Skip to main content
Log in

Role of apolipoproteins in ψδ and NKT cell-mediated innate immunity

  • Published:
Immunologic Research Aims and scope Submit manuscript

Abstract

Recent findings reveal unanticipated connections between the fields of lipid metabolism and immunology. They concern ψδ and NKT cells, nonconventional T cell populations that do not recognize protein antigens and are involved in immunity against cancer, defense against infections, or in regulation of classical immune responses. In this review, we summarize data linking perturbations of apolipoprotein levels and nonconventional T cells with inflammatory processes such as autoimmune diseases or atherosclerosis. We integrate and discuss recent findings on the implication of apolipoproteins in antigen recognition by ψδ and NKT cells, with emphasis on apolipoproteins A-I and E. These findings also provide indications that apolipoproteins influence antitumor immunosurveillance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Pennington DJ, Vermijlen D, Wise EL, et al: The integration of conventional and unconventional T cells that characterizes cell-mediated responses. Adv Immunol 2005;87:27–59.

    PubMed  Google Scholar 

  2. Hayday AC: ψδ cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 2000;18:975–1026.

    PubMed  CAS  Google Scholar 

  3. Kabelitz D, Wesch D: Features and functions of gamma delta T lymphocytes: focus on chemokines and their receptors. Crit Rev Immunol 2003;23:339–370.

    PubMed  CAS  Google Scholar 

  4. Kabelitz D, Marischen L, Oberg HH, et al: Epithelial defence by gamma delta T cells. Int Arch Allergy Immunol 2005;137:73–81.

    PubMed  CAS  Google Scholar 

  5. Hayday A, Theodoridis E, Ramsburg E, et al: Intraepithelial lymphocytes: exploring the Third Way in immunology. Nat Immunol 2001;2:997–1003.

    PubMed  CAS  Google Scholar 

  6. Holtmeier W: Compartmentalization gamma/delta T cells and their putative role in mucosal immunity. Crit Rev Immunol 2003;23:473–488.

    PubMed  Google Scholar 

  7. Girardi M: Cutaneous biology of gammadelta T cells. Adv Dermatol 2004;20:203–215.

    PubMed  Google Scholar 

  8. Carding SR, Egan PJ: Gammadelta T cells: functional plasticity and heterogeneity. Nat Rev Immunol 2002;2:336–345.

    PubMed  CAS  Google Scholar 

  9. Porcelli S, Brenner MB, Band H: Biology of the human gamma delta T-cell receptor. Immunol Rev 1991;120:137–183.

    PubMed  CAS  Google Scholar 

  10. Heilig JS, Tonegawa S: Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 1986;322:836–840.

    PubMed  CAS  Google Scholar 

  11. Kunzmann V, Wilhelm M: Anti-lymphoma effect of gammadelta T cells. Leuk Lymphoma 2005;46:671–680.

    PubMed  CAS  Google Scholar 

  12. Viey E, Fromont G, Escudier B, et al: Phosphostim-activated gamma delta T cells kill autologous metastatic renal cell carcinoma. J Immunol 2005;174:1338–1347.

    PubMed  CAS  Google Scholar 

  13. Corvaisier M, Moreau-Aubry A, Diez E, et al: V gamma 9V delta 2 T cell response to colon carcinoma cells. J Immunol 2005;175:5481–5488.

    PubMed  CAS  Google Scholar 

  14. Zocchi MR, Poggi A: Role of gammadelta T lymphocytes in tumor defense. Front Bio 2004;9:2588–2604.

    CAS  Google Scholar 

  15. Ziegler HK: The role of gamma/delta T cells in immunity to infection and regulation of inflammation. Immunol Res 2004;29:293–302.

    PubMed  CAS  Google Scholar 

  16. Halary F, Peyrat MA, Champagne E, et al: Control of self-reactive cytotoxic T lymphocytes expressing gamma delta T cell receptors by natural killer inhibitory receptors. Eur J Immunol 1997;27:2812–2821.

    PubMed  CAS  Google Scholar 

  17. Vivier E, Anfossi N: Inhibitory NK-cell receptors on T cells: witness of the past, actors of the future. Nat Rev Immunol 2004;4:190–198.

    PubMed  CAS  Google Scholar 

  18. Groh V, Rhinehart R, Secrist H, et al: Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 1999;96:6879–6884.

    PubMed  CAS  Google Scholar 

  19. Cerwenka A, Lanier LL: NKG2D ligands: unconventional MHC class I-like molecules exploited by viruses and cancer. Tissue Antigens 2003;61:335–343.

