The enigmatic role of sulfatides: New insights into cellular functions and mechanisms of protein recognition

Advances in Experimental Medicine and Biology

Volumn 991, Issue , 2013, Pages 27-40

  Xiao, Shuyan ^a   Finkielstein, Carla V ^a   Capelluto, Daniel G S ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Ceramide; Cluster of differentiation 1; Disabled 2; Plasma membrane; Platelet aggregation; Sulfatide binding proteins; Sulfatides

Indexed keywords

ADAPTOR PROTEIN; DISABLED 2 PROTEIN; SULFATIDE; UNCLASSIFIED DRUG;

AUTOIMMUNITY; CARDIOVASCULAR DISEASE; CELL FUNCTION; CELLULAR DISTRIBUTION; HOST PATHOGEN INTERACTION; HUMAN; INNATE IMMUNITY; LIPID DEGRADATION; LIPOGENESIS; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR PATHOLOGY; MOLECULAR RECOGNITION; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION;

EUKARYOTA;

EID: 84884991504     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-6331-9_3     Document Type: Review

References (125)

1. Adams JC, Lawler J (2011) The thrombospondins. CSH Perspect Biol 3(10):a009712
2. Ahn VE, Faull KF, Whitelegge JP, Fluharty AL, Prive GG (2003) Crystal structure of saposin B reveals a dimeric shell for lipid binding. Proc Natl Acad Sci USA 100:38-43
3. Alajlouni R, Drahos KE, Finkielstein CV, Capelluto DG (2011) Lipid-mediated membrane binding properties of Disabled-2. Biochim Biophys Acta 1808: 2734-2744
4. Alderson NL, Rembiesa BM, Walla MD, Bielawska A, Bielawski J, Hama H (2004) The human FA2H gene encodes a fatty acid 2-hydroxylase. J Biol Chem 279:48562-48568
5. Andrews RK, Booth WJ, Bendall LJ, Berndt MC (1995) The amino Acid sequence glutamine-628 to valine-646 within the A1 repeat domain mediates binding of von Willebrand factor to bovine brain sulfatides and equine tendon collagen. Platelets 6:245-251
6. Barral DC, Brenner MB (2007) CD1 antigen presentation: how it works. Nat Rev Immunol 7:929-941
7. Bendelac A, Savage PB, Teyton L (2007) The biology of NKT cells. Annu Rev Immunol 25:297-336
8. Blomqvist M, Rhost S, Teneberg S, Lofbom L, Osterbye T, Brigl M, Mansson JE, Cardell SL (2009) Multiple tissue-specific isoforms of sulfatide activate CD1d-restricted type II NKT cells. Eur J Immunol 39:1726-1735
9. Borthakur G, Cruz MA, Dong JF, McIntire L, Li F, Lopez JA, Thiagarajan P (2003) Sulfatides inhibit platelet adhesion to von Willebrand factor in fl owing blood. J Thromb Haemost 1:1288-1295
10. Bruun JM, Roeske-Nielsen A, Richelsen B, Fredman P, Buschard K (2007) Sulfatide increases adiponectin and decreases TNF-alpha, IL-6, and IL-8 in human adipose tissue in vitro. Mol Cell Endocrinol 263:142-148
11. Calderon RO, Attema B, DeVries GH (1995) Lipid composition of neuronal cell bodies and neurites from cultured dorsal root ganglia. J Neurochem 64:424-429
12. Chen M, Geng JG (2006) P-selectin mediates adhesion of leukocytes, platelets, and cancer cells in in fl ammation, thrombosis, and cancer growth and metastasis. Arch Immunol Ther Exp (Warsz) 54:75-84
13. Chi S, Qi Z (2006) Regulatory effect of sulphatides on BKCa channels. Br J Pharmacol 149:1031-1038
14. Choi BK, Schifferli DM (1999) Lysine residue 117 of the FasG adhesin of enterotoxigenic Escherichia coli is essential for binding of 987Pfimbriae to sulfatide. Infect Immun 67:5755-5761
15. Coetzee T, Fujita N, Dupree J, Shi R, Blight A, 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
