NKT cells stimulated by long fatty Acyl chain sulfatides significantly reduces the incidence of type 1 diabetes in nonobese diabetic mice

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Subramanian, Lakshmimathy ^a,b   Blumenfeld, Hartley ^a,b   Tohn, Robert ^a,b   Ly, Dalam ^a,b,c   Aguilera, Carlos ^d   Maricic, Igor ^d   Mansson, Jan Eric ^e   Buschard, Karsten ^f   Kumar, Vipin ^d   Delovitch, Terry L ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

^e SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^f Rigshospitalet   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; SULFATIDE; CD1D ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL STIMULATION; CELL TRANSFER; CELL TYPE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DENDRITIC CELL; DRUG EFFICACY; INSULIN DEPENDENT DIABETES MELLITUS; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER CELL; NONHUMAN; TREATMENT RESPONSE; ANIMAL; CYTOLOGY; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; LYMPH NODE; METABOLISM; MOUSE MUTANT; NATURAL KILLER T CELL; NONOBESE DIABETIC MOUSE; PANCREAS; SECRETION (PROCESS); STRUCTURE ACTIVITY RELATION;

MUS;

ANIMALS; ANTIGENS, CD1D; CD4-POSITIVE T-LYMPHOCYTES; DIABETES MELLITUS, TYPE 1; FLOW CYTOMETRY; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKIN-4; LYMPH NODES; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; PANCREAS; STRUCTURE-ACTIVITY RELATIONSHIP; SULFOGLYCOSPHINGOLIPIDS;

EID: 84861384875     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037771     Document Type: Article

References (50)