    PubMed  CAS  Google Scholar 

  20. Girardi M, Hayday AC: Immunosurveillance by gammadelta T cells: focus on the murine system. Chem Immunol Allergy 2005;86:136–150.

    PubMed  CAS  Google Scholar 

  21. Bonneville M, Fournie JJ: Sensing cell stress and transformation through V gamma9V delta2 T cell-mediated recognition of the isoprenoid pathway metabolites. Microbes Infect 2005;7:503–509.

    PubMed  CAS  Google Scholar 

  22. Ismaili J, Olislagers V, Poupot R, et al: Human gamma delta T cells induce dendritic cell maturation. Clin Immunol 2002;103:296–302.

    PubMed  CAS  Google Scholar 

  23. Jameson JM, Sharp LL, Witherden DA, Havran WL: Regulation of skin cell homeostasis by gamma delta T cells. Front Biosci 2004;9:2640–2651.

    PubMed  CAS  Google Scholar 

  24. Yang H, Antony PA, Wildhaber BE, Teitelbaum DH: Intestinal intraepithelial lymphocyte gamma delta-T cell-derived keratinocyte growth factor modulates epithelial growth in the mouse. J Immunol 2004;172:4151–4158.

    PubMed  CAS  Google Scholar 

  25. Workalemahu G, Foerster M, Kroegel C: Expression and synthesis of fibroblast growth factor-9 in human {gamma} {delta} T-lymphocytes. Response to isopentenyl pyrophosphate and TGF-β 1/IL-15. J Leukoc Biol 2004;75:657–663.

    PubMed  CAS  Google Scholar 

  26. Taguchi A, Miyazaki M, Sakuragi S, et al: Gamma/delta T cell lymphoma. Intern Med 2004;43:120–125.

    Google Scholar 

  27. Haas W, Pereira P, Tonegawa S: Gamma/delta cells. Annu Rev Immunol 1993;11:637–685.

    PubMed  CAS  Google Scholar 

  28. Hayday A, Tigelaar R: Immunoregulation in the tissues by gammadelta T cells. Nat Rev Immunol 2003;3:233–242.

    PubMed  CAS  Google Scholar 

  29. Adams EJ, Chien YH, Garcia KC: Structure of a gammadelta T cell receptor in complex with the nonclassical MHC T22. Science 2005;308:227–231.

    PubMed  CAS  Google Scholar 

  30. Shin S, El-Diwany R, Schaffert S, et al: Antigen recognition determinants of gammadelta T cell receptors. Science 2005;308:252–255.

    PubMed  CAS  Google Scholar 

  31. Spada FM, Grant EP, Peters PJ, et al: Self-recognition of CD1 by gamma/delta T cells: implications for innate immunity. J Exp Med 2000;191:937–948.

    PubMed  CAS  Google Scholar 

  32. Bukowski JF, Morita CT, Band H, et al: Crucial role of TCR gamma chain junctional region in prenyl pyrophosphate antigen recognition by gamma delta T cells. J Immunol 1998;161:286–293.

    PubMed  CAS  Google Scholar 

  33. Poupot M, Fournie JJ: Non-peptide antigens activating human Vgamma9/V delta2 T lymphocytes. Immunol Lett 2004;95:129–138.

    PubMed  CAS  Google Scholar 

  34. Green AE, Lissina A, Hutchinson SL, et al: Recognition of nonpeptide antigens by human V gamma 9V delta 2 T cells requires contact with cells of human origin. Clin Exp Immunol 2004;136:472–482.

    PubMed  CAS  Google Scholar 

  35. Rojas RE, Torres M, Fournie JJ, et al: Phosphoantigen presentation by macrophages to mycobacterium tuberculosis-reactive V gamma9V delta2+ T cells: modulation by chloroquine. Infect Immunol 2002;70:4019–4027.

    CAS  Google Scholar 

  36. Gober HJ, Kistowska M, Angman L, et al: Human T cell receptor gammadelta cells recognize endogenous mevalonate metabolites in tumor cells. J Exp Med 2003;197:163–168.

    PubMed  CAS  Google Scholar 

  37. Das H, Wang L, Kamath A, et al: Vgamma2V delta2 T-cell receptor-mediated recognition of aminobisphosphonates. Blood 2001;98:1616–1618.

    PubMed  CAS  Google Scholar 

  38. Kunzmann V, Bauer E, Feurle J, et al: Stimulation of gamma delta T cells by aminobisphosphonates and induction of antiplasma cell activity in multiple myeloma. Blood 2000;96:384–392.

