The role of invariant natural killer T cells in lupus and atherogenesis

Immunologic Research

Volumn 34, Issue 1, 2006, Pages 49-66

  Major, Amy S ^a   Singh, Ram R ^b   Joyce, Sebastian ^a   Van Kaer, Luc ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Galactosylceramide; Atherosclerosis; CD1d; Glycolipids; Immunomodulation; Immunotherapy; Invariant natural killer T cells; Systemic lupus erythematosus

Indexed keywords

ANIMALS; ANTIGEN-PRESENTING CELLS; ATHEROSCLEROSIS; HUMANS; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; T-LYMPHOCYTES;

EID: 33646864753     PISSN: 0257277X     EISSN: None     Source Type: Journal    
DOI: 10.1385/IR:34:1:49     Document Type: Article

References (82)

1. Binder CJ, Chang MK, Shaw PX, et al: Innate and acquired immunity in atherogenesis. Nat Med 2002;8:1218-1226.
2. Wick G, Knoflach M, Xu Q: Autoimmune and inflammatory mechanisms in atherosclerosis. Annu Rev Immunol 2004;22:361-403.
3. Lockshin MD, Salmon JE, Roman MJ: Atherosclerosis and lupus: a work in progress. Arthritis Rheum 2001;44:2215-2217.
4. Bendelac A, Rivera MN, Park SH, Roark JH: Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu Rev Immunol 1997;15:535-562.
5. 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.
6. Van Kaer L: Regulation of immune responses by CD1d-restricted natural killer T cells. Immunol Res 2004;30:139-153.
7. Brigl M, Brenner MB: CD1: antigen presentation and T cell function. Annu Rev Immunol 2004;22:817-890.
8. Godfrey DI, Kronenberg M: Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest 2004;114:1379-1388.
9. Kronenberg M: Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005;26:877-900.
10. Bezbradica JS, Joyce S: Natural T lymphocytes and dendritic cells: an innate duet that arouses and tempers immune responses; in Gorczynski RM (ed): Altered Immunoregulation and Human Disease, Trivandrum, Kerala, India, Research Signpost 2005, pp. 137-163.
11. Kawano T, Cui J, Koezuka Y, et al: CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 1997;278:1626-1629.
12. Gumperz JE, Roy C, Makowska A, et al: Murine CD1d-restricted T cell recognition of cellular lipids. Immunity 2000;12:211-221.
13. Wu DY, Segal NH, Sidobre S, Kronenberg M, Chapman PB: Cross-presentation of disialoganglioside GD3 to natural killer T cells. J Exp Med 2003;198:173-181.
14. Fischer K, Scotet E, Niemeyer M, et al: Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc Natl Acad Sci USA 2004;101:10685-10690.
15. Amprey JL, Im JS, Turco SJ, 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.
16. Stanic AK, De Silva AD, Park JJ, et al: Defective presentation of the CD1d1-restricted natural Va14Ja18 NKT lymphocyte antigen caused by β-D-glucosylceramide synthase deficiency. Proc Natl Acad Sci USA 2003;100:1849-1854.
17. Zhou D, Mattner J, Cantu C, et al: Lysosomal glycophingolipid recognition by NKT cells. Science 2004;306:1786-1789.
18. Mattner J, DeBord KL, Ismail N, et al: Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 2005;434:525-529.
19. Kinjo Y, Wu DY, Kim G, et al: Recognition of bacterial glycosphingolipids by natural killer T cells. Nature 2005;434:520-525.
20. Sriram V, Du W, Gervay-Hague J, Brutkiewicz RR: Cell wall glycosphingolipids of Sphingomonas paucimobilis are CD1d-specific ligand for NKT cells. Eur J Immunol 2005;35:1692-1701.
21. Van Kaer L, Joyce S: Innate immunity: NKT cells in the spotlight. Curr Biol 2005;15:R429-R431.
22. Joyce S, Woods AS, Yewdell JW, et al: Natural ligand of mouse CD1d1: cellular glycosylphosphatidylinositol. Science 1998;279:1541-1544.
23. Park J-J, Kang SJ, De Silva AD, et al: Lipid-protein interactions: biosynthetic assembly of CD1 with lipids in the endoplasmic reticulum is evolutionarily conserved. Proc Natl Acad Sci USA 2004;101:1022-1026.
24. De Silva AD, Park JJ, Matsuki N, et al: Lipid protein interactions: the assembly of CD1d1 with cellular phospholipids occurs in the endoplasmic reticulum. J Immunol 2002;168:723-733.
25. Brozovic S, Nagaishi T, Yoshida M, et al: CD1d function is regulated by microsomal triglyceride transfer protein. Nat Med 2004;10:535-539.
26. Dougan SK, Salas A, Rava P, et al: Microsomal triglyceride transfer protein lipidation and control of CD1d on antigen-presenting cells. J Exp Med 2005;202:529-539.
27. Kang SJ, Cresswell P: Saposins facilitate CD1d-restricted presentation of an exogenous lipid antigen to T cells. Nat Immunol 2004;5:175-181.
