Significance of glycosphingolipid fatty acid chain length on membrane microdomain-mediated signal transduction

FEBS Letters

Volumn 584, Issue 9, 2010, Pages 1642-1652

  Iwabuchi, Kazuhisa ^a,b   Nakayama, Hitoshi ^b   Iwahara, Chihiro ^a   Takamori, Kenji ^a  

^a JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JUNTENDO UNIVERSITY   (Japan)

Author keywords

Fatty acid chain; Glycosphingolipid; Microdomain; Src family kinase

Indexed keywords

FATTY ACID; GLYCOSPHINGOLIPID; LACTOSYLCERAMIDE; PATTERN RECOGNITION RECEPTOR; PROTEIN KINASE LYN; VERY LONG CHAIN FATTY ACID; CDW17 ANTIGEN; LEUKOCYTE ANTIGEN; LYN PROTEIN-TYROSINE KINASE; PROTEIN TYROSINE KINASE;

CELL DIFFERENTIATION; CELL FUNCTION; CELL MEMBRANE; CELL STRAIN HL 60; CONTROLLED STUDY; ENZYME ACTIVATION; FATTY ACID ANALYSIS; HUMAN; HUMAN CELL; LIGAND BINDING; MOLECULAR RECOGNITION; NEUTROPHIL; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD; FATTY ACIDS; GLYCOSPHINGOLIPIDS; HUMANS; LACTOSYLCERAMIDES; MEMBRANE MICRODOMAINS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 77951932472     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.10.043     Document Type: Review

References (77)

1. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
2. Lai E.C. Lipid rafts make for slippery platforms. J. Cell Biol. 2003, 162:365-370.
3. van Meer G. Cellular lipidomics. Embo J. 2005, 24:3159-3165.
4. Hakomori S., Handa K., Iwabuchi K., Yamamura S., Prinetti A. New insights in glycosphingolipid function: " glycosignaling domain" , a cell surface assembly of glycosphingolipids with signal transducer molecules, involved in cell adhesion coupled with signaling. Glycobiology 1998, 8:xi-xix.
5. Fujita A., Cheng J., Hirakawa M., Furukawa K., Kusunoki S., Fujimoto T. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell 2007, 18:2112-2122.
6. Iwabuchi K., et al. Involvement of very long fatty acid-containing lactosylceramide in lactosylceramide-mediated superoxide generation and migration in neutrophils. Glycoconj J. 2008, 25:357-374.
7. Kusumi A., Suzuki K. Toward understanding the dynamics of membrane-raft-based molecular interactions. Biochim. Biophys. Acta 2005, 1746:234-251.
8. Kaga N., Kazuno S., Taka H., Iwabuchi K., Murayama K. Isolation and mass spectrometry characterization of molecular species of lactosylceramides using liquid chromatography-electrospray ion trap mass spectrometry. Anal. Biochem. 2005, 337:316-324.
9. Maeda Y., Tashima Y., Houjou T., Fujita M., Yoko-o T., Jigami Y., Taguchi R., Kinoshita T. Fatty acid remodeling of GPI-anchored proteins is required for their raft association. Mol. Biol. Cell 2007, 18:1497-1506.
10. Nakayama H., Yoshizaki F., Prinetti A., Sonnino S., Mauri L., Takamori K., Ogawa H., Iwabuchi K. Lyn-coupled LacCer-enriched lipid rafts are required for CD11b/CD18-mediated neutrophil phagocytosis of nonopsonized microorganisms. J. Leukoc. Biol. 2008, 83:728-741.
11. Suzuki K.G., Fujiwara T.K., Edidin M., Kusumi A. Dynamic recruitment of phospholipase C gamma at transiently immobilized GPI-anchored receptor clusters induces IP3-Ca2+ signaling: single-molecule tracking study 2. J. Cell Biol. 2007, 177:731-742.
12. Suzuki K.G., Fujiwara T.K., Sanematsu F., Iino R., Edidin M., Kusumi A. GPI-anchored receptor clusters transiently recruit Lyn and G alpha for temporary cluster immobilization and Lyn activation: single-molecule tracking study 1. J. Cell Biol. 2007, 177:717-730.
13. Degroote S., Wolthoorn J., van Meer G. The cell biology of glycosphingolipids. Semin. Cell Dev. Biol. 2004, 15:375-387.
14. Hakomori S. Structure, organization, and function of glycosphingolipids in membrane. Curr. Opin. Hematol. 2003, 10:16-24.
15. Sonnino S., Prinetti A., Mauri L., Chigorno V., Tettamanti G. Dynamic and structural properties of sphingolipids as driving forces for the formation of membrane domains. Chem. Rev. 2006, 106:2111-2125.
16. Rock P., Allietta M., Young W.W., Thompson T.E., Tillack T.W. Ganglioside GM1 and asialo-GM1 at low concentration are preferentially incorporated into the gel phase in two-component, two-phase phosphatidylcholine bilayers. Biochemistry 1991, 30:19-25.
17. Tillack T.W., Allietta M., Moran R.E., Young W.W. Localization of globoside and Forssman glycolipids on erythrocyte membranes. Biochim. Biophys. Acta 1983, 733:15-24.
18. Rietveld A., Simons K. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta 1998, 1376:467-479.
19. Li X.M., Momsen M.M., Brockman H.L., Brown R.E. Lactosylceramide: effect of acyl chain structure on phase behavior and molecular packing. Biophys. J. 2002, 83:1535-1546.
20. Pike L.J. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 2006, 47:1597-1598.
21. Mukherjee S., Maxfield F.R. Membrane domains. Annu. Rev. Cell Dev. Biol. 2004, 20:839-866.
22. Brown D.A., London E. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes?. Biochem. Biophys. Res. Commun. 1997, 240:1-7.
23. Greenberg S., Grinstein S. Phagocytosis and innate immunity. Curr. Opin. Immunol. 2002, 14:136-145.
24. Stephens L., Ellson C., Hawkins P. Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr. Opin. Cell Biol. 2002, 14:203-213.
25. Gordon S. Pattern recognition receptors: doubling up for the innate immune response. Cell 2002, 111:927-930.
26. Blander J.M., Medzhitov R. Regulation of phagosome maturation by signals from toll-like receptors. Science 2004, 304:1014-1018.
27. Doyle S.E., et al. Toll-like receptors induce a phagocytic gene program through p38. J. Exp. Med. 2004, 199:81-90.
28. Ezekowitz R.A., Sastry K., Bailly P., Warner A. Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. J. Exp. Med. 1990, 172:1785-1794.