    PubMed  CAS  Google Scholar 

  39. Bergstrom JD, Bostedor RG, Masarachia PJ, et al: Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase. Arch Biochem Biophys 2000;373:231–241.

    PubMed  CAS  Google Scholar 

  40. Thompson K, Rogers MJ: Statins prevent bisphosphonate-induced gamma, delta-T-cell proliferation and activation in vitro. J Bone Miner Res 2004;19:278–288.

    PubMed  CAS  Google Scholar 

  41. Bukowski JF, Morita CT, Brenner MB: Human gamma delta T cells recognize alkylamines derived from microbes, edible plants, and tea: implications for innate immunity. Immunity 1999;11:57–65.

    PubMed  CAS  Google Scholar 

  42. Thompson K, Rojas-Navea J, Rogers MJ: Alkylamines cause V {gamma} 9V {delta} 2 T-cell activation and proliferation by inhibiting the mevalonate pathway. Blood 2005.

  43. Haregewoin A, Soman G, Hom RC, et al: Human gamma delta+ T cells respond to mycobacterial heatshock protein. Nature 1989;340:309–312.

    PubMed  CAS  Google Scholar 

  44. Fisch P, Malkovsky M, Kovats S, et al: Recognition by human V gamma 9/V delta 2 T cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science 1990;250:1269–1273.

    PubMed  CAS  Google Scholar 

  45. Kaur I, Voss SD, Gupta RS, et al: Human peripheral gamma delta T cells recognize hsp60 molecules on Daudi Burkitt's lymphoma cells. J Immunol 1993;150:2046–2055.

    PubMed  CAS  Google Scholar 

  46. Laad AD, Thomas ML, Fakih AR, Chiplunkar SV: Human gamma delta T cells recognize heat shock protein-60 on oral tumor cells. Int J Cancer 1999;80:709–714.

    PubMed  CAS  Google Scholar 

  47. Kabelitz D, Bender A, Schondelmaier S, et al: A large fraction of human peripheral blood gamma/delta+ T cells is activated by Mycobacterium tuberculosis but not by its 65-kD heat shock protein. J Exp Med 1990;171:667–679.

    PubMed  CAS  Google Scholar 

  48. Constant P, Davodeau F, Peyrat MA, et al: Stimulation of human gamma delta T cells by nonpeptidic mycobacterial ligands. Science 1994;264:267–270.

    PubMed  CAS  Google Scholar 

  49. Scotet E, Martinez LO, Grant E, et al: Tumor recognition following V gamma9V delta2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity 2005;22:71–80.

    PubMed  CAS  Google Scholar 

  50. Martinez LO, Jacquet S, Esteve JP, et al: Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 2003;421:75–79.

    PubMed  CAS  Google Scholar 

  51. Papamichail M, Perez SA, Gritzapis AD, Baxevanis CN: Natural killer lymphocytes: biology, development, and function. Cancer Immunol Immunother 2004;53:176–186.

    PubMed  Google Scholar 

  52. Kronenberg M: Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005;26:877–900.

    Google Scholar 

  53. Coles MC, Raulet DH: NK1.1+T cells in the liver arise in the thymus and are selected by interactions with class I molecules on CD4+CD8+ cells. J Immunol 2000;164:2412–2418.

    PubMed  CAS  Google Scholar 

  54. Gapin L, Matsuda JL, Surh CD, Kronenberg M: NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat Immunol 2001; 2: 971–978.

    PubMed  CAS  Google Scholar 

  55. Wei, DG, Lee, H, Park, SH, et al: Expansion and long-range differentiation of the NKT cell lineage in mice expressing CD1d exclusively on cortical thymocytes. J Exp Med 2005; 239–248.

  56. Matsuda JL, Kronenberg M: Presentation of self and microbial lipids by CD1 molecules. Curr Opin Immunol 2001; 13: 19–25.

    PubMed  CAS  Google Scholar 

  57. Metelitsa LS, Naidenko OV, Kant A, et al.: Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J Immunol 2001; 167: 3114–3122.

    PubMed  CAS  Google Scholar 

  58. Fuss IJ, Heller F, Boirivant M, et al: Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. J Clin Invest 2004; 113: 1490–1497.

    PubMed  CAS  Google Scholar 

  59. Numata Y, Tazuma S, Nishioka T, et al: Immune response in mouse experimental cholangitis associated with colitis induced by dextran sulfate sodium. J Gastroenterol Hepatol 2004; 19: 910–915.

