Brain glycolipids suppress T helper cells and inhibit autoimmune demyelination

Journal of Neuroscience

Volumn 34, Issue 25, 2014, Pages 8646-8658

  Mycko, Marcin P ^a   Sliwinska, Beata ^a   Cichalewska, Maria ^a   Cwiklinska, Hanna ^a   Raine, Cedric S ^b   Selmaj, Krzysztof W ^a  

^a MEDICAL UNIVERSITY OF LODZ   (Poland)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Autoimmune demyelination; Experimental autoimmune encephalomyelitis; Glycolipids; Multiple sclerosis; T cells; Th17

Indexed keywords

CD1D ANTIGEN; EARLY GROWTH RESPONSE FACTOR 2; GALECTIN 4; GLYCOLIPID; MESSENGER RNA; MYELIN PROTEIN; SULFATIDE;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CLONAL ANERGY; DEMYELINATION; DISEASE PREDISPOSITION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HELPER CELL; HISTOPATHOLOGY; IMMUNE RESPONSE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; RNA EXTRACTION; SPLEEN CELL; T CELL CULTURE; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; WESTERN BLOTTING;

AUTOIMMUNE DEMYELINATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GLYCOLIPIDS; MULTIPLE SCLEROSIS; T CELLS; TH17;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELLS, CULTURED; DEMYELINATING AUTOIMMUNE DISEASES, CNS; FEMALE; GLYCOLIPIDS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84902440137     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0885-14.2014     Document Type: Article

References (53)