16. D'Hooge R, Van Dam D, Franck F, Gieselmann V, De Deyn PP (2001) Hyperactivity, neuromotor defects, and impaired learning and memory in a mouse model for metachromatic leukodystrophy. Brain Res 907:35-43
17. De Libero G, Mori L (2012) Novel insights into lipid antigen presentation. Trends Immunol 33:103-111
18. Drahos KE, Welsh JD, Finkielstein CV, Capelluto DG (2009) Sulfatides partition disabled-2 in response to platelet activation. PLoS One 4:e8007
19. Dupree JL, Coetzee T, Suzuki K, Popko B (1998) Myelin abnormalities in mice deficient in galactocerebroside and sulfatide. J Neurocytol 27:649-659
20. Eckhardt M (2008) The role and metabolism of sulfatide in the nervous system. Mol Neurobiol 37:93-103
21. Eckhardt M, Hedayati KK, Pitsch J, Lullmann-Rauch R, Beck H, Fewou SN, Gieselmann V (2007) Sulfatide storage in neurons causes hyperexcitability and axonal degeneration in a mouse model of metachromatic leukodystrophy. J Neurosci 27:9009-9021
22. Fantini J, Hammache D, Delezay O, Pieroni G, Tamalet C, Yahi N (1998) Sulfatide inhibits HIV-1 entry into CD4-/CXCR4+ cells. Virology 246:211-220
23. Fredman P, Mansson JE, Rynmark BM, Josefsen K, Ekblond A, Halldner L, Osterbye T, Horn T, Buschard K (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
24. Frenette PS, Johnson RC, Hynes RO, Wagner DD (1995) Platelets roll on stimulated endothelium in vivo: an interaction mediated by endothelial P-selectin. Proc Natl Acad Sci U S A 92:7450-7454
25. Frenette PS, Moyna C, Hartwell DW, Lowe JB, Hynes RO, Wagner DD (1998) Platelet-endothelial interactions in in fl amed mesenteric venules. Blood 91:1318-1324
26. Frenette PS, Wagner DD (1996) Adhesion molecules-Part 1. N Engl J Med 334(23):1526-1529
27. Frenette PS, Wagner DD (1996) Adhesion molecules-Part II: blood vessels and blood cells. N Engl J Med 335:43-45
28. Gahmberg CG (1997) Leukocyte adhesion: CD11/ CD18 integrins and intercellular adhesion molecules. Curr Opin Cell Biol 9:643-650
29. Gnewuch C, Jaques G, Havemann K, Wiegandt H (1994) Re-assessment of acidic glycosphingolipids in small-cell-lung-cancer tissues and cell lines. Int J Cancer 8:125-126
30. Goncalves C, Berthiaume F, Mourez M, Dubreuil JD (2008) Escherichia coli STb toxin binding to sulfatide and its inhibition by carragenan. FEMS Microbiol Lett 281:30-35
31. Guchhait P, Shrimpton CN, Honke K, Rumbaut RE, Lopez JA, Thiagarajan P (2008) Effect of an antisulfatide single-chain antibody probe on platelet function. Thromb Haemost 99:552-557
32. Guo NH, Krutzsch HC, Negre E, Vogel T, Blake DA, Roberts DD (1992) Heparin-and sulfatide-binding peptides from the type I repeats of human thrombospondin promote melanoma cell adhesion. Proc Natl Acad Sci U S A 89:3040-3044
33. Halder RC, Jahng A, Maricic I, Kumar V (2007) Mini review: immune response to myelin-derived sulfatide and CNS-demyelination. Neurochem Res 32:257-262
34. Harrison D, Hussain SA, Combs AC, Ervasti JM, Yurchenco PD, Hohenester E (2007) Crystal structure and cell surface anchorage sites of laminin alpha1LG4-5. J Biol Chem 282:11573-11581
35. Hirahara Y, Tsuda M, Wada Y, Honke K (2000) cDNA cloning, genomic cloning, and tissue-specific regulation of mouse cerebroside sulfotransferase. Eur J Biochem 267:1909-1917
36. Hiraiwa N, Fukuda Y, Imura H, Tadano-Aritomi K, Nagai K, Ishizuka I, Kannagi R (1990) Accumulation of highly acidic sulfated glycosphingolipids in human hepatocellular carcinoma defined by a series of monoclonal antibodies. Cancer Res 50:2917-2928