    PubMed  Google Scholar 

  60. Miyamoto K, Miyake S, Yamamura T: A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 2001; 413: 531–534.

    PubMed  CAS  Google Scholar 

  61. Miyake S, Yamamura T: Therapeutic potential of glycolipid ligands for natural killer (NK) T cells in the suppression of autoimmune diseases. Curr Drug Targets Immune Endocr Metabol Disord 2005; 5: 315–322.

    PubMed  CAS  Google Scholar 

  62. Griseri, T, Beaudoin, L, Novak, J, et al: Invariant NKT cells exacerbate type 1 diabetes induced by CD8 T cells. J Immunol 2005; 175: 2091–2101.

    PubMed  CAS  Google Scholar 

  63. Smyth MJ, Crowe NY, Hayakawa Y, et al: NKT cells—conductors of tumor immunity? Curr Opin Immunol 2002; 14: 165–171.

    PubMed  CAS  Google Scholar 

  64. Beaudoin, L, Laloux V, Novak, J, et al.: NKT cells inhibit the onset of diabetes by impairing the development of pathogenic T cells specific for pancreatic beta cells. Immunity 2002; 17: 725–736.

    PubMed  CAS  Google Scholar 

  65. Spada FM, Koezuka Y, Porcelli SA: CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J Exp Med 1998; 188: 1529–1534.

    PubMed  CAS  Google Scholar 

  66. Nakai, Y, Iwabuchi, K, Fujii, S, et al: Natural killer T cells accelerate atherogenesis in mice. Blood 2004; 104: 2051–2059.

    PubMed  CAS  Google Scholar 

  67. Zhou D, Mattner J, Cantu C, 3rd, et al: Lysosomal glycosphingolipid recognition by NKT cells. Science 2004; 306: 1786–1789.

    PubMed  CAS  Google Scholar 

  68. Gumperz JE, Roy C, Makowska A, et al: Murine CD1d-restricted T cell recognition of cellular lipids. Immunity 2000; 12: 211–221.

    PubMed  CAS  Google Scholar 

  69. Rauch J, Gumperz J, Robinson C, et al: Structural features of the acyl chain determine self-phospholipid antigen receognition by a CD1d-restricted invariant NKT (iNKT) cell. J Biol Chem 2003; 278: 47508–47515.

    PubMed  CAS  Google Scholar 

  70. 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.

    PubMed  CAS  Google Scholar 

  71. van den Elzen P, Garg S, Leon, L, et al: Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005; 437: 906–910.

    PubMed  Google Scholar 

  72. Zhou D, Cantu C, III, Sagiv Y, et al: Editing of CD1d-bound lipid antigens by endosomal lipid transfer proteins. Science 2004; 303: 523–527.

    PubMed  CAS  Google Scholar 

  73. Brozovic S, Nagaishi T, Yoshida M, et al: CD1d function is regulated by microsomal triglyceride transfer protein. Nat Med 2004; 10: 535–539.

    PubMed  CAS  Google Scholar 

  74. Shoulders CC, Shelness GS: Current biology of MTP: implications for selective inhibition. Curr Top Med Chem 2005; 5: 283–300.

    PubMed  CAS  Google Scholar 

  75. Hansson GK: Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685–1695.

    PubMed  CAS  Google Scholar 

  76. Ross R: Atherosclerosis—an inflammatory disease. N Engl J Med 1999; 340: 115–126.

    PubMed  CAS  Google Scholar 

  77. Curtiss LK, Boisvert WA: Apolipoprotein E and atherosclerosis. Curr Opin Lipidol 2000; 11: 243–251.

    PubMed  CAS  Google Scholar 

  78. Chait A, Han CY, Oram JF, Heinecke JW: Thematic review series: the immune system and atherogenesis. Lipoprotein-associated inflammatory proteins: markers or mediators of cardiovascular disease? J Lipid Res 2005; 46: 389–403.

    PubMed  CAS  Google Scholar 

  79. Mahley RW: Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 1988; 240: 622–630.

    PubMed  CAS  Google Scholar 

  80. Ribalta J, Vallve JC, Girona J, Masara L: Apolipoprotein and apolipoprotein receptor genes, blood lipids and disease. Curr Opin Clin Nutr Metab Care 2003; 6: 177–187.

    PubMed  CAS  Google Scholar 

  81. Boisvert WA, Spangenberg J, Curtiss LK: Treatment of severe hypercholesterolemia in apolipoprotein E-deficient mice by bone marrow transplantation. J Clin Invest 1995; 96: 1118–1124.