1. Adams EJ, LuomaAM (2013) The adaptable major histocompatibility complex (MHC) fold: structure and function of nonclassical and MHC class I-like molecules. Annu Rev Immunol 31:529-561. CrossRef Medline
2. Aggarwal S, Yurlova L, Simons M (2011) Central nervous system myelin: structure, synthesis and assembly. Trends Cell Biol 21:585-593. CrossRef Medline
3. Bettelli E, Korn T, Oukka M, Kuchroo VK (2008) Induction and effector functions of T(H)17 cells. Nature 453:1051-1057. CrossRef Medline
4. Bosio A, Binczek E, Stoffel W (1996) Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc Natl Acad Sci U S A 93: 13280-13285. CrossRef Medline
5. Bridger GJ, Skerlj RT, Thornton D, Padmanabhan S, Martellucci SA, Henson GW, Abrams MJ, Yamamoto N, De Vreese K, Pauwels R (1995) Synthesis and structure-activity relationships of phenylenebis(methylene)-linked bis-tetraazamacrocycles that inhibit HIV replication: effects of macrocyclic ring size and substituents on the aromatic linker. J Med Chem 38:366-378. CrossRef Medline
6. Chappert P, Schwartz RH (2010) Induction of T cell anergy: integration of environmental cues and infectious tolerance. Curr Opin Immunol 22: 552-559. CrossRef Medline
7. Coetzee T, Fujita N, Dupree J, Shi R, Blight A, Suzuki K, Suzuki K, Popko B (1996) Myelination in the absence of galactocerebroside and sulfatide: normal structure with abnormal function and regional instability. Cell 86:209-219. CrossRef Medline
8. Cuzner ML, Davison AN (1973) Changes in cerebral lysosomal enzyme activity and lipids in multiple sclerosis. J Neurol Sci 19:29-36. CrossRef Medline
9. Delacour D, Gouyer V, Zanetta JP, Drobecq H, Leteurtre E, Grard G, Moreau-Hannedouche O, Maes E, Pons A, André S, Le Bivic A, Gabius HJ, Manninen A, Simons K, Huet G (2005) Galectin-4 and sulfatides in apical membrane trafficking in enterocyte-like cells. J Cell Biol 169:491-501. CrossRef Medline
10. Ding Z, Kawashima H, Suzuki Y, Suzuki T, Ward PA, MiyasakaM (1997) A sulfatide receptor distinct from L-selectin is involved in lymphocyte activation. FEBS Lett 418:310-314. CrossRef Medline
11. Ding Z, Kawashima H, MiyasakaM (2000) Sulfatide binding and activation of leukocytes through an L-selectin-independent pathway. J Leukoc Biol 68:65-72. CrossRef Medline
12. Ding Z, Issekutz TB, Downey GP, Waddell TK (2003) L-selectin stimulation enhances functional expression of surface CXCR4 in lymphocytes: implications for cellular activation during adhesion and migration. Blood 101: 4245-4252. CrossRef Medline
13. + T cells. Eur J Immunol 37:2949-2960. CrossRef Medline
14. Gallatin WM, Weissman IL, Butcher EC (1983) A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304:30-34. CrossRef Medline
15. Ghoreschi K, Laurence A, Yang XP, Hirahara K, O'Shea JJ (2011) T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol 32:395-401. CrossRef Medline
16. Girardi E, Maricic I, Wang J, Mac TT, Iyer P, Kumar V, Zajonc DM (2012) Type II natural killer T cells use features of both innate-like and conventional T cells to recognize sulfatide self antigens. Nat Immunol 13:851-856. CrossRef Medline
17. Guy CS, Vignali KM, Temirov J, Bettini ML, Overacre AE, Smeltzer M, Zhang H, Huppa JB, Tsai YH, Lobry C, Xie J, Dempsey PJ, Crawford HC, Aifantis I, Davis MM, Vignali DA (2013) Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat Immunol 14:262-270. CrossRef Medline
18. Hatse S, Princen K, Bridger G, De Clercq E, Schols D (2002) Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett 527:255-262. CrossRef Medline
19. Ho PP, et al. (2012) Identification of naturally occurring fatty acids of the myelin sheath that resolve neuroinflammation. Sci Transl Med 4:137ra173. CrossRef Medline
20. Ideo H, Seko A, Yamashita K (2007) Recognition mechanism of galectin-4 for cholesterol 3-sulfate. J Biol Chem 282:21081-21089. CrossRef Medline