37. Hohenester E, Tisi D, Talts JF, Timpl R (1999) The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol Cell 4:783-792
38. Honke K, Hirahara Y, Dupree J, Suzuki K, Popko B, Fukushima K, Fukushima J, Nagasawa T, Yoshida N, Wada Y, Taniguchi N (2002) Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc Natl Acad Sci USA 99(7):4227-4232. doi: 10.1073/pnas.032068299
39. Honke K, Zhang Y, Cheng X, Kotani N, Taniguchi N (2004) Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj J 21:59-62
40. Hu R, Li G, Kamijo Y, Aoyama T, Nakajima T, Inoue T, Node K, Kannagi R, Kyogashima M, Hara A (2007) Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj J 24:565-571
41. Huang CL, Cheng JC, Liao CH, Stern A, Hsieh JT, Wang CH, Hsu HL, Tseng CP (2004) Disabled-2 is a negative regulator of integrin alpha(IIb)beta(3)- mediatedfibrinogen adhesion and cell signaling. J Biol Chem 279:42279-42289
42. Huang CL, Cheng JC, Stern A, Hsieh JT, Liao CH, Tseng CP (2006) Disabled-2 is a novel alphaIIbintegrin-binding protein that negatively regulates platelet-fibrinogen interactions and platelet aggregation. J Cell Sci 119:4420-4430
43. Huesca M, Borgia S, Hoffman P, Lingwood CA (1996) Acidic pH changes receptor binding specificity of Helicobacter pylori: a binary adhesion model in which surface heat shock (stress) proteins mediate sulfatide recognition in gastric colonization. Infect Immun 64:2643-2648
44. Huesca M, Goodwin A, Bhagwansingh A, Hoffman P, Lingwood CA (1998) Characterization of an acidicpH-inducible stress protein (hsp70), a putative sulfatide binding adhesin, from Helicobacter pylori. Infect Immun 66(9):4061-4067
45. Inoue T, Taguchi I, Abe S, Li G, Hu R, Nakajima T, Hara A, Aoyama T, Kannagi R, Kyogashima M, Node K (2010) Sulfatides are associated with neointimal thickening after vascular injury. Atherosclerosis 211(1):291-296
46. Isaac G, Pernber Z, Gieselmann V, Hansson E, Bergquist J, Mansson JE (2006) Sulfatide with short fatty acid dominates in astrocytes and neurons. FEBS J 273:1782-1790
47. Ishizuka I (1997) Chemistry and functional distribution of sulfoglycolipids. Prog Lipid Res 36(4): 245-319
48. Iwamura C, Shinoda K, Endo Y, Watanabe Y, Tumes DJ, Motohashi S, Kawahara K, Kinjo Y, Nakayama T (2012) Regulation of memory CD4 T-cell pool size and function by natural killer T cells in vivo. Proc Natl Acad Sci U S A 109:16992-16997
49. Jackson SP (2007) The growing complexity of platelet aggregation. Blood 109:5087-5095
50. Jahng A, Maricic I, Aguilera C, Cardell S, Halder RC, Kumar V (2004) Prevention of autoimmunity by targeting a distinct, noninvariant CD1d-reactive T cell population reactive to sulfatide. J Exp Med 199: 947-957
51. Jansson L, Tobias J, Jarefjall C, Lebens M, Svennerholm AM, Teneberg S (2009) Sulfatide recognition by colonization factor antigen CS6 from enterotoxigenic Escherichia coli. PLoS One 4:e4487
52. Jeon SB, Yoon HJ, Park SH, Kim IH, Park EJ (2008) Sulfatide, a major lipid component of myelin sheath, activates in fl ammatory responses as an endogenous stimulator in brain-resident immune cells. J Immunol 181:8077-8087
53. Kalb E, Engel J (1991) Binding and calcium-induced aggregation of laminin onto lipid bilayers. J Biol Chem 266:19047-19052