    PubMed  CAS  Google Scholar 

  82. Linton MF, Atkinson JB, Fazio S: Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science 1995; 267: 1034–1037.

    PubMed  CAS  Google Scholar 

  83. Van Eck M, Herijgers N, Yates J, et al: Bone marrow transplantation in apolipoprotein E-deficient mice. Effect of ApoE gene dosage on serum lipid concentrations, (beta) VLDL catabolism, and atherosclerosis. Arterioscler Thromb Vasc Biol 1997; 17: 3117–3126.

    PubMed  Google Scholar 

  84. Piedrahita JA, Zhang SH, Hagaman JR, et al: Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 1992; 89: 4471–4475.

    PubMed  CAS  Google Scholar 

  85. Fazio S, Babaev VR, Murray AB, et al: Increased atherosclerosis in mice reconstituted with apolipoprotein E null macrophages. Proc Natl Acad Sci USA 1997; 94: 4647–4652.

    PubMed  CAS  Google Scholar 

  86. Boisvert WA, Spangenberg J, Curtiss LK: Role of leukocyte-specific LDL receptors on plasma lipoprotein cholesterol and atherosclerosis in mice. Arterioscler Thromb Vasc Biol 1997; 17: 340–347.

    PubMed  CAS  Google Scholar 

  87. Linton MF, Babaev, VR, Gleaves LA, Fazio S: A direct role for the macrophage low density lipoprotein receptor in atherosclerotic lesion formation. J Biol Chem 1999; 274: 19204–19210.

    PubMed  CAS  Google Scholar 

  88. Connelly MA, Williams DL: Scavenger receptor BI: a scavenger receptor with a mission to transport high density lipoprotein lipids. Curr Opin Lipidol 2004; 15: 287–295.

    PubMed  CAS  Google Scholar 

  89. Karackattu SL, Picard MH, Krieger M: Lymphocytes are not required for the rapid onset of coronary heart disease in scavenger receptor class B type I/apolipoprotein E double knockout mice. Arterioscler Thromb Vasc Biol 2005; 25: 803–808.

    PubMed  CAS  Google Scholar 

  90. Witztum JL, Palinski W: Are immunological mechanisms relevant for the development of atherosclerosis? Clin Immunol 1999; 90: 153–156.

    PubMed  CAS  Google Scholar 

  91. Moeller F, Nielsen LB: Aortic recruitment of blood lymphocytes is most pronounced in early stages of lesion formation in apolipoprotein-E-deficient mice. Atherosclerosis 2003; 168: 49–56.

    PubMed  CAS  Google Scholar 

  92. Paulsson G, Zhou X, Tornquist E, et al: Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2000; 20: 10–17.

    PubMed  CAS  Google Scholar 

  93. Elhage R, Gourdy P, Brouchet L, et al: Deleting TCR alpha beta+ or CD4+ T lymphocytes leads to opposite effects on site-specific atherosclerosis in female apolipoprotein E-deficient mice. Am J Pathol 2004; 165: 2013–2018.

    PubMed  Google Scholar 

  94. Ostos MA, Recalde D, Zakin MM, Scott-Atgara D: Implication of natural killer T cells in atherosclerosis development during a LPS-induced chronic inflammation. FEBS Lett 2002; 519: 23–29.

    PubMed  CAS  Google Scholar 

  95. 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.

    PubMed  CAS  Google Scholar 

  96. Nakai Y, Iwabuchi K, Fujii S, et al: Natural killer T cells accelerate atherogenesis in mice. Blood 2004; 104: 2051–2059.

    PubMed  CAS  Google Scholar 

  97. Tupin E, Nicoletti A, Elhage R, et al: CD1d-dependent activation of NKT cells aggravates atherosclerosis. J Exp Med 2004; 199: 417–422.

    PubMed  CAS  Google Scholar 

  98. Peiser L, Mukhopadhyay S, Gordon S: Scavenger receptors in innate immunity. Curr Opin Immunol 2002; 14: 123–128.

    PubMed  CAS  Google Scholar 

  99. Laskowitz DT, Lee DM, Schmechel D, Staats HF: Altered immune responses in apolipoprotein E-deficient mice. J Lipid Res 2000; 41: 613–620.

    PubMed  CAS  Google Scholar 

  100. Karussis D, Michaelson DM, Grigoriadis N, et al: Lack of apolipoprotein-E exacerbates experimental allergic encephalomyelitis. Mult Scler 2003; 9: 476–480.

    PubMed  CAS  Google Scholar 

  101. Ludewig B, Jaggi M, Dumrese T, et al: Hypercholesterolemia exacerbates virus-induced immunopathologic liver disease via suppression of antiviral cytotoxic T cell responses. J Immunol 2001; 166: 3369–3376.

