Natural killer T cells in multiple sclerosis and its animal model, experimental autoimmune encephalomyelitis

Immunology

Volumn 146, Issue 1, 2015, Pages 1-10

  Van Kaer, Luc ^a   Wu, Lan ^a   Parekh, Vrajesh V ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Experimental autoimmune encephalomyelitis; Glycolipid antigens; Immunotherapy; Multiple sclerosis; Natural killer T cells

Indexed keywords

LIPID; CD1D ANTIGEN; GALACTOSYLCERAMIDE;

ANIMAL MODEL; AUTOIMMUNITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; EXPERIMENTAL MODEL; HUMAN; IMMUNOMODULATION; IMMUNOPATHOGENESIS; MULTIPLE SCLEROSIS; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE ACTIVATION; VARIANT NATURAL KILLER T CELL; ANIMAL; C57BL MOUSE; DISEASE MODEL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MOUSE; PROCEDURES;

ANIMALS; ANTIGENS, CD1D; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; GALACTOSYLCERAMIDES; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; NATURAL KILLER T-CELLS;

EID: 84938424067     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12485     Document Type: Review

References (95)

1. Goverman J. Autoimmune T cell responses in the central nervous system. Nat Rev Immunol 2009; 9:393-407.
2. Feinstein A, Freeman J, Lo AC. Treatment of progressive multiple sclerosis: what works, what does not, and what is needed. Lancet Neurol 2015; 14:194-207.
3. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007; 25:297-336.
4. Taniguchi M, Harada M, Kojo S, Nakayama T, Wakao H. The regulatory role of Vα14 NKT cells in innate and acquired immune response. Annu Rev Immunol 2003; 21:483-513.
5. Kronenberg M. Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005; 26:877-900.
6. Brigl M, Brenner MB. CD1: antigen presentation and T cell function. Annu Rev Immunol 2004; 22:817-90.
7. Van Kaer L, Parekh VV, Wu L. Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 2011; 343:43-55.
8. Viale R, Ware R, Maricic I, Chaturvedi V, Kumar V. NKT cell subsets can exert opposing effects in autoimmunity, tumor surveillance and inflammation. Curr Immunol Rev 2012; 8:287-96.
9. 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.
10. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K et al. CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 1997; 278:1626-9.
11. Borg NA, Wun KS, Kjer-Nielsen L, Wilce MC, Pellicci DG, Koh R et al. CD1d-lipid-antigen recognition by the semi-invariant NKT T-cell receptor. Nature 2007; 448:44-9.
12. Van Kaer L, Joyce S. The hunt for iNKT cell antigens: α-galactosidase-deficient mice to the rescue? Immunity 2010; 33:143-5.
13. Brennan PJ, Tatituri RV, Heiss C, Watts GF, Hsu FF, Veerapen N et al. Activation of iNKT cells by a distinct constituent of the endogenous glucosylceramide fraction. Proc Natl Acad Sci USA 2014; 111:13433-8.
14. Kain L, Webb B, Anderson BL, Deng S, Holt M, Costanzo A et al. The identification of the endogenous ligands of natural killer T cells reveals the presence of mammalian α-linked glycosylceramides. Immunity 2014; 41:543-54.
15. Gapin L. The making of NKT cells. Nat Immunol 2008; 9:1009-11.
16. Parekh VV, Lalani S, Van Kaer L. The in vivo response of invariant natural killer T cells to glycolipid antigens. Int Rev Immunol 2007; 26:31-48.
17. Matsuda JL, Mallevaey T, Scott-Browne J, Gapin L. CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 2008; 20:358-68.
18. Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 2013; 14:1146-54.
19. Vinuesa CG, Cyster JG. How T cells earn the follicular rite of passage. Immunity 2011; 35:671-80.
20. Sag D, Krause P, Hedrick CC, Kronenberg M, Wingender G. IL-10-producing NKT10 cells are a distinct regulatory invariant NKT cell subset. J Clin Invest 2014; 124:3725-40.
21. Lynch L, Michelet X, Zhang S, Brennan PJ, Moseman A, Lester C et al. Regulatory iNKT cells lack expression of the transcription factor PLZF and control the homeostasis of T(reg) cells and macrophages in adipose tissue. Nat Immunol 2015; 16:85-95.
22. + invariant NKT cells induced by TGF-β. J Immunol 2010; 185:2157-63.