54. Kamlekar RK, Gao Y, Kenoth R, Molotkovsky JG, Prendergast FG, Malinina L, Patel DJ, Wessels WS, Venyaminov SY, Brown RE (2010) Human GLTP: three distinct functions for the three tryptophans in a novel peripheral amphitropic fold. Biophys J 99: 2626-2635
55. Kanter JL, Narayana S, Ho PP, Catz I, Warren KG, Sobel RA, Steinman L, Robinson WH (2006) Lipid microarrays identify key mediators of autoimmune brain in fl ammation. Nat Med 12:138-143
56. Kolter T, Sandhoff K (2005) Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu Rev Cell Dev Biol 21:81-103
57. Kushi Y, Arita M, Ishizuka I, Kasama T, Fredman P, Handa S (1996) Sulfatide is expressed in both erythrocytes and platelets of bovine origin. Biochim Biophys Acta 1304(3):254-262
58. Kwiatkowska K (2010) One lipid, multiple functions: how various pools of PI(4,5)P(2) are created in the plasma membrane. Cell Mol Life Sci 67:3927-3946
59. Kyogashima M (2004) The role of sulfatide in thrombogenesis and haemostasis. Arch Biochem Biophys 426:157-162
60. Larsen E, Celi A, Gilbert GE, Furie BC, Erban JK, Bonfanti R, Wagner DD, Furie B (1989) PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes. Cell 59:305-312
61. Li J, Pearl DK, Pfeiffer SE, Yates AJ (1994) Patterns of reactivity with anti-glycolipid antibodies in human primary brain tumors. J Neurosci Res 39:148-158
62. Liu Y, Chen Y, Momin A, Shaner R, Wang E, Bowen NJ, Matyunina LV, Walker LD, McDonald JF, Sullards MC, Merrill AH Jr (2010) Elevation of sulfatides in ovarian cancer: an integrated transcriptomic and lipidomic analysis including tissue-imaging mass spectrometry. Mol Cancer 9:186
63. Makhlouf AM, Fathalla MM, Zakhary MA, Makarem MH (2004) Sulfatides in ovarian tumors: clinicopathological correlates. Int J Gynecol Cancer 14:89-93
64. Malinina L, Malakhova ML, Kanack AT, Lu M, Abagyan R, Brown RE, Patel DJ (2006) The liganding of glycolipid transfer protein is controlled by glycolipid acyl structure. PLoS Biol 4:e362
65. Malinina L, Malakhova ML, Teplov A, Brown RE, Patel DJ (2004) Structural basis for glycosphingolipid transfer specificity. Nature 430:1048-1053
66. Marcus J, Honigbaum S, Shroff S, Honke K, Rosenbluth J, Dupree JL (2006) Sulfatide is essential for the maintenance of CNS myelin and axon structure. Glia 53:372-381
67. Matsushita T, Meyer D, Sadler JE (2000) Localization of von willebrand factor-binding sites for platelet glycoprotein Ib and botrocetin by charged-toalanine scanning mutagenesis. J Biol Chem 275: 11044-11049
68. Mattjus P (2009) Glycolipid transfer proteins and membrane interaction. Biochim Biophys Acta 1788:267-272
69. Matyas GR, Beck Z, Karasavvas N, Alving CR (2009) Lipid binding properties of 4E10, 2F5, and WR304 monoclonal antibodies that neutralize HIV-1. Biochim Biophys Acta 1788:660-665
70. Merten M, Beythien C, Gutensohn K, Kuhnl 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
71. Merten M, Thiagarajan P (2000) P-selectin expression on platelets determines size and stability of platelet aggregates. Circulation 102:1931-1936
72. Merten M, Thiagarajan P (2001) Role for sulfatides in platelet aggregation. Circulation 104:2955-2960
73. Moody DB, Zajonc DM, Wilson IA (2005) Anatomy of CD1-lipid antigen complexes. Nat Rev Immunol 5:387-399
74. Morichika H, Hamanaka Y, Tai T, Ishizuka I (1996) Sulfatides as a predictive factor of lymph node metastasis in patients with colorectal adenocarcinoma. Cancer 78(1):43-47