    PubMed  CAS  Google Scholar 

  102. Fazekas F, Strasser-Fuchs S, Kollegger H, et al: Apolipoprotein E epsilon 4 is associated with rapid progression of multiple sclerosis. Neurology 2001; 57: 853–857.

    PubMed  CAS  Google Scholar 

  103. Schmidt S, Barcellos LF, DeSombre K, et al: Association of polymorphisms in the apolipoprotein E region with susceptibility to and progression of multiple sclerosis. Am J Hum Genet 2002; 70: 708–717.

    PubMed  CAS  Google Scholar 

  104. Tenger C, Zhou X: Apolipoprotein E modulates immune activation by acting on the antigen-presenting cell. Immunology 2003; 109: 392–397.

    PubMed  CAS  Google Scholar 

  105. Martinez LO, Jacquet S, Terce F, et al: New insight on the molecular mechanisms of high-density lipoprotein cellular interactions. Cell Mol Life Sci 2004; 61: 2343–2360.

    PubMed  CAS  Google Scholar 

  106. Chambenoit O, Hamon Y, Marguet D, et al: Specific docking of apolipoprotein A-I at the cell surface requires a functional ABCA1 transporter. J Biol Chem 2001; 276: 9955–9960.

    PubMed  CAS  Google Scholar 

  107. Fidge NH: High density lipoprotein receptors, binding proteins, and ligands. J Lipid Res 1999; 40: 187–201.

    PubMed  CAS  Google Scholar 

  108. Hidaka H, Hidaka E, Tozuka M, et al: The identification of specific high density lipoprotein 3 binding sites on human blood monocytes using fluorescence-labeled ligand. J Lipid Res 1999; 40: 1131–1139.

    PubMed  CAS  Google Scholar 

  109. Bocharov AV, Vishnyakova TG, Baranova IN, et al: Characterization of a 95 kDa high affinity human high density lipoprotein-binding protein. Biochemistry 2001; 40: 4407–4416.

    PubMed  CAS  Google Scholar 

  110. Kozyraki R, Fyfe J, Kristiansen M, et al: The intrinsic factor-vitamin B12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of high-density lipoprotein. Nat Med 1999; 5: 656–661.

    PubMed  CAS  Google Scholar 

  111. Hara H, Yokoyama S: Interaction of free apolipoproteins with macrophages. Formation of high density lipoprotein-like lipoproteins and reduction of cellular cholesterol. J Biol Chem 1991; 266: 3080–3086.

    PubMed  CAS  Google Scholar 

  112. Franceschini, G: Apolipoprotein function in health and disease: insights from natural mutations. Eur J Clin Invest 1996; 26: 733–746.

    PubMed  CAS  Google Scholar 

  113. Hyka N, Dayer JM, Modoux C, et al: Apolipoprotein A-I inhibits the production of interleukin-1 beta and tumor necrosis factor-alpha by blocking contact-mediated activation of monocytes by T lymphocytes. Blood 2001; 97: 2381–2389.

    PubMed  CAS  Google Scholar 

  114. Schaefer EJ, Kay LL, Zech LA, Brewer Jr, HB: Tangier disease. High density lipoprotein deficiency due to defective metabolism of an abnormal apolipoprotein A-i (ApoA-ITangier). J Clin Invest 1982; 70: 934–945.

    PubMed  CAS  Google Scholar 

  115. Ng DS, Leiter LA, Vezina C, et al: Apolipoprotein A-I Q[-2]X causing isolated apolipoprotein A-I deficiency in a family with an alphalipoproteinemia. J Clin Invest 1994; 93: 223–229.

    PubMed  CAS  Google Scholar 

  116. Rubin EM, Krauss RM, Spangler EA, et al: Inhibition of early atherogenesis in transgenic mice by human apolipoprotein AI. Nature 1991; 353: 265–267.

    PubMed  CAS  Google Scholar 

  117. Tangirala RK, Tsukamoto K, Chun SH, et al: Regression of atherosclerosis induced by liver-directed gene transfer of apolipoprotein A-I in mice. Circulation 1999; 100: 1816–1822.

    PubMed  CAS  Google Scholar 

  118. Hughes SD, Verstuyft J, Rubin EM: HDL deficiency in genetically engineered mice requires elevated LDL to accelerate atherogenesis. Atherioscler Thromb Vasc Biol 1997; 17: 1725–1729.

    CAS  Google Scholar 

  119. Burger D, Dayer JM: The role of human T-lymphocyte-monocyte contact in inflammation and tissue destruction. Autoimmun Rev 2002;4 Suppl 3: S169–176.

    Google Scholar 

  120. Burger D, Dayer JM: High-density lipoprotein-associated apolipoprotein A-I: the missing link between infection and chronic inflmmation? Autoimmun Rev 2002;1:111–117.

    PubMed  CAS  Google Scholar 

  121. Doherty NS, Littman BH, Reilly K, et al.: Analysis of changes in acute-phase plasma proteins in an acute inflammatory response and in rheumatoid arthritis using two-dimensional gel electrophoresis. Electrophoresis 1998;19:355–363.

    PubMed  CAS  Google Scholar 

  122. Lakatos J, Harsagyi A: Serum total, HDL, LDL cholesterol, and triglyceride levels in patients with rheumatoid arthritis. Clin Biochem 1988;21:93–96.

    PubMed  CAS  Google Scholar 

  123. Park YB, Lee SK, Lee WK, et al.: Lipid profiles in untreated patients with rheumatoid arthritis. J Rheumatol 1999;26:1701–1704.

    PubMed  CAS  Google Scholar 

  124. Tselepis AD, Elisaf M, Besis S, et al.: Association of the inflammatory state in active juvenile rheumatoid arthritis with hypo-high-density lipoproteinemia and reduced lipoprotein-associated platelet-activating factor acetylhydrolase activity. Arthritis Rheum 1999;42:373–383.

    PubMed  CAS  Google Scholar 

  125. Ananth L, Prete PE, Kashyap ML: Apolipoproteins A-I and B and cholesterol in synovial fluid of patients with rheumatoid arthritis. Metabolism 1993;42: 803–806.

    PubMed  CAS  Google Scholar 

  126. Bresnihan B, Gogarty M, Fitzgerald O, et al.: Apolipoprotein A-I infiltration in rheumatoid arthritis synovial tissue: a control mechanism of cytokine production? Arthritis Res Ther 2004;6:R563-R566.

    CAS  Google Scholar 

  127. Dinu AR, Merrill JT, Shen C, et al.: Frequency of antibodies to the cholesterol transport protein apolipoprotein A1 in patients with SLE. Lupus 1998;7:355–360.

    PubMed  CAS  Google Scholar 

  128. Sena A, Pedrosa R, Ferret-Sena V, et al.: Interferon betala therapy changes lipoprotein metabolism in patients with multiple sclerosis. Clin Chem Lab Med 2000;38:209–213.

    PubMed  CAS  Google Scholar 

  129. Ashby DT, Rye KA, Clay MA, et al.: Factors influencing the ability of HDL to inhibit expression of vascular cell adhesion molecule-l in endothelial cells. Arterioscler Thromb Vasc Biol 1998;18:1450–1455.

    PubMed  CAS  Google Scholar 

  130. Rossol M, Hantzschel H, Wagner U: [T cell-dependent monocyte activation, TNFalpha and apolipoprotein A-I in autoimmunity and inflammation]. Z Rheumatol 2005;64:249–254.

    PubMed  CAS  Google Scholar 

  131. Freedman MS, Bitar R, Antel JP: Gamma-delta T-cell-human glial cell interactions. II. Relationship between heat shock protein expression and susceptibility to cytolysis. J Neuroimmunol 1997;74:143–148.

    PubMed  CAS  Google Scholar 

  132. Liedtke W, Meyer G, Faustmann PM, et al.: Clonal expansion and decreased occurrence of peripheral blood gamma delta T cells of the V delta 2J delta 3 lineage in multiple sclerosis patients. Int Immunol 1997; 9:1031–1041.

    PubMed  CAS  Google Scholar 

  133. Yamamoto T, Hara T, Nanba E, et al.: Abnormal expansion of peripheral gamma delta T cells in patients with neurologic disorders. Brain Behav Immun 1997;11: 157–166.

    PubMed  CAS  Google Scholar 

  134. Wiendl H, Malotka J, Holzwarth B, et al.: An autoreactive gamma delta TCR derived from a polymositis lesion. J Immunol 2002;169:515–521.

    PubMed  CAS  Google Scholar 

  135. Roura-Mir IC, Alcalde L, Vargas F, et al.: Gamma delta lymphocytes in endocrine autoimmunity: evidence of expansion in Graves' disease but not in type 1 diabetes. Clin Exp Immunol 1993;92:288–295.