28. Zhou D, Cantu C, Sagiv Y, et al: Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 2004;303:523-527.
29. van den Elzen P, Garg S, Leon L, et al: Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005;437:906-910.
30. Prigozy TI, Naidenko O, Qasba P, et al: Glycolipid antigen processing for presentation by CD1d molecules. Science 2001;291:664-667.
31. Kobayashi E, Motoki K, Uchida T, Fukushima H, Koezuka Y: KRN7000, a novel immunomodulator, and its antitumor activities. Oncol Res 1995;7:529-534.
32. Bezbradica JS, Stanic AK, Matsuki N, et al: Distinct roles of dendritic cells and B cells in Va14Ja18 natural T cell activation in vivo. J Immunol 2005;174:4694-4705.
33. Schmieg J, Yang G, Franck RW, Van Rooijen N, Tsuji M: Glycolipid presentation to natural killer T cells differs in an organ-dependent fashion. Proc Natl Acad Sci USA 2005;102:1127-1132.
34. Eberl G, MacDonald HR: Rapid death and regeneration of NKT cells in anti-CD3epsilon- or IL-12-treated mice: a major role for bone marrow in NKT cell homeostasis. Immunity 1998;9:345-353.
35. Eberl G, MacDonald HR: Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells. Eur J Immunol 2000;30:985-992.
36. Leite-de-Moraes MC, Herbelin A, Gouarin C, Koezuka Y, Schneider E, Dy M: Fas/Fas ligand interactions promote activation-induced cell death of NK T lymphocytes. J Immunol 2000;165:4367-4371.
37. Wilson MT, Johansson C, Olivares-Villagomez D, et al: The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion. Proc Natl Acad Sci USA 2003;100:10913-10918.
38. Parekh VV, Singh AK, Wilson MT, et al: Quantitative and qualitative differences in the in vivo response of NKT cells to distinct α- and β-anomeric glycolipids. J Immunol 2004;173:3693-3706.
39. Singh N, Hong S, Scherer DC, et al: Cutting edge: Activation of NKT cells by CD1d and α-galactosylceramide directs conventional T cells to the acquisition of a Th2 phenotype. J Immunol 1999;163:2373-2377.
40. Fujii S, Shimizu K, Kronenberg M, Steinman RM: Prolonged IFN-γ-producing NKT response induced with α-galactosylceramide- loaded DCs. Nat Immunol 2002;3:867-874.
41. Matsuda JL, Gapin L, Baron JL, et al: Mouse Vα14i natural killer T cells are resistant to cytokine polarization in vivo. Proc Natl Acad Sci USA 2003;100:8395-8400.
42. Parekh VV, Wilson MT, Olivares-Villagomez D, et al: Glycolipid antigen induces long-term natural killer T cell anergy in mice. J Clin Invest 2005;115:2572-2583.
43. Crowe NY, Uldrich AP, Kyparissoudis K, et al: Glycolipid antigen drives rapid expansion and sustained cytokine production by NKT cells. J Immunol 2003;171:4020-4027.
44. Harada M, Seino KI, Wakao H, et al: Down-regulation of the invariant Vα14 antigen receptor in NKT cells upon activation. Int Immunol 2004;16:241-247.
45. Ulrich AP, Crowe NY, Kyparissoudis K, et al: NKT cell stimulation with glycolipid antigen in vivo: costimulation-dependent expansion, bim-dependent contraction, and hyporesponsiveness to further antigenic challenge. J Immunol 2005;175:3092-3101.
46. Hong S, Wilson MT, Serizawa I, et al: The natural killer T-cell ligand α-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat Med 2001;7:1052-1056.
47. Singh AK, Wilson MT, Hong S, et al: Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J Exp Med 2001;194:1801-1811.
48. Singh AK, Yang J-Q, Parekh VV, et al: The natural killer T cell ligand α-galactosylceramide prevents or promotes pristane-induced lupus in mice. Eur J Immunol 2005;35:1143-1154.
49. Hayakawa Y, Berzins SP, Crowe NY, Godfrey DI, Smyth MJ: Antigen-induced tolerance by intrathymic modulation of self-recognizing inhibitory receptors. Nat Immunol 2004;5:590-596.
50. Van Kaer L: α-Galactosylceramide therapy for autoimmune diseases: prospects and obstacles. Nat Rev Immunol 2005;5:31-42.
51. Cui J, Watanabe N, Kawano T, et al: Inhibition of T helper cell type 2 cell differentiation and immunoglobulin E response by ligand-activated Vα14 natural killer T cells. J Exp Med 1999;190:783-792.
52. + Treg cells in the prevention of autoimmune myasthenia. J Immunol 2005;175:7898-7904.
53. Mars LT, Novak J, Liblau RS, Lehuen A: Therapeutic manipulation of iNKT cells in autoimmunity: modes of action and potential risks. Trends Immunol 2004;25:471-476.
54. Parekh VV, Wilson MT, Van Kaer L: iNKT-cell responses to glycolipids. Crit Rev Immunol 2005;25:183-213.