29. Jiang Z., et al. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 2005, 6:565-570.
30. Elomaa O., et al. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 1995, 80:603-609.
31. Peiser L., Gough P.J., Kodama T., Gordon S. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect. Immun. 2000, 68:1953-1963.
32. Herre J., et al. Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 2004, 104:4038-4045.
33. Brown E.J. Complement receptors and phagocytosis. Curr. Opin. Immunol. 1991, 3:76-82.
34. Iwabuchi K., Nagaoka I. Lactosylceramide-enriched glycosphingolipid signaling domain mediates superoxide generation from human neutrophils. Blood 2002, 100:1454-1464.
35. Sato T., et al. Induction of human neutrophil chemotaxis by Candida albicans-derived beta-1, 6-long glycoside side-chain-branched beta-glucan. J. Leukoc. Biol. 2006, 80:204-211.
36. Angstrom J., et al. The lactosylceramide binding specificity of Helicobacter pylori. Glycobiology 1998, 8:297-309.
37. Hahn P.Y., Evans S.E., Kottom T.J., Standing J.E., Pagano R.E., Limper A.H. Pneumocystis carinii cell wall beta-glucan induces release of macrophage inflammatory protein-2 from alveolar epithelial cells via a lactosylceramide-mediated mechanism. J. Biol. Chem. 2003, 278:2043-2050.
38. Karlsson K.A. Animal glycolipids as attachment sites for microbes. Chem. Phys. Lipids 1986, 42:153-172.
39. Saukkonen K., Burnette W.N., Mar V.L., Masure H.R., Tuomanen E.I. Pertussis toxin has eukaryotic-like carbohydrate recognition domains. Proc. Natl. Acad. Sci. USA 1992, 89:118-122.
40. Zimmerman J.W., Lindermuth J., Fish P.A., Palace G.P., Stevenson T.T., DeMong D.E. A novel carbohydrate-glycosphingolipid interaction between a beta-(1-3)-glucan immunomodulator, PGG-glucan, and lactosylceramide of human leukocytes. J. Biol. Chem. 1998, 273:22014-22020.
41. Fukuda M.N., Dell A., Oates J.E., Wu P., Klock J.C., Fukuda M. Structures of glycosphingolipids isolated from human granulocytes. The presence of a series of linear poly-N-acetyllactosaminylceramide and its significance in glycolipids of whole blood cells. J. Biol. Chem. 1985, 260:1067-1082.
42. Teneberg S., Angstrom J., Ljungh A. Carbohydrate recognition by enterohemorrhagic Escherichia coli: characterization of a novel glycosphingolipid from cat small intestine. Glycobiology 2004, 14:187-196.
43. Stromberg N., Karlsson K.A. Characterization of the binding of propionibacterium granulosum to glycosphingolipids adsorbed on surfaces. An apparent recognition of lactose which is dependent on the ceramide structure. J. Biol. Chem. 1990, 265:11244-11250.
44. Stromberg N., Ryd M., Lindberg A.A., Karlsson K.A. Studies on the binding of bacteria to glycolipids. Two species of Propionibacterium apparently recognize separate epitopes on lactose of lactosylceramide. FEBS Lett. 1988, 232:193-198.
45. Payne D., Tatham D., Williamson E.D., Titball R.W. The pH 6 antigen of Yersinia pestis binds to beta1-linked galactosyl residues in glycosphingolipids. Infect. Immun. 1998, 66:4545-4548.
46. Jansson L., Tobias J., Lebens M., Svennerholm A.M., Teneberg S. The major subunit, CfaB, of colonization factor antigen i from enterotoxigenic Escherichia coli is a glycosphingolipid binding protein. Infect. Immun. 2006, 74:3488-3497.
47. Stromberg N., Deal C., Nyberg G., Normark S., So M., Karlsson K.A. Identification of carbohydrate structures that are possible receptors for Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 1988, 85:4902-4906.
48. Backenson P.B., Coleman J.L., Benach J.L. Borrelia burgdorferi shows specificity of binding to glycosphingolipids. Infect. Immun. 1995, 63:2811-2817.
49. Stromberg N., Karlsson K.A. Characterization of the binding of Actinomyces naeslundii (ATCC 12104) and Actinomyces viscosus (ATCC 19246) to glycosphingolipids, using a solid-phase overlay approach. J. Biol. Chem. 1990, 265:11251-11258.
50. Abul-Milh M., Paradis S.E., Dubreuil J.D., Jacques M. Binding of Actinobacillus pleuropneumoniae lipopolysaccharides to glycosphingolipids evaluated by thin-layer chromatography. Infect. Immun. 1999, 67:4983-4987.
51. Yiu S.C., Lingwood C.A. Polyisobutylmethacrylate modifies glycolipid binding specificity of verotoxin 1 in thin-layer chromatogram overlay procedures. Anal. Biochem. 1992, 202:188-192.
52. Iwabuchi K., Yamamura S., Prinetti A., Handa K., Hakomori S. GM3-enriched microdomain involved in cell adhesion and signal transduction through carbohydrate-carbohydrate interaction in mouse melanoma B16 cells. J. Biol. Chem. 1998, 273:9130-9138.