    PubMed  CAS  Google Scholar 

  136. Holoshitz J: Activation of gammadelta T cells by mycobacterial antigens in rheumatoid arthritis. Microbes Infect 1999;1:197–202.

    PubMed  CAS  Google Scholar 

  137. Kapp JA, Kapp LM, McKenna KC: Gammadelta T cells play an essential role in several forms of tolerance. Immunol Res 2004;29:93–102.

    PubMed  CAS  Google Scholar 

  138. Kapp JA, Kapp LM, McKenna KC, Lake JP: Gammadelta T-cell clones from intestinal intraepithelial lymphocytes inhibit development of CTL responses ex vivo. Immunology 2004;111:155–164.

    PubMed  CAS  Google Scholar 

  139. Mincheva-Nilsson L: Pregnancy and gamma/delta T cells: taking on the hard questions. Reprod Biol Endocrinol 2003;1:120.

    PubMed  Google Scholar 

  140. Holt PG, Sly PD: gammadelta T cells provide a breath of fresh air for asthma research. Nat Med 1999;5: 1127–1128.

    PubMed  CAS  Google Scholar 

  141. Lahn M: The role of gammadelta T cells in the airways. J Mol Med 2000;78:409–425.

    PubMed  CAS  Google Scholar 

  142. Ponomarev ED, Novikova M, Yassai M, et al.: Gamma delta T cell regulation of IFN-gamma production by central nervous system-infiltrating encephalitogenic T cells: correlation with recovery from experimental autoimmune encephalomyelitis. J Immunol 2004;173: 1587–1595.

    PubMed  CAS  Google Scholar 

  143. Girardi M, Lewis J, Glusac E, et al.: Resident skin-specific gammadelta T cells provide local, nonredundant regulation of cutaneous inflammation. J Exp Med 2002;195:855–867.

    PubMed  CAS  Google Scholar 

  144. Hoffmann JC, Peters K, Henschke S, et al.: Role of T lymphocytes in rat 2,4,6-trinitrobenzene sulphonic acid (TNBS) induced colitis: increased mortality after gammadelta T cell depletion and no effect of alphabeta T cell depletion. Gut 2001;48:489–495.

    PubMed  CAS  Google Scholar 

  145. Guan H, Zu G, Slater M, et al.: Gammadelta T cells regulate the development of hapten-specific CD8+effector T cells in contact hypersensitivity responses. J Invest Dermatol 2002;119:137–142.

    PubMed  CAS  Google Scholar 

  146. Egan PJ, Carding SR: Downmodulation of the inflammatory response to bacterial infection by gammadelta T cells cytotoxic for activated macrophages. J Exp Med 2000;191:2145–2158.

    PubMed  CAS  Google Scholar 

  147. Fahrer AM, Konigshofer Y, Kerr EM, et al.: Attributes of gammadelta intraepithelial lymphocytes as suggested by their transcriptional profile. Proc Natl Acad Sci USA 2001;98:10261–10266

    PubMed  CAS  Google Scholar 

  148. Meissner N, Radke J, Hedges JF, et al.: Serial analysis of gene expression in circulating gamma delta T cell subsets defines distinct immunoregulatory phenotypes and unexpected gene expression profiles. J Immunol 2003;170:356–364.

    PubMed  CAS  Google Scholar 

  149. Shires J, Theodoridis E, Hayday AC: Biological insights into TCR gammadelta+ and TCRalphabeta+intraepithelial lymphocytes provided by serial analysis of gene expression (SAGE). Immunity 2001;15: 419–434.

    PubMed  CAS  Google Scholar 

  150. Brandes M, Willimann K, Moser B: Professional antigen-presentation function by human gammadelta T Cells. Science 2005;309:264–268.

    PubMed  CAS  Google Scholar 

  151. Born WK, Vollmer M, Reardon C, et al.: Hybridomas expressing gammadelta T-cell receptors respond to cardiolipin and beta2-glycoprotein 1 (apolipoprotein H). Scand J Immunol 2003;58:374–381.

    PubMed  CAS  Google Scholar 

  152. Recalde D, Ostos MA, Badell E, et al: Human apolipoprotein A-IV reduces secretion of proinflammatory cytokines and atherosclerotic effects of a chronic infection mimicked by lipopolysaccharide. Arterioscler Thromb Vasc Biol 2004;24:756–761.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Champagne, E., Martinez, L.O., Vantourout, P. et al. Role of apolipoproteins in ψδ and NKT cell-mediated innate immunity. Immunol Res 33, 241–255 (2005). https://doi.org/10.1385/IR:33:3:241

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/IR:33:3:241

Key Words

Navigation