55. Kotzin BL: Systemic lupus erythematosus. Cell 1996;85:303-306.
56. Singh RR: SLE: translating lessons from model systems to human disease. Trends Immunol 2005;26:572-579.
57. 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.
58. + NK T cells associated with disease development in autoimmune-prone mice. J Immunol 1996;156:4035-4040.
59. Oishi Y, Sumida T, Sakamoto A, et al: Selective reduction and recovery of invariant Vα24JαQ T cell receptor T cells in correlation with disease activity in patients with systemic lupus erythematosus. J Rheumatol 2001;28:275-283.
60. + NKT cell numbers are decreased in a wide variety of diseases that are characterized by autoreactive tissue damage. Clin Immunol 2001;100:144-148.
61. + double-negative regulatory natural killer T cells in autoimmune diseases. Arthritis Rheum 2001;44:1127-1138.
62. Yang J-Q, Saxena V, Xu H, Van Kaer L, Wang CR, Singh RR: Repeated α-galactosylceramide administration results in expansion of Vα14 NKT cells and alleviates inflammatory dermatitis in MRL-lpr/lpr mice. J Immunol 2003;171:4439-4446.
63. Yang JQ, Chun T, Liu H, et al: CD1d deficiency exacerbates inflammatory dermatitis in MRL-lpr/lpr mice. Eur J Immunol 2004;34:1723-1732.
64. Forestier C, Molano A, Im JS, et al: Expansion and hyperactivity of CD1d-restricted NKT cells during the progression of systemic lupus erythematosus in (New Zealand Black x New Zealand White)F1 mice. J Immunol 2005;175:763-770.
65. Zeng D, Liu Y, Sidobre S, Kronenberg M, Strober S: Activation of natural killer T cells in NZB/W mice induces Th1-type immune responses exacerbating lupus. J Clin Invest 2003;112:1211-1222.
66. Yang JQ, Singh AK, Wilson MT, et al: Immunoregulatory role of CD1d in the hydrocarbon oil-induced model of lupus nephritis. J Immunol 2003;171:2142-2153.
67. + T cells that promptly produce interleukin 4. Proc Natl Acad Sci USA 1995;92:11931-11934.
68. Garner B, Priestman DA, Stocker R, Harvey DJ, Butters TD, Platt FM: Increased glycosphingolipid levels in serum and aortae of apolipoprotein E gene knockout mice. J Lipid Res 2002;43:205-214.
69. Mukhin DN, Chao FF, Kruth HS: Glycosphingolipid accumulation in the aortic wall is another feature of human atherosclerosis. Arterioscl Thromb Vasc Biol 1995;15:1607-1615.
70. Melian A, Geng YJ, Sukhova GK, Libby P, Porcelli S: CD1 expression in human atherosclerosis. A potential mechanism for T cell activation by foam cells. Am J Pathol 1999;155:775-786.
71. Chan WL, Pejnovic N, Hamilton H, et al: Atherosclerotic abdominal aortic aneurysm and the interaction between autologous human plaque-derived vascular smooth muscle cells, type 1 NKT, and helper T cells. Circ Res 2005;96:675-683.
72. Bobryshev YV, Lord RS: Expression of heat shock protein-70 by dendritic cells in the arterial intima and its potential significance in atherogenesis. J Vasc Surg 2002;35:368-375.
73. Breslow JL: Mouse models of atherosclerosis. Science 1996;272:685-688.
74. Major AS, Wilson MT, McCaleb JL, et al: Quantitative and qualitative differences in proatherogenic NKT cells in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2004;24:2351-2357.
75. Nakai Y, Iwabuchi K, Fujii S, et al: Natural killer T cells accelerate atherogenesis in mice. Blood 2004;104:2051-2059.
76. 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;4:1230-1237.
77. Ostos MA, Recalde D, Zakin MM, Scott-Algara D: Implication of natural killer T cells in atherosclerosis development during a LPS-induced chronic inflammation. FEBS Lett 2002;519:23-29.
78. Major AS, Van Kaer L: The role of natural killer T cells in atherosclerosis. Curr Immunol Rev 2005;1:261-274.
79. Tupin E, Nicoletti A, Elhage R, et al: CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med 2004;199:417-422.
80. Aslanian AM, Chapman HA, Charo IF: Transient role for CD1d-restricted natural killer T cells in the formation of atherosclerotic lesions. Arterioscl Thromb Vasc Biol 2005;25:628-632.
81. King VL, Szilvassy SJ, Daugherty A: Interleukin-4 deficiency decreases atherosclerotic lesion formation in a site-specific manner in female LDL receptor-/- mice. Arterioscler Thromb Vasc Biol 2002;22:456-461.
82. Davenport P, Tipping PG: The role of interleukin-4 and interleukin-12 in the progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol 2003;163:1117-1125.