53. Symington F.W. CDw17: a neutrophil glycolipid antigen regulated by activation. J. Immunol. 1989, 142:2784-2790.
54. Sato T., et al. Induction of human neutrophil chemotaxis by Candida albicans-derived b-1, 6 long glycoside side chains-branched b-glucan. J. Leukoc. Biol. 2006, 84:204-211.
55. Cassone A., Marconi P., Bistoni F. Cell wall of Candida albicans and host response. Crit. Rev. Microbiol. 1987, 15:87-95.
56. Ohno N., et al. Solubilization of yeast cell-wall beta-(1-3)-d-glucan by sodium hypochlorite oxidation and dimethyl sulfoxide extraction. Carbohydr. Res. 1999, 316:161-172.
57. Liang J., Melican D., Cafro L., Palace G., Fisette L., Armstrong R., Patchen M.L. Enhanced clearance of a multiple antibiotic resistant Staphylococcus aureus in rats treated with PGG-glucan is associated with increased leukocyte counts and increased neutrophil oxidative burst activity. Int. J. Immunopharmacol. 1998, 20:595-614.
58. Wakshull E., et al. PGG-glucan, a soluble beta-(1, 3)-glucan, enhances the oxidative burst response, microbicidal activity, and activates an NF-kappa B-like factor in human PMN: evidence for a glycosphingolipid beta-(1, 3)-glucan receptor. Immunopharmacology 1999, 41:89-107.
59. Le Cabec V., Cols C., Maridonneau-Parini I. Nonopsonic phagocytosis of zymosan and Mycobacterium kansasii by CR3 (CD11b/CD18) involves distinct molecular determinants and is or is not coupled with NADPH oxidase activation. Infect. Immun. 2000, 68:4736-4745.
60. Arnaout M.A. Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 1990, 75:1037-1050.
61. Piccardoni P., et al. SRC-dependent outside-in signalling is a key step in the process of autoregulation of beta2 integrins in polymorphonuclear cells. Biochem. J. 2004, 380:57-65.
62. Thornton B.P., Vetvicka V., Pitman M., Goldman R.C., Ross G.D. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J. Immunol. 1996, 156:1235-1246.
63. Xia Y., Vetvicka V., Yan J., Hanikyrova M., Mayadas T., Ross G.D. The beta-glucan-binding lectin site of mouse CR3 (CD11b/CD18) and its function in generating a primed state of the receptor that mediates cytotoxic activation in response to iC3b-opsonized target cells. J. Immunol. 1999, 162:2281-2290.
64. Vetvicka V., Thornton B.P., Ross G.D. Soluble beta-glucan polysaccharide binding to the lectin site of neutrophil or natural killer cell complement receptor type 3 (CD11b/CD18) generates a primed state of the receptor capable of mediating cytotoxicity of iC3b-opsonized target cells [see comments]. J. Clin. Invest. 1996, 98:50-61.
65. Evangelista V., et al. Src family kinases mediate neutrophil adhesion to adherent platelets. Blood 2007, 109:2461-2469.
66. Rabb H., Michishita M., Sharma C.P., Brown D., Arnaout M.A. Cytoplasmic tails of human complement receptor type 3 (CR3, CD11b/CD18) regulate ligand avidity and the internalization of occupied receptors. J. Immunol. 1993, 151:990-1002.
67. Dedhar S., Hannigan G.E. Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr. Opin. Cell Biol. 1996, 8:657-669.
68. Dharmawardhane S., Brownson D., Lennartz M., Bokoch G.M. Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J. Leukoc. Biol. 1999, 66:521-527.
69. Stockl J., Majdic O., Pickl W.F., Rosenkranz A., Prager E., Gschwantler E., Knapp W. Granulocyte activation via a binding site near the C-terminal region of complement receptor type 3 alpha-chain (CD11b) potentially involved in intramembrane complex formation with glycosylphosphatidylinositol-anchored Fc gamma RIIIB (CD16) molecules. J. Immunol. 1995, 154:5452-5463.
70. Bretscher M.S. Membrane structure: some general principles. Science 1973, 181:622-629.
71. Kusumi A., Koyama-Honda I., Suzuki K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 2004, 5:213-230.
72. Allende D., Vidal A., McIntosh T.J. Jumping to rafts: gatekeeper role of bilayer elasticity. Trends Biochem. Sci. 2004, 29:325-330.
73. Tanford C. The Hydrophobic Effect: Formation of Micelles and Biological Membranes 1980, John Wiley and Sons Inc, New York.
74. Grant C.W., Mehlhorn I.E., Florio E., Barber K.R. A long chain spin label for glycosphingolipid studies: transbilayer fatty acid interdigitation of lactosyl ceramide. Biochim. Biophys. Acta 1987, 902:169-177.
75. Fra A.M., Masserini M., Palestini P., Sonnino S., Simons K. A photo-reactive derivative of ganglioside GM1 specifically cross-links VIP21-caveolin on the cell surface. FEBS Lett. 1995, 375:11-14.
76. Prinetti A., Marano N., Prioni S., Chigorno V., Mