Natural killer T cells in lipoprotein metabolism and atherosclerosis

Godfrey S. Getz; Paul A. VanderLaan; Catherine A. Reardon

doi:10.1160/TH11-05-0336

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2011; 106(05): 814-819
DOI: 10.1160/TH11-05-0336

Theme Issue Article

Schattauer GmbH

Natural killer T cells in lipoprotein metabolism and atherosclerosis

Godfrey S. Getz

¹Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, Maastricht, the Netherlands

,

Paul A. VanderLaan

¹Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, Maastricht, the Netherlands

,

Catherine A. Reardon

¹Department of Molecular Genetics, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, Maastricht, the Netherlands

› Author Affiliations

Abstract

PDF Download

Summary

Cells of both the innate and adaptive immune system participate in the development of atherosclerosis, a chronic inflammatory disorder of medium and large arteries. Natural killer T (NKT) cells express surface markers characteristic of natural killer cells and conventional T cells and bridge the innate and adaptive immune systems. The development and activation of NKT cells is dependent upon CD1d, a MHC-class I-type molecule that presents lipids, especially glycolipids to the T cell receptors on NKT cells. There are two classes of NKT cells; invariant NKT cells that express a semi-invariant T cell receptor and variant NKT cells. This review summarises studies in murine models in which the effect of the activation, overexpression or deletion of NKT cells or only invariant NKT cells on atherosclerosis has been examined.

Keywords

Atherosclerosis - CD1d - NKT cells

PDF (135 kb)

