK1.1(+) and NK1.1(-) subsets of intermediate TCR cells which are constituents of innate immunity. Cell Immunol. 2001;211:96-104.
41. Hansen DS, Siomos MA, Buckingham L, Scalzo AA, Schofield L. Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity. 2003;18:391-402.
42. Kee SJ, Kwon YS, Park YW, Cho YN, Lee SJ, Kim TJ, et al. Dysfunction of natural killer T cells in patients with active Mycobacterium tuberculosis infection. Infect Immun. 2012;80:2100-8.
43. Levy O, Orange JS, Hibberd P, Steinberg S, LaRussa P, Weinberg A, et al. Disseminated varicella infection due to the vaccine strain of varicella-zoster virus, in a patient with a novel deficiency in natural killer T cells. J Infect Dis. 2003;188:948-53.
44. Banovic T, Yanilla M, Simmons R, Robertson I, Schroder WA, Raffelt NC, et al. Disseminated varicella infection caused by varicella vaccine strain in a child with low invariant natural killer T cells and diminished CD1d expression. J Infect Dis. 2011;204:1893-901.
45. Pasquier B, Yin L, Fondaneche MC, Relouzat F, Bloch-Queyrat C, Lambert N, et al. Defective NKT cell development in mice and humans lacking the adapter SAP, the X-linked lymphoproliferative syndrome gene product. J Exp Med. 2005;201:695-701.
46. Nichols KE, Hom J, Gong SY, Ganguly A, Ma CS, Cannons JL, et al. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat Med. 2005;11:340-5.
47. Rigaud S, Fondaneche MC, Lambert N, Pasquier B, Mateo V, Soulas P, et al. XIAP deficiency in humans causes an X-linked lymphoproliferative syndrome. Nature (Lond). 2006;444:110-4.
48. Yuan W, Dasgupta A, Cresswell P. Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling. Nat Immunol. 2006;7:835-42.
49. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X, Knipe DM, et al. Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J Virol. 2011;85:8093-104.
50. Hage CA, Kohli LL, Cho S, Brutkiewicz RR, Twigg HL 3rd, Knox KS. Human immunodeficiency virus gp120 downregulates CD1d cell surface expression. Immunol Lett. 2005;98:131-5.
51. Chen N, McCarthy C, Drakesmith H, Li D, Cerundolo V, McMichael AJ, et al. HIV-1 down-regulates the expression of CD1d via Nef. Eur J Immunol. 2006;36:278-86.
52. Sanchez DJ, Gumperz JE, Ganem D. Regulation of CD1d expression and function by a herpesvirus infection. J Clin Invest. 2005;115:1369-78.
53. Kim EY, Battaile JT, Patel AC, You Y, Agapov E, Grayson MH, et al. Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med. 2008;14:633-40.
54. Lappas CM, Day YJ, Marshall MA, Engelhard VH, Linden J. Adenosine A2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation. J Exp Med. 2006;203:2639-48.
55. Selmi C, Balkwill DL, Invernizzi P, Ansari AA, Coppel RL, Podda M, et al. Patients with primary biliary cirrhosis react against a ubiquitous xenobiotic-metabolizing bacterium. Hepatology. 2003;38:1250-7.
56. Mattner J, Savage PB, Leung P, Oertelt SS, Wang V, Trivedi O, et al. Liver autoimmunity triggered by microbial activation of natural killer T cells. Cell Host Microbe. 2008;3:304-15.
57. Kita H, Naidenko OV, Kronenberg M, Ansari AA, Rogers P, He XS, et al. Quantitation and phenotypic analysis of natural killer T cells in primary biliary cirrhosis using a human CD1d tetramer. Gastroenterology. 2002;123:1031-43.
58. Park SH, Benlagha K, Lee D, Balish E, Bendelac A. Unaltered phenotype, tissue distribution and function of V alpha14(+) NKT cells in germ-free mice. Eur J Immunol. 2000;30:620-5.
59. Wingender G, Stepniak D, Krebs P, Lin L, McBride S, Wei B, et al. Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice. Gastroenterology. 2012;143:418-28.
60. Olszak T, An D, Zeissig S, Vera MP, Richter J, Franke A, et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science. 2012;336:489-93.
61. Heller F, Fuss IJ, Nieuwenhuis EE, Blumberg RS, Strober W. Oxazolone colitis, a Th2 colitis model resembling ulcerative colitis, is mediated by IL-13-producing NK-T cells. Immunity. 2002;17:629-38.
62. Chang YJ, Kim HY, Albacker LA, Lee HH, Baumgarth N, Akira S, et al. Influenza infection in suckling mice expands an NKT cell subset that protects against airway hyperreactivity. J Clin Invest. 2011;121:57-69.
63. Brigl M, Bry L, Kent SC, Gumperz JE, Brenner MB. Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol. 2003;4:1230-7.
64. Nagarajan NA, Kronenberg M. Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J Immunol. 2007;178:2706-13.
65. Fischer K, Scotet E, Niemeyer M, Koebernick H, Zerrahn J, Maillet S, et al. Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc Natl Acad Sci USA. 2004;101:10685-90.
66. Kinjo Y, Wu D, Kim G, Xing GW, Poles MA, Ho DD, et al. Recognition of bacterial glycosphingolipids by natural killer T cells. Nature (Lond). 2005;434:520-5.