1. Fredman P, Mansson JE, Rynmark BM, Josefsen K, Ekblond A, et al. (2000) The glycosphingolipid sulfatide in the islets of Langerhans in rat pancreas is processed through recycling: possible involvement in insulin trafficking. Glycobiology 10: 39-50.
2. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, et al. (2004) Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide. J Exp Med 199: 947-957.
3. Wilson SB, Delovitch TL, (2003) Janus-like role of regulatory iNKT cells in autoimmune disease and tumour immunity. Nat Rev Immunol 3: 211-222.
4. Hussain S, Wagner M, Ly D, Delovitch TL, (2005) Role of regulatory invariant CD1d-restricted natural killer T-cells in protection against type 1 diabetes. Immunol Res 31: 177-188.
5. Arrenberg P, Halder R, Dai Y, Maricic I, Kumar V, (2010) Oligoclonality and innate-like features in the TCR repertoire of type II NKT cells reactive to a beta-linked self-glycolipid. Proc Natl Acad Sci U S A 107: 10984-10989.
6. Ambrosino E, Terabe M, Halder RC, Peng J, Takaku S, et al. (2007) Cross-regulation between type I and type II NKT cells in regulating tumor immunity: a new immunoregulatory axis. J Immunol 179: 5126-5136.
7. Bendelac A, Savage PB, Teyton L, (2007) The biology of NKT cells. Annu Rev Immunol 25: 297-336.
8. Jeon SB, Yoon HJ, Park SH, Kim IH, Park EJ, (2008) Sulfatide, a major lipid component of myelin sheath, activates inflammatory responses as an endogenous stimulator in brain-resident immune cells. J Immunol 181: 8077-8087.
9. Zajonc DM, Maricic I, Wu D, Halder R, Roy K, et al. (2005) Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity. J Exp Med 202: 1517-1526.
10. Zajonc DM, Kronenberg M, (2009) Carbohydrate specificity of the recognition of diverse glycolipids by natural killer T cells. Immunol Rev 230: 188-200.
11. Hong S, Wilson MT, Serizawa I, Wu L, Singh N, et al. (2001) The natural killer T-cell ligand alpha-galactosylceramide prevents autoimmune diabetes in non-obese diabetic mice. Nat Med 7: 1052-1056.
12. Naumov YN, Bahjat KS, Gausling R, Abraham R, Exley MA, et al. (2001) Activation of CD1d-restricted T cells protects NOD mice from developing diabetes by regulating dendritic cell subsets. Proc Natl Acad Sci U S A 98: 13838-13843.
13. Sharif S, Arreaza GA, Zucker P, Mi QS, Sondhi J, et al. (2001) Activation of natural killer T cells by alpha-galactosylceramide treatment prevents the onset and recurrence of autoimmune Type 1 diabetes. Nat Med 7: 1057-1062.
14. Wang B, Geng YB, Wang CR, (2001) CD1-restricted NK T cells protect nonobese diabetic mice from developing diabetes. J Exp Med 194: 313-320.
15. Lehuen A, Diana J, Zaccone P, Cooke A, (2010) Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol 10: 501-513.
16. Ly D, Mi QS, Hussain S, Delovitch TL, (2006) Protection from type 1 diabetes by invariant NK T cells requires the activity of CD4+CD25+ regulatory T cells. J Immunol 177: 3695-3704.
17. Mi QS, Ly D, Zucker P, McGarry M, Delovitch TL, (2004) Interleukin-4 but not interleukin-10 protects against spontaneous and recurrent type 1 diabetes by activated CD1d-restricted invariant natural killer T-cells. Diabetes 53: 1303-1310.
18. Duarte N, Stenstrom M, Campino S, Bergman ML, Lundholm M, et al. (2004) Prevention of diabetes in nonobese diabetic mice mediated by CD1d-restricted nonclassical NKT cells. J Immunol 173: 3112-3118.
19. Halder RC, Aguilera C, Maricic I, Kumar V, (2007) Type II NKT cell-mediated anergy induction in type I NKT cells prevents inflammatory liver disease. J Clin Invest 117: 2302-2312.
20. Sundell IB, Halder R, Zhang M, Maricic I, Koka PS, et al. (2010) Sulfatide administration leads to inhibition of HIV-1 replication and enhanced hematopoeisis. J Stem Cells 5: 33-42.
21. Arrenberg P, Maricic I, Kumar V, (2011) Sulfatide-mediated activation of type II natural killer T cells prevents hepatic ischemic reperfusion injury in mice. Gastroenterology 140: 646-655.
22. Arrenberg P, Halder R, Kumar V, (2009) Cross-regulation between distinct natural killer T cell subsets influences immune response to self and foreign antigens. J Cell Physiol 218: 246-250.
23. Buschard K, Lindblad U, Bog-Hansen E, Blomqvist M, Bengtsson K, et al. (2005) Low serum concentration of sulfatide and presence of sulfated galactosylceramide are associated with type 2 diabetes. Diabetic Med. 22: 1190-1198.
24. Blomqvist M, Osterbye T, Mansson JE, Horn T, Buschard K, et al. (2003) Selective lack of the C16:0 fatty acid isoform of sulfatide in pancreas of type II diabetic animal models. Apmis 111: 867-877.
25. Blomqvist M, Kaas A, Mansson JE, Formby B, Rynmark BM, et al. (2003) Developmental expression of the type I diabetes related antigen sulfatide and sulfated lactosylceramide in mammalian pancreas. J Cell Biochem 89: 301-310.
26. Osterbye T, Jorgensen KH, Fredman P, Tranum-Jensen J, Kaas A, et al. (2001) Sulfatide promotes the folding of proinsulin, preserves insulin crystals, and mediates its monomerization. Glycobiology 11: 473-479.
27. Buschard K, Blomqvist M, Mansson JE, Fredman P, Juhl K, et al. (2006) C16:0 sulfatide inhibits insulin secretion in rat beta-cells by reducing the sensitivity of KATP channels to ATP inhibition. Diabetes 55: 2826-2834.
28. Roeske-Nielsen A, Fredman P, Mansson JE, Bendtzen K, Buschard K, (2004) Beta-galactosylceramide increases and sulfatide decreases cytokine and chemokine production in whole blood cells. Immunol Lett 91: 205-211.
29. Buschard K, Hanspers K, Fredman P, Reich EP, (2001) Treatment with sulfatide or its precursor, galactosylceramide, prevents diabetes in NOD mice. Autoimmunity 34: 9-17.
30. Ly D, Tohn R, Rubin B, Blumenfeld H, Besra GS, et al. (2010) An alpha-galactosylceramide C20:2 N-acyl variant enhances anti-inflammatory and regulatory T cell-independent responses that prevent type 1 diabetes. Clin Exp Immunol 160: 185-198.
31. Tohn R, Blumenfeld H, Haeryfar SM, Veerapen N, Besra GS, et al. (2011) Stimulation of a shorter duration in the state of anergy by an invariant natural killer T cell agonist enhances its efficiency of protection from type 1 diabetes. Clin Exp Immunol 164: 26-41.
32. Blomqvist M, Rhost S, Teneberg S, Lofbom L, Osterbye T, et al. (2009) Multiple tissue-specific isoforms of sulfatide activate CD1d-restricted type II NKT cells. Eur J Immunol 39: 1726-1735.
33. Wilson MT, Johansson C, Olivares-Villagomez D, Singh AK, Stanic AK, et al. (2003) The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion. Proc Natl Acad Sci U S A 100: 10913-10918.
34. Buschard K, Blomqvist M, Osterbye T, Fredman P, (2005) Involvement of sulfatide in beta cells and type 1 and type 2 diabetes. Diabetologia 48: 1957-1962.
35. Buschard K, Schloot NC, Kaas A, Bock T, Horn T, et al. (1999) Inhibition of insulin-specific autoreactive T-cells by sulphatide which is variably expressed in beta cells. Diabetologia 42: 1212-1218.
36. Matsuda JL, Gapin L, Baron JL, Sidobre S, Stetson DB, et al. (2003) Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo. Proc Natl Acad Sci U S A 100: 8395-8400.
37. Fujii S, Liu K, Smith C, Bonito AJ, Steinman RM, (2004) The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J Exp Med 199: 1607-1618.
38. Kojo S, Seino K, Harada M, Watarai H, Wakao H, et al. (2005) Induction of regulatory properties in dendritic cells by Valpha14 NKT cells. J Immunol 175: 3648-3655.
39. Yamaura A, Hotta C, Nakazawa M, Van KL, Minami M, (2008) Human invariant Valpha24+ natural killer T cells acquire regulatory functions by interacting with IL-10-treated dendritic cells. Blood 111: 4254-4263.
40. Kadri N, Korpos E, Gupta S, Briet C, Löfbom L, et al. (2012) CD4+ type II NKT cells mediate ICOS and programmed death-1-dependent regulation of Type 1 diabetes. J Immunol 188: 3138-3149.
41. Wang J, Cho S, Ueno A, Cheng L, Xu BY, et al. (2008) Ligand-dependent induction of noninflammatory dendritic cells by anergic invariant NKT cells minimizes autoimmune inflammation. J Immunol 181: 2438-2445.
42. Blumenfeld HJ, Tohn R, Haeryfar SM, Liu Y, Savage PB, et al. (2011) Structure-guided design of an invariant natural killer T cell agonist for optimum protection from type 1 diabetes in non-obese diabetic mice. Clin Exp Immunol 166: 121-133.
43. Goff RD, Gao Y, Mattner J, Zhou D, Yin N, et al. (2004) Effects of lipid chain lengths in alpha-galactosylceramides on cytokine release by natural killer T cells. J Am Chem Soc 126: 13602-13603.
44. Hava DL, Brigl M, van den Elzen P, Zajonc DM, Wilson IA, et al. (2005) CD1 assembly and the formation of CD1-antigen complexes. Curr Opin Immunol 17: 88-94.
45. Miyamoto K, Miyake S, Yamamura T, (2001) A synthetic glycolipid prevents autoimmune encephalomyelitis byinducing TH2 bias of natural killer T cells. Nature 413: 531-534.46.
46. Rauch J, Gumperz J, Robinson C, Skold M, Roy C, et al. (2003) Structural features of the acyl chain determine self-phospholipid antigen recognition by a CD1d-restricted invariant NKT (iNKT) cell. J Biol Chem 278: 47508-47515.
47. Yu KO, Im JS, Molano A, Dutronc Y, Illarionov PA, et al. (2005) Modulation of CD1d-restricted NKT cell responses by using N-acyl variants of alpha-galactosylceramides. Proc Natl Acad Sci U S A 102: 3383-3388.
48. McCarthy C, Shepherd D, Fleire S, Stronge VS, Koch M, et al. (2007) The length of lipids bound to human CD1d molecules modulates the affinity of NKT cell TCR and the threshold of NKT cell activation. J Exp Med 204: 1131-1144.
49. Blomqvist M, Carrier M, Andrews T, Pettersson K, Mansson JE, et al. (2005) In vivo administration of the C16:0 fatty acid isoform of sulfatide increases pancreatic sulfatide and enhances glucose-stimulated insulin secretion in Zucker fatty (fa/fa) rats. Diabetes Metab Res Rev 21: 158-166.
50. Rosengren B, Fredman P, Mansson JE, Svennerholm L, (1989) Lysosulfatide (galactosylsphingosine-3-O-sulfate) from metachromatic leukodystrophy and normal human brain. J Neurochem 52: 1035-1041.