References

References
1 Packard RR, Lichtman AH, Libby P. Innate and adaptive immunity in atherosclerosis. Semin Immunopathol 2009; 31: 5-22.
2 Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Rev Immunol 2011; 3: 204-221.
3 Getz GS, VanderLaan PA, Reardon CA. The immune system and murine atherosclerosis. Curr Drug Targets 2007; 8: 1297-1306.
4 Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol 2007; 25: 297-336.
5 Kronenberg M. Towards an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005; 26: 877-900.
6 Van Kaer L, Parekh VV, Wu L. Invariant natural killer T cells: bridging innate and adaptive immunity. Cell Tissue Res 2011; 343: 43-55.
7 Bobryshev YV, Lord RSA. Co-accumulation of dendritic cells and natural killer T cells within rupture-prone regions in human atherosclerotic plaques. J Histochem Cytochem 2005; 53: 781-785.
8 Garner B, Priestman DA, Stocker R. et al. Increased glycosphingolipid levels in serum and aortae of apolipoprotein E gene knockout mice. J Lipid Res 2002; 43: 205-214.
9 Kronenberg M, Gapin L. The unconventional lifestyle of NKT cells. Nat Rev Immunol 2002; 2: 557-568.
10 Berzins SP, Smyth MJ, Baxter AG. Presumed guilty: natural killer T cell defects and human disease. Nat Rev Immunol 2011; 11: 131-142.
11 Tupin E, Kinjo Y, Kronenberg M. The unique role of natural killer T cells in the response to microorganisms. Nat Rev Microbiol 2007; 5: 405-417.
12 Mallevaey T, Fontaine J, Breuilh L. et al. Invariant and noninvariant natural killer T cells exert opposite regulatory functions on the immune response during murine schistosomiasis. Infect Immun 2007; 75: 2171-2180.
13 Leadbetter EA, Brigl M, Illarionov P. et al. NK T cells provide lipid antigen-specific cognate help for B cells. Proc Natl Acad Sci USA 2008; 105: 8339-8344.
14 Lievens D, Eijgelaar WJ, Biessen EA. et al. The multi-functionality of CD40L and its receptor CD40 in atherosclerosis. Thromb Haemost 2009; 102: 206-214.
15 Gotsman I, Sharpe AH, Lichtman AH. T-cell costimulation and coinhibition in atherosclerosis. Circ Res 2008; 103: 1220-1231.
16 Kim S, Lalani S, Parekh VV, Wu L, Van Kaer L. Glycolipid ligands of invariant natural killer T cells as vaccine adjuvants. Expert Rev Vaccines. 2008; 7: 1519-1532.
17 Barral DC, Brenner MB. CD1 antigen presentation: how it works. Nat Rev Immunol 2007; 7: 929-41.
18 Zimmer MI, Nguyen HP, Wang B. et al. Polymorphisms in CD1d affect antigen presentation and the activation of CD1d-restricted T cells. Proc Natl Acad Sci USA 2009; 106: 1909-1914.
19 Yanaba K, Bouaziz JD, Haas KM. et al. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 2008; 28: 639-650.
20 Dougan SK, Kaser A, Blumberg RS. CD1 expression on antigen-presenting cells. Curr Top Microbiol Immunol 2007; 314: 113-141.
21 Lee WY, Moriarty TJ, Wong CH. et al. An intravascular immune response to Borrelia burgdorferi involves Kupffer cells and iNKT cells. Nat Immunol 2010; 11: 295-302.
22 Geissmann F, Cameron TO, Sidobre S. et al. Intravascular immune surveillance by CXCR6+ NKT cells patrolling liver sinusoids. PLoS Biol 2005; 3: e113
23 Lacasse J, Martin LH. Detection of CD1 mRNA in Paneth cells of the mouse intestine by in situ hybridization. J Histochem Cytochem. 1992; 40: 1527-1534.
24 Wingender G, Kronenberg M. Role of NKT cells in the digestive system: IV. The role of canonical natural killer T cells in mucosal immunity and infection. Am J Physiol Gastrointest Liver Physiol 2008; 294: G1-G8.
25 Nieuwenhuis EE, Matsumoto T, Lindenbergh D. et al. Cd1d-dependent regulation of bacterial colonization in the intestine of mice. J Clin Invest 2009; 119: 1241-1250.
26 Zhou D, Mattner J, Cantu C. 3rd,et al. Lysosomal glycosphingolipid recognition by NKT cells. Science 2004; 306: 1786-1789.
27 Speak AO, Salio M, Neville DC. et al. Implications for invariant natural killer T cell ligands due to the restricted presence of isoglobotrihexosylceramide in mammals. Proc Natl Acad Sci USA 2007; 104: 5971-5976.
28 Porubsky S, Speak AO, Luckow B. et al. Normal development and function of invariant natural killer T cells in mice with isoglobotrihexosylceramide (iGb3) deficiency. Proc Natl Acad Sci USA 2007; 104: 5977-5982.
29 VanderLaan PA, Reardon CA, Sagiv Y. et al. Characterization of the natural killer T-cell response in an adoptive transfer model of atherosclerosis. Am J Pathol 2007; 170: 1100-1107.
30 Shashkin P, Dragulev B, Ley K. Macrophage differentiation to foam cells. Curr Pharm Des 2005; 11: 3061-3072.
31 Liu Y, Teige A, Mondoc E. et al. Endogenous collagen peptide activation of CD1d-restricted NKT cells ameliorates tissue-specific inflammation in mice. J Clin Invest 2011; 121: 249-264.
32 van den Elzen P, Garg S, León L. et al. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005; 437: 906-910.
33 Allan LL, Hoefl K, Zheng DJ. et al. Apolipoprotein-mediated lipid antigen presentation in B cells provides a pathway for innate help by NKT cells. Blood 2009; 114: 2411-2416.
34 Miller YI, Viriyakosol S, Worrall DS. et al. Toll-like receptor 4-dependent and -independent cytokine secretion induced by minimally oxidized low-density lipoprotein in macrophages. Arterioscler Thromb Vasc Biol 2005; 25: 1213-1219.
35 Braun NA, Mendez-Fernandez YV, Covarrubias R. et al. Development of spontaneous anergy in invariant natural killer T cells in a mouse model of dyslipidemia. Arterioscler Thromb Vasc Biol 2010; 30: 1758-1765.
36 Nakai Y, Iwabuchi K, Fujii S. et al. Natural killer T cells accelerate atherogenesis in mice. Blood 2004; 104: 2051-2059.
37 Tupin E, Nicoletti A, Elhage R. et al. CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med 2004; 199: 417-422.
38 van Puijvelde GH, van Wanrooij EJ, Hauer AD. et al. Effect of natural killer T cell activation on the initiation of atherosclerosis. Thromb Haemost 2009; 102: 223-230.
39 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.
40 Bendelac A, Henniker RD, Lantz O. Increased interleukin 4 and immunoglobulin E production in transgenic mice over expressing NK1 T cells. J Exp Med 1996; 184: 1285-1293.
41 Reardon CA, Blachowicz L, Lukens J. et al. Genetic background selectively influences innominate artery atherosclerosis: immune system deficiency as a probe. Arterioscler Thromb Vasc Biol 2003; 23: 1449-1454.
42 Reardon CA, Blachowicz L, White T. et al. Effect of immune deficiency on lipoproteins and atherosclerosis in male apoprotein E deficient mice. Arterioscler Thromb Vasc Biol 2001; 21: 1011-1016.
43 Aslanian AM, Chapman HA, Charo IF. Transient role for CD1d-restricted natural killer T cells in the formation of atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2005; 25: 628-632.
44 Mendiratta SK, Martin WD, Hong S. et al. CD1d1 mutant mice are deficient in natural T cells that promptly produce IL-4. Immunity 1997; 6: 469-477.
45 Chen YH, Chiu NM, Manual M. et al. Impaired NK1+ T cell development and early IL-4 production in CD1- deficient mice. Immunity 1997; 6: 459-467.
46 Rogers L, Burchat S, Gage J. et al. Deficiency of invariant Vα14 natural killer T cells decreases atherosclerosis in LDL receptor null mice. Cardiovasc Res 2008; 78: 167-174.
47 Berzofsky JA, Terabe M. The contrasting roles of NKT cells in tumor immunity. Curr Mol Med 2009; 9: 667-672.
48 Binder CJ. Natural IgM antibodies against oxidation-specific epitopes. J Clin Immunol 2010; 30 (Suppl. 01) S56-60.
49 Bouaziz JD, Yanaba K, Tedder FR. Regulatory B cells as inhibitors of immune responses and inflammation. Immunol Rev 2008; 224: 201-244.
50 Felio K, Nguyen H, Dascher CC. et al. CD1-restricted adaptive immune responses to Mycobacteria in human group 1 CD1 transgenic mice. J Exp Med 2009; 206: 2497-2499.