67. Mattner J, Debord KL, Ismail N, Goff RD, Cantu C 3rd, Zhou D, et al. Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature (Lond). 2005;434:525-9.
68. Sriram V, Du W, Gervay-Hague J, Brutkiewicz RR. Cell wall glycosphingolipids of Sphingomonas paucimobilis are CD1d-specific ligands for NKT cells. Eur J Immunol. 2005;35:1692-701.
69. Neef A, Witzenberger R, Kampfer P. Detection of sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes. J Ind Microbiol Biotechnol. 1999;23:261-7.
70. Long X, Deng S, Mattner J, Zang Z, Zhou D, McNary N, et al. Synthesis and evaluation of stimulatory properties of Sphingomonadaceae glycolipids. Nat Chem Biol. 2007;3:559-64.
71. Kinjo Y, Pei B, Bufali S, Raju R, Richardson SK, Imamura M, et al. Natural Sphingomonas glycolipids vary greatly in their ability to activate natural killer T cells. Chem Biol. 2008;15:654-64.
72. Brown LCW, Penaranda C, Kashyap PC, Williams BB, Clardy J, Kronenberg M, et al. Production of an NKT cell stimulatory glycosphingolipid by a prominent member of the human gut microbiota PLoS Biol 2013 (in press).
73. Kinjo Y, Tupin E, Wu D, Fujio M, Garcia-Navarro R, Benhnia MR, et al. Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat Immunol. 2006;7:978-86.
74. Ben-Menachem G, Kubler-Kielb J, Coxon B, Yergey A, Schneerson R. A newly discovered cholesteryl galactoside from Borrelia burgdorferi. Proc Natl Acad Sci USA. 2003;100:7913-8.
75. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet. 2009;374:893-902.
76. Li Y, Girardi E, Wang J, Yu ED, Painter GF, Kronenberg M, et al. The Valpha14 invariant natural killer T cell TCR forces microbial glycolipids and CD1d into a conserved binding mode. J Exp Med. 2010;207:2383-93.
77. Girardi E, Yu ED, Li Y, Tarumoto N, Pei B, Wang J, et al. Unique interplay between sugar and lipid in determining the antigenic potency of bacterial antigens for NKT cells. PLoS Biol. 2011;9:e1001189.
78. Wu D, Zajonc DM, Fujio M, Sullivan BA, Kinjo Y, Kronenberg M, et al. Design of natural killer T cell activators: structure and function of a microbial glycosphingolipid bound to mouse CD1d. Proc Natl Acad Sci USA. 2006;103:3972-7.
79. Tupin E, Benhnia MR, Kinjo Y, Patsey R, Lena CJ, Haller MC, et al. NKT cells prevent chronic joint inflammation after infection with Borrelia burgdorferi. Proc Natl Acad Sci USA. 2008;105:19863-8.
80. Olson CM Jr, Bates TC, Izadi H, Radolf JD, Huber SA, Boyson JE, et al. Local production of IFN-gamma by invariant NKT cells modulates acute Lyme carditis. J Immunol. 2009;182:3728-34.
81. Lee WY, Moriarty TJ, Wong CH, Zhou H, Strieter RM, van Rooijen N, et al. An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol. 2010;11:295-302.
82. Geissmann F, Cameron TO, Sidobre S, Manlongat N, Kronenberg M, Briskin MJ, et al. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol. 2005;3:e113.
83. Brigl M, Tatituri RV, Watts GF, Bhowruth V, Leadbetter EA, Barton N, et al. Innate and cytokine-driven signals, rather than microbial antigens, dominate in natural killer T cell activation during microbial infection. J Exp Med. 2011;208:1163-77.
84. Ko SY, Ko HJ, Chang WS, Park SH, Kweon MN, Kang CY. Alpha- galactosylceramide can act as a nasal vaccine adjuvant inducing protective immune responses against viral infection and tumor. J Immunol. 2005;175:3309-17.
85. Youn HJ, Ko SY, Lee KA, Ko HJ, Lee YS, Fujihashi K, et al. A single intranasal immunization with inactivated influenza virus and alpha-galactosylceramide induces long-term protective immunity without redirecting antigen to the central nervous system. Vaccine. 2007;25:5189-98.
86. Kamijuku H, Nagata Y, Jiang X, Ichinohe T, Tashiro T, Mori K, et al. Mechanism of NKT cell activation by intranasal coadministration of alpha-galactosylceramide, which can induce cross-protection against influenza viruses. Mucosal Immunol. 2008;1:208-18.
87. Guillonneau C, Mintern JD, Hubert FX, Hurt AC, Besra GS, Porcelli S, et al. Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc Natl Acad Sci USA. 2009;106:3330-5.
88. Li X, Fujio M, Imamura M, Wu D, Vasan S, Wong CH, et al. Design of a potent CD1d-binding NKT cell ligand as a vaccine adjuvant. Proc Natl Acad Sci USA. 2010;107:13010-5.
89. Lindqvist M, Persson J, Thorn K, Harandi AM. The mucosal adjuvant effect of alpha-galactosylceramide for induction of protective immunity to sexually transmitted viral infection. J Immunol. 2009;182:6435-43.