75. Nakajima T, Kamijo Y, Yuzhe H, Kimura T, Tanaka N, Sugiyama E, Nakamura K, Kyogashima M, Hara A, Aoyama T (2013) Peroxisome proliferator-activated receptor alpha mediates enhancement of gene expression of cerebroside sulfotransferase in several murine organs. Glycoconj J in press
76. Nakayama T, Matsushita T, Yamamoto K, Mutsuga N, Kojima T, Katsumi A, Nakao N, Sadler JE, Naoe T, Saito H (2008) Identification of amino acid residues responsible for von Willebrand factor binding to sulfatide by charged-to-alanine-scanning mutagenesis. Int J Hematol 87:363-370
77. Norton WT, Autilio LA (1965) The chemical composition of bovine CNS myelin. Ann N Y Acad Sci 122:77-85
78. 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
79. Peng L, Suzuki K (1987) Ultrastructural study of neurons in metachromatic leukodystrophy. Clin Neuropathol 6:224-230
80. Perino J, Foo CH, Spehner D, Cohen GH, Eisenberg RJ, Crance JM, Favier AL (2011) Role of sulfatide in vaccinia virus infection. Biol Cell 103:319-331
81. Pernber Z, Molander-Melin M, Berthold CH, Hansson E, Fredman P (2002) Expression of the myelin and oligodendrocyte progenitor marker sulfatide in neurons and astrocytes of adult rat brain. J Neurosci Res 69:86-93
82. Plow EF, Pierschbacher MD, Ruoslahti E, Marguerie GA, Ginsberg MH (1985) The effect of Arg-Gly-Aspcontaining peptides onfibrinogen and von Willebrand factor binding to platelets. Proc Natl Acad Sci U S A 82:8057-8061
83. Pouyani T, Seed B (1995) PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell 83:333-343
84. Ramakrishnan H, Hedayati KK, Lullmann-Rauch R, Wessig C, Fewou SN, Maier H, Goebel HH, Gieselmann V, Eckhardt M (2007) Increasing sulfatide synthesis in myelin-forming cells of arylsulfatase A-deficient mice causes demyelination and neurological symptoms reminiscent of human metachromatic leukodystrophy. J Neurosci 27:9482-9490
85. Roberts DD, Haverstick DM, Dixit VM, Frazier WA, Santoro SA, Ginsburg V (1985) The platelet glycoprotein thrombospondin binds specifically to sulfated glycolipids. J Biol Chem 260:9405-9411
86. Roberts DD, Rao CN, Liotta LA, Gralnick HR, Ginsburg V (1986) Comparison of the specificities of laminin, thrombospondin, and von Willebrand factor for binding to sulfated glycolipids. J Biol Chem 261:6872-6877
87. 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
88. Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, Lopez JA (1999) The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 190:803-814
89. Saadat L, Dupree JL, Kilkus J, Han X, Traka M, Proia RL, Dawson G, Popko B (2010) Absence of oligodendroglial glucosylceramide synthesis does not result in CNS myelin abnormalities or alter the dysmyelinating phenotype of CGT-deficient mice. Glia 58:391-398
90. Sakakibara N, Gasa S, Kamio K, Makita A, Nonomura K, Togashi M, Koyanagi T, Hatae Y, Takeda K (1991) Distinctive glycolipid patterns in Wilms' tumor and renal cell carcinoma. Cancer Lett 57:187-192
91. Samygina VR, Popov AN, Cabo-Bilbao A, Ochoa-Lizarralde B, Goni-de-Cerio F, Zhai X, Molotkovsky JG, Patel DJ, Brown RE, Malinina L (2011) Enhanced selectivity for sulfatide by engineered human glycolipid transfer protein. Structure 19:1644-1654
92. Sandhoff R, Grieshaber H, Djafarzadeh R, Sijmonsma TP, Proudfoot AE, Handel TM, Wiegandt H, Nelson PJ, Grone HJ (2005) Chemokines bind to sulfatides as revealed by surface plasmon resonance. Biochim Biophys Acta 1687:52-63