23. Van Kaer L, Parekh VV, Wu L. Invariant NK T cells: potential for immunotherapeutic targeting with glycolipid antigens. Immunotherapy 2011; 3:59-75.
24. Singh N, Hong S, Scherer DC, Serizawa I, Burdin N, Kronenberg M et al. Cutting edge: activation of NK T cells by CD1d and α-galactosylceramide directs conventional T cells to the acquisition of a Th2 phenotype. J Immunol 1999; 163:2373-7.
25. Van Kaer L. α-Galactosylceramide therapy for autoimmune diseases: prospects and obstacles. Nat Rev Immunol 2005; 5:31-42.
26. Hong S, Wilson MT, Serizawa I, Wu L, Singh N, Naidenko OV et al. The natural killer T-cell ligand α-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat Med 2001; 7:1052-6.
27. + Tregs and NKT cells: regulators regulating regulators. Trends Immunol 2006; 27:322-7.
28. Arrenberg P, Halder R, Dai Y, Maricic I, Kumar V. Oligoclonality and innate-like features in the TCR repertoire of type II NKT cells reactive to a β-linked self-glycolipid. Proc Natl Acad Sci USA 2010; 107:10984-9.
29. Rhost S, Sedimbi S, Kadri N, Cardell SL. Immunomodulatory type II natural killer T lymphocytes in health and disease. Scand J Immunol 2012; 76:246-55.
30. Arrenberg P, Halder R, Kumar V. Cross-regulation between distinct natural killer T cell subsets influences immune response to self and foreign antigens. J Cell Physiol 2009; 218:246-50.
31. Exley MA, Tahir SM, Cheng O, Shaulov A, Joyce R, Avigan D et al. A major fraction of human bone marrow lymphocytes are Th2-like CD1d-reactive T cells that can suppress mixed lymphocyte responses. J Immunol 2001; 167:5531-4.
32. 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.
33. 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.
34. Maricic I, Girardi E, Zajonc DM, Kumar V. Recognition of lysophosphatidylcholine by type II NKT cells and protection from an inflammatory liver disease. J Immunol 2014; 193:4580-9.
35. Girardi E, Maricic I, Wang J, Mac TT, Iyer P, Kumar V et al. Type II natural killer T cells use features of both innate-like and conventional T cells to recognize sulfatide self antigens. Nat Immunol 2012; 13:851-6.
36. Zhao J, Weng X, Bagchi S, Wang CR. Polyclonal type II natural killer T cells require PLZF and SAP for their development and contribute to CpG-mediated antitumor response. Proc Natl Acad Sci USA 2014; 111:2674-9.
37. Kumar V, Delovitch TL. Different subsets of natural killer T cells may vary in their roles in health and disease. Immunology 2014; 142:321-36.
38. Ambrosino E, Terabe M, Halder RC, Peng J, Takaku S, Miyake S et al. Cross-regulation between type I and type II NKT cells in regulating tumor immunity: a new immunoregulatory axis. J Immunol 2007; 179:5126-36.
39. Halder RC, Aguilera C, Maricic I, Kumar V. Type II NKT cell-mediated anergy induction in type I NKT cells prevents inflammatory liver disease. J Clin Invest 2007; 117:2302-12.
40. MacDonald HR. CD1d-glycolipid tetramers: a new tool to monitor natural killer T cells in health and disease [comment]. J Exp Med 2000; 192:F15-20.
41. + T cell antigen receptor defines a population of natural killer T cells with distinct glycolipid antigen-recognition properties. Nat Immunol 2011; 12:616-23.
42. Mendiratta SK, Martin WD, Hong S, Boesteanu A, Joyce S, Van Kaer L. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 1997; 6:469-77.
43. Smiley ST, Kaplan MH, Grusby MJ. Immunoglobulin E production in the absence of interleukin-4-secreting CD1-dependent cells. Science 1997; 275:977-9.
44. + T cell development and early IL-4 production in CD1-deficient mice. Immunity 1997; 6:459-67.
45. Scanlon ST, Thomas SY, Ferreira CM, Bai L, Krausz T, Savage PB et al. Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation. J Exp Med 2011; 208:2113-24.
46. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I et al. Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 1997; 278:1623-6.
47. 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.
48. Bendelac A, Hunziker RD, Lantz O. Increased interleukin 4 and immunoglobulin E production in transgenic mice overexpressing NK1 T cells. J Exp Med 1996; 184:1285-93.
49. - T cells in transgenic mice. J Immunol 2003; 170:2390-8.