21. Iwasaki Y, Fujio K, Okamura T, Yanai A, Sumitomo S, Shoda H, Tamura T, Yoshida H, Charnay P, YamamotoK (2013) Egr-2 transcription factor is required for Blimp-1-mediated IL-10 production in IL-27-stimulated CD4(+) T cells. Eur J Immunol 43:1063-1073. CrossRef Medline
22. Jahng AW, Maricic I, Pedersen B, Burdin N, Naidenko O, Kronenberg M, Koezuka Y, Kumar V (2001) Activation of natural killer T cells potentiates or prevents experimental autoimmune encephalomyelitis. J Exp Med 194:1789-1799. CrossRef Medline
23. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, Kumar V (2004) Prevention of autoimmunity by targeting a distinct, noninvariant CD1dreactive T cell population reactive to sulfatide. J Exp Med 199:947-957. CrossRef Medline
24. 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. CrossRef Medline
25. Kanamori M, Tasumi Y, Iyoda T, Ushida M, Inaba K (2012) Sulfatide inhibits alpha-galactosylceramide presentation by dendritic cells. Int Immunol 24:129-136. CrossRef Medline
26. Kanter JL, Narayana S, Ho PP, Catz I, Warren KG, Sobel RA, Steinman L, RobinsonWH (2006) Lipid microarrays identify key mediators of autoimmune brain inflammation. Nat Med 12:138-143. CrossRef Medline
27. Konno A, Nunogami K, Wada T, Yachie A, Suzuki Y, Takahashi N, Suzuki T, Miyamoto D, Kiso M, Hasegawa A, Miyawaki T (1996) Inhibitory action of sulfatide, a putative ligand for L-selectin, on B cell proliferation and Ig production. Int Immunol 8:1905-1913. CrossRef Medline
28. Laudanna C, Constantin G, Baron P, Scarpini E, Scarlato G, Cabrini G, Dechecchi C, Rossi F, Cassatella MA, Berton G (1994) Sulfatides trigger increase of cytosolic free calcium and enhanced expression of tumor necrosis factor-alpha and interleukin-8 mRNA in human neutrophils: evidence for a role of L-selectin as a signaling molecule. J Biol Chem 269: 4021-4026. Medline
29. Mars LT, Gautron AS, Novak J, Beaudoin L, Diana J, Liblau RS, Lehuen A (2008) Invariant NKT cells regulate experimental autoimmune encephalomyelitis and infiltrate the central nervous system in a CD1dindependent manner. J Immunol 181:2321-2329. CrossRef Medline
30. Merten M, Beythien C, Gutensohn K, Kühnl P, Meinertz T, Thiagarajan P (2005) Sulfatides activate platelets through P-selectin and enhance platelet and platelet-leukocyte aggregation. Arterioscler Thromb Vasc Biol 25: 258-263. CrossRef Medline
31. Miao T, Raymond M, Bhullar P, Ghaffari E, Symonds AL, Meier UC, Giovannoni G, Li S, Wang P (2013) Early growth response gene-2 controls IL-17 expression and Th17 differentiation by negatively regulating Batf. J Immunol 190:58-65. CrossRef Medline
32. Mycko MP, Ferrero I, Wilson A, Jiang W, Bianchi T, Trumpp A, MacDonald HR (2009) Selective requirement for c-Myc at an early stage of V(alpha)14iNKTcell development. J Immunol 182:4641-4648. CrossRef Medline
33. Nylander A, Hafler DA (2012) Multiple sclerosis. J Clin Invest 122:1180-1188. CrossRef Medline
34. Ogawa D, Shikata K, Honke K, Sato S, Matsuda M, Nagase R, Tone A, Okada S, Usui H, Wada J, Miyasaka M, Kawashima H, Suzuki Y, Suzuki T, Taniguchi N, Hirahara Y, Tadano-Aritomi K, Ishizuka I, Tedder TF, Makino H (2004) Cerebroside sulfotransferase deficiency ameliorates L-selectin-dependent monocyte infiltration in the kidney after ureteral obstruction. J Biol Chem 279:2085-2090. CrossRef Medline
35. Patel O, Pellicci DG, Gras S, Sandoval-Romero ML, Uldrich AP, Mallevaey T, Clarke AJ, Le Nours J, Theodossis A, Cardell SL, Gapin L, Godfrey DI, Rossjohn J (2012) Recognition of CD1d-sulfatide mediated by a type II natural killer T cell antigen receptor. Nat Immunol 13:857-863. CrossRef Medline
36. Rabinovich GA, Croci DO (2012) Regulatory circuits mediated by lectinglycan interactions in autoimmunity and cancer. Immunity 36:322-335. CrossRef Medline
37. Ransohoff RM, Brown MA (2012) Innate immunity in the central nervous system. J Clin Invest 122:1164-1171. CrossRef Medline