93. Sarlieve LL, Zalc B, Neskovic NM, Zanetta JP, Rebel G (1984) Structure and immunological localization of spleen sulfolipid. Biochim Biophys Acta 795:166-168
94. Shamshiev A, Gober HJ, Donda A, Mazorra Z, Mori L, De Libero G (2002) Presentation of the same glycolipid by different CD1 molecules. J Exp Med 195:1013-1021
95. Shimazawa M, Kondo K, Hara H, Nakashima M, Umemura K (2005) Sulfatides, L-and P-selectin ligands, exacerbate the intimal hyperplasia occurring after endothelial injury. Eur J Pharmacol 520:118-126
96. Simonis D, Schlesinger M, Seelandt C, Borsig L, Bendas G (2010) Analysis of SM4 sulfatide as a P-selectin ligand using model membranes. Biophys Chem 150:98-104
97. Sugiyama T, Miyazawa M, Mikami M, Goto Y, Nishijima Y, Ikeda M, Hirasawa T, Muramatsu T, Takekoshi S, Iwamori M (2012) Enhanced expression of sulfatide, a sulfated glycolipid, in well-differentiated endometrial adenocarcinoma. Int J Gynecol Cancer 22:1192-1197
98. Sundell IB, Halder R, Zhang M, Maricic I, Koka PS, Kumar V (2010) Sulfatide administration leads to inhibition of HIV-1 replication and enhanced hematopoeisis. J Stem Cells 5:33-42
99. Suzuki T, Sometani A, Yamazaki Y, Horiike G, Mizutani Y, Masuda H, Yamada M, Tahara H, Xu G, Miyamoto D, Oku N, Okada S, Kiso M, Hasegawa A, Ito T, Kawaoka Y, Suzuki Y (1996) Sulphatide binds to human and animal in fl uenza A viruses, and inhibits the viral infection. Biochem J 318:389-393
100. Svennerholm L, Bostrom K, Fredman P, Jungbjer B, Mansson JE, Rynmark BM (1992) Membrane lipids of human peripheral nerve and spinal cord. Biochim Biophys Acta 1128:1-7
101. Takahashi T, Murakami K, Nagakura M, Kishita H, Watanabe S, Honke K, Ogura K, Tai T, Kawasaki K, Miyamoto D, Hidari KI, Guo CT, Suzuki Y, Suzuki T (2008) Sulfatide is required for efficient replication of in fl uenza A virus. J Virol 82:5940-5950
102. Talts JF, Andac Z, Gohring W, Brancaccio A, Timpl R (1999) Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. EMBO J 18:863-870
103. Taraboletti G, Rao CN, Krutzsch HC, Liotta LA, Roberts DD (1990) Sulfatide-binding domain of the laminin A chain. J Biol Chem 265:12253-12258
104. Theilmeier G, Lenaerts T, Remacle C, Collen D, Vermylen J, Hoylaerts MF (1999) Circulating activated platelets assist THP-1 monocytoid/endothelial cell interaction under shear stress. Blood 94:2725-2734
105. Thudichum JL (1884) A treatise on the chemical constitution of the brain. Balliere, Tindall, and Cox, London
106. Tjong SC, Wu PL, Wang CM, Huang WN, Ho NL, Wu WG (2007) Role of glycosphingolipid conformational change in membrane pore forming activity of cobra cardiotoxin. Biochemistry 46:12111-12123
107. van Zyl R, Gieselmann V, Eckhardt M (2010) Elevated sulfatide levels in neurons cause lethal audiogenic seizures in mice. J Neurochem 112:282-295
108. Vargas ME, Watanabe J, Singh SJ, Robinson WH, Barres BA (2010) Endogenous antibodies promote rapid myelin clearance and effective axon regeneration after nerve injury. Proc Natl Acad Sci USA 107:11993-11998
109. Vos JP, Lopes-Cardozo M, Gadella BM (1994) Metabolic and functional aspects of sulfogalactolipids. Biochim Biophys Acta 1211:125-149