50. Wen X, Rao P, Carreno LJ, Kim S, Lawrenczyk A, Porcelli SA et al. Human CD1d knock-in mouse model demonstrates potent antitumor potential of human CD1d-restricted invariant natural killer T cells. Proc Natl Acad Sci USA 2013; 110:2963-8.
51. + T cells with a transgenic variant TCR. J Immunol 2000; 165:168-74.
52. Chen YH, Wang B, Chun T, Zhao L, Cardell S, Behar SM et al. Expression of CD1d2 on thymocytes is not sufficient for the development of NK T cells in CD1d1-deficient mice. J Immunol 1999; 162:4560-6.
53. Wei DG, Lee H, Park SH, Beaudoin L, Teyton L, Lehuen A et al. Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J Exp Med 2005; 202:239-48.
54. Schumann J, Pittoni P, Tonti E, Macdonald HR, Dellabona P, Casorati G. Targeted expression of human CD1d in transgenic mice reveals independent roles for thymocytes and thymic APCs in positive and negative selection of Vα14i NKT cells. J Immunol 2005; 175:7303-10.
55. Yue SC, Shaulov A, Wang R, Balk SP, Exley MA. CD1d ligation on human monocytes directly signals rapid NF-κB activation and production of bioactive IL-12. Proc Natl Acad Sci USA 2005; 102:11811-6.
56. Illes Z, Kondo T, Newcombe J, Oka N, Tabira T, Yamamura T. Differential expression of NK T cell Va24JaQ invariant TCR chain in the lesions of multiple sclerosis and chronic inflammatory demyelinating polyneuropathy. J Immunol 2000; 164:4375-81.
57. + NKT cell numbers are decreased in a wide variety of diseases that are characterized by autoreactive tissue damage. Clin Immunol 2001; 100:144-8.
58. Gigli G, Caielli S, Cutuli D, Falcone M. Innate immunity modulates autoimmunity: type 1 interferon-β treatment in multiple sclerosis promotes growth and function of regulatory invariant natural killer T cells through dendritic cell maturation. Immunology 2007; 122:409-17.
59. + NKT cells derived from multiple sclerosis in remission. Int Immunol 2003; 15:279-88.
60. Sakuishi K, Miyake S, Yamamura T. Role of NK cells and invariant NKT cells in multiple sclerosis. Results Probl Cell Differ 2010; 51:127-47.
61. Shamshiev A, Donda A, Carena I, Mori L, Kappos L, De Libero G. Self glycolipids as T-cell autoantigens. Eur J Immunol 1999; 29:1667-75.
62. Baxter AG. The origin and application of experimental autoimmune encephalomyelitis. Nat Rev Immunol 2007; 7:904-12.
63. McCarthy DP, Richards MH, Miller SD. Mouse models of multiple sclerosis: experimental autoimmune encephalomyelitis and Theiler's virus-induced demyelinating disease. Methods Mol Biol 2012; 900:381-401.
64. Levine S, Sowinski R. Experimental allergic encephalomyelitis in inbred and outbred mice. J Immunol 1973; 110:139-43.
65. + T cells that promptly produce interleukin 4. Proc Natl Acad Sci USA 1995; 92:11931-4.
66. Singh AK, Yang J-Q, Parekh VV, Wei J, Wang C-R, Joyce S et al. The natural killer T cell ligand a-galactosylceramide prevents or promotes pristane-induced lupus in mice. Eur J Immunol 2005; 35:1143-54.
67. Jahng AW, Maricic I, Pedersen B, Burdin N, Naidenko O, Kronenberg M et al. Activation of natural killer T cells potentiates or prevents experimental autoimmune encephalomyelitis. J Exp Med 2001; 194:1789-99.
68. Furlan R, Bergami A, Cantarella D, Brambilla E, Taniguchi M, Dellabona P et al. Activation of invariant NKT cells by a-GalCer administration protects mice from MOG35-55 induced EAE: critical roles for administration route and IFN-γ. Eur J Immunol 2003; 33:1830-8.
69. Denney L, Kok WL, Cole SL, Sanderson S, McMichael AJ, Ho LP. Activation of invariant NKT cells in early phase of experimental autoimmune encephalomyelitis results in differentiation of Ly6Chi inflammatory monocyte to M2 macrophages and improved outcome. J Immunol 2012; 189:551-7.
70. Singh AK, Wilson MT, Hong S, Olivares-Villagomez D, Du C, Stanic AK et al. Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J Exp Med 2001; 194:1801-11.
71. Teige A, Teige I, Lavasani S, Bockermann R, Mondoc E, Homdahl R et al. CD1-dependent regulation of chronic central nervous system inflammation in experimental autoimmune encephalomyelitis. J Immunol 2004; 172:186-94.