38. Roy KC, Maricic I, Khurana A, Smith TR, Halder RC, Kumar V (2008) Involvement of secretory and endosomal compartments in presentation of an exogenous self-glycolipid to type IINKTcells. J Immunol 180:2942-2950. CrossRef Medline
39. Singh AK, Wilson MT, Hong S, Olivares-Villagómez D, Du C, Stanic AK, Joyce S, Sriram S, Koezuka Y, Van Kaer L (2001) Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J Exp Med 194:1801-1811. CrossRef Medline
40. Stancic M, Slijepcevic D, Nomden A, Vos MJ, de Jonge JC, Sikkema AH, Gabius HJ, Hoekstra D, Baron W (2012) Galectin-4, a novel neuronal regulator of myelination. Glia 60:919-935. CrossRef Medline
41. Stechly L, Morelle W, Dessein AF, André S, Grard G, Trinel D, Dejonghe MJ, Leteurtre E, Drobecq H, Trugnan G, Gabius HJ, Huet G (2009) Galectin-4-regulated delivery of glycoproteins to the brush border membrane of enterocyte-like cells. Traffic 10:438-450. CrossRef Medline
42. Storan MJ, Magnaldo T, Biol-N'Garagba MC, Zick Y, Key B (2004) Expression and putative role of lactoseries carbohydrates present on NCAM in the rat primary olfactory pathway. JCompNeurol 475:289-302. CrossRef Medline
43. Sud'ina GF, Brock TG, Pushkareva MA, Galkina SI, Turutin DV, Peters-Golden M, Ullrich V (2001) Sulphatides trigger polymorphonuclear granulocyte spreading on collagen-coated surfaces and inhibit subsequent activation of 5-lipoxygenase. Biochem J 359:621-629. CrossRef Medline
44. Suzuki K, Kamoshita S, Eto Y, Tourtellotte WW, Gonatas JO (1973) Myelin in multiple sclerosis: composition of myelin from normal-appearing white matter. Arch Neurol 28:293-297. CrossRef Medline
45. Suzuki Y, Toda Y, Tamatani T, Watanabe T, Suzuki T, Nakao T, Murase K, Kiso M, Hasegawa A, Tadano-Aritomi K (1993) Sulfated glycolipids are ligands for a lymphocyte homing receptor, L-selectin (LECAM-1), binding epitope in sulfated sugar chain. Biochem Biophys Res Commun 190: 426-434. CrossRef Medline
46. Turutin DV, Kubareva EA, Pushkareva MA, Ullrich V, Sud'ina GF (2003) Activation of NF-kappa B transcription factor in human neutrophils by sulphatides and L-selectin cross-linking. FEBS Lett 536:241-245. CrossRef Medline
47. Velasco S, Díez-Revuelta N, Hernández-Iglesias T, Kaltner H, André S, Gabius HJ, Abad-Rodríguez J (2013) Neuronal Galectin-4 is required for axon growth and for the organization of axonal membrane L1 delivery and clustering. J Neurochem 125:49-62. CrossRef Medline
48. Wei Q, Eviatar-Ribak T, Miskimins WK, Miskimins R (2007) Galectin-4 is involved in p27-mediated activation of the myelin basic protein promoter. J Neurochem 101:1214-1223. CrossRef Medline
49. Wilson R, Tocher DR (1991) Lipid and fatty acid composition is altered in plaque tissue from multiple sclerosis brain compared with normal brain white matter. Lipids 26:9-15. CrossRef Medline
50. Woelk H, Borri P (1973) Lipid and fatty acid composition of myelin purified from normal and MS brains. Eur Neurol 10:250-260. CrossRef Medline
51. Yahara S, Kawamura N, Kishimoto Y, Saida T, Tourtellotte WW (1982) A change in the cerebrosides and sulfatides in a demyelinating nervous system: development of the methodology and study of multiple sclerosis and Wallerian degeneration. J Neurol Sci 54:303-315. CrossRef Medline
52. Yamada M, Kubo H, Kobayashi S, Ishizawa K, He M, Suzuki T, Fujino N, Kunishima H, Hatta M, Nishimaki K, Aoyagi T, Tokuda K, Kitagawa M, Yano H, Tamamura H, Fujii N, Kaku M (2011) The increase in surface CXCR4 expression on lung extravascular neutrophils and its effects on neutrophils during endotoxin-induced lung injury. Cell Mol Immunol 8:305-314. CrossRef Medline
53. Zajonc DM, Maricic I, Wu D, Halder R, Roy K, Wong CH, Kumar V, Wilson IA (2005) Structural basis for CD1d presentation of a sulfatide derived from myelin and its implications for autoimmunity. J Exp Med 202:1517-1526. CrossRef Medline