110. Wang CH, Liu JH, Lee SC, Hsiao CD, Wu WG (2006) Glycosphingolipid- facilitated membrane insertion and internalization of cobra cardiotoxin. The sulfatide.cardiotoxin complex structure in a membrane-like environment suggests a lipid-dependent cell-penetrating mechanism for membrane binding polypeptides. J Biol Chem 281:656-667
111. Wang L, Kamijo Y, Matsumoto A, Nakajima T, Higuchi M, Kannagi R, Kyogashima M, Aoyama T, Hara A (2011) Kidney transplantation recovers the reduction level of serum sulfatide in ESRD patients via processes correlated to oxidative stress and platelet count. Glycoconj J 28:125-135
112. Watarai S, Onuma M, Yamamoto S, Yasuda T (1990) Inhibitory effect of liposomes containing sulfatide or cholesterol sulfate on syncytium formation induced by bovine immunodeficiency virus-infected cells. J Biochem 108:507-509
113. Welsh JD, Charonko JJ, Salmanzadeh A, Drahos KE, Shafiee H, Stremler MA, Davalos RV, Capelluto DG, Vlachos PP, Finkielstein CV (2011) Disabled-2 modulates homotypic and heterotypic platelet interactions by binding to sulfatides. Br J Haematol 154:122-133
114. Winzeler AM, Mandemakers WJ, Sun MZ, Stafford M, Phillips CT, Barres BA (2011) The lipid sulfatide is a novel myelin-associated inhibitor of CNS axon outgrowth. J Neurosci 31:6481-6492
115. Wu PL, Chiu CR, Huang WN, Wu WG (2012) The role of sulfatide lipid domains in the membrane pore-forming activity of cobra cardiotoxin. Biochim Biophys Acta 1818:1378-1385
116. Xiao S, Charonko JJ, Fu X, Salmanzadeh A, Davalos RV, Vlachos PP, Finkielstein CV, Capelluto DG (2012) Structure, sulfatide binding properties, and inhibition of platelet aggregation by a Disabled-2 protein-derived peptide. J Biol Chem 287:37691-37702
117. Yaghootfam A, Sorkalla T, Haberlein H, Gieselmann V, Kappler J, Eckhardt M (2007) Cerebroside sulfotransferase forms homodimers in living cells. Biochemistry 46:9260-9269
118. Yang H, Lang S, Zhai Z, Li L, Kahr WH, Chen P, Brkic J, Spring CM, Flick MJ, Degen JL, Freedman J, Ni H (2009) Fibrinogen is required for maintenance of platelet intracellular and cell-surface P-selectin expression. Blood 114:425-436
119. Yuki D, Sugiura Y, Zaima N, Akatsu H, Hashizume Y, Yamamoto T, Fujiwara M, Sugiyama K, Setou M (2011) Hydroxylated and non-hydroxylated sulfatide are distinctly distributed in the human cerebral cortex. Neuroscience 193:44-53
120. Zajonc DM, Elsliger MA, Teyton L, Wilson IA (2003) Crystal structure of CD1a in complex with a sulfatide self antigen at a resolution of 2.15 A. Nat Immunol 4:808-815
121. 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
122. Zeng Z, Castano AR, Segelke BW, Stura EA, Peterson PA, Wilson IA (1997) Crystal structure of mouse CD1: an MHC-like fold with a large hydrophobic binding groove. Science 277:339-345
123. Zhang X, Nakajima T, Kamijo Y, Li G, Hu R, Kannagi R, Kyogashima M, Aoyama T, Hara A (2009) Acute kidney injury induced by protein-overload nephropathy down-regulates gene expression of hepatic cerebroside sulfotransferase in mice, resulting in reduction of liver and serum sulfatides. Biochem Biophys Res Commun 390:1382-1388
124. Zhang XL, Rafi MA, DeGala G, Wenger DA (1990) Insertion in the mRNA of a metachromatic leukodystrophy patient with sphingolipid activator protein-1 deficiency. Proc Natl Acad Sci USA 87:1426-1430
125. Zhou Z, Thiagarajan P, Udden M, Lopez JA, Guchhait P (2011) Erythrocyte membrane sulfatide plays a crucial role in the adhesion of sickle erythrocytes to endothelium. Thromb Haemost 105:1046-1052