72. Mars LT, Laloux V, Goude K, Desbois S, Saoudi A, Van Kaer L et al. Cutting edge: Vα14-Jα281 NKT cells naturally regulate experimental autoimmune encephalomyelitis in nonobese diabetic mice. J Immunol 2002; 168:6007-11.
73. Mars LT, Gautron AS, Novak J, Beaudoin L, Diana J, Liblau RS et al. Invariant NKT cells regulate experimental autoimmune encephalomyelitis and infiltrate the central nervous system in a CD1d-independent manner. J Immunol 2008; 181:2321-9.
74. Kawai E, Sato F, Omura S, Martinez NE, Reddy PC, Taniguchi M et al. Organ-specific protective role of NKT cells in virus-induced inflammatory demyelination and myocarditis depends on mouse strain. J Neuroimmunol 2015; 278:174-84.
75. Yokote H, Miyake S, Croxford JL, Oki S, Mizusawa H, Yamamura T. NKT cell-dependent amelioration of a mouse model of multiple sclerosis by altering gut flora. Am J Pathol 2008; 173:1714-23.
76. Parekh VV, Singh AK, Wilson MT, Olivares-Villagomez D, Bezbradica JS, Inazawa H et al. Quantitative and qualitative differences in the in vivo response of NKT cells to distinct α- and β-anomeric glycolipids. J Immunol 2004; 173:3693-706.
77. Qian G, Qin X, Zang YQ, Ge B, Guo TB, Wan B et al. High doses of α-galactosylceramide potentiate experimental autoimmune encephalomyelitis by directly enhancing Th17 response. Cell Res 2010; 20:480-91.
78. Mars LT, Araujo L, Kerschen P, Diem S, Bourgeois E, Van LP et al. Invariant NKT cells inhibit development of the Th17 lineage. Proc Natl Acad Sci USA 2009; 106:6238-43.
79. Pal E, Tabira T, Kawano T, Taniguchi M, Miyake S, Yamamura T. Costimulation-dependent modulation of experimental autoimmune encephalomyelitis by ligand stimulation of Vα14 NK T cells. J Immunol 2001; 166:662-8.
80. Miyamoto K, Miyake S, Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 2001; 413:531-4.
81. Shiozaki M, Tashiro T, Koshino H, Shigeura T, Watarai H, Taniguchi M et al. Synthesis and biological activity of hydroxylated analogues of KRN7000 (α-galactosylceramide). Carbohydr Res 2013; 370:46-66.
82. Oh SJ, Chung DH. Invariant NKT cells producing IL-4 or IL-10, but not IFN-γ, inhibit the Th1 response in experimental autoimmune encephalomyelitis, whereas none of these cells inhibits the Th17 response. J Immunol 2011; 186:6815-21.
83. Kojo S, Seino K-I, Harada M, Watarai H, Wakao H, Uchida T et al. Induction of regulatory properties in dendritic cells by Vα14 NKT cells. J Immunol 2005; 175:3648-55.
84. Parekh VV, Wu L, Olivares-Villagomez D, Wilson KT, Van Kaer L. Activated invariant NKT cells control central nervous system autoimmunity in a mechanism that involves myeloid-derived suppressor cells. J Immunol 2013; 190:1948-60.
85. Wang J, Cho S, Ueno A, Cheng L, Xu BY, Desrosiers MD et al. Ligand-dependent induction of noninflammatory dendritic cells by anergic invariant NKT cells minimizes autoimmune inflammation. J Immunol 2008; 181:2438-45.
86. Naumov YN, Bahjat KS, Gausling R, Abraham R, Exley MA, Koezuka Y et al. Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc Natl Acad Sci USA 2001; 98:13838-43.
87. Condamine T, Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 2011; 32:19-25.
88. + regulatory T cells. J Immunol 2006; 177:3695-704.
89. + regulatory T cells in the prevention of autoimmune myasthenia. J Immunol 2005; 175:7898-904.
90. Maldonado RA, von Andrian UH. How tolerogenic dendritic cells induce regulatory T cells. Adv Immunol 2010; 108:111-65.
91. + immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006; 66:1123-31.
92. Maricic I, Halder R, Bischof F, Kumar V. Dendritic cells and anergic type I NKT cells play a crucial role in sulfatide-mediated immune regulation in experimental autoimmune encephalomyelitis. J Immunol 2014; 193:1035-46.
93. Brossay L, Chioda M, Burdin N, Koezuka Y, Casorati G, Dellabona P et al. CD1d-mediated recognition of an α-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J Exp Med 1998; 188:1521-8.
94. Spada FM, Koezuka Y, Porcelli SA. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J Exp Med 1998; 188:1529-34.
95. Fujii SI, Shimizu K, Okamoto Y, Kunii N, Nakayama T, Motohashi S et al. NKT cells as an ideal anti-tumor immunotherapeutic. Front Immunol 2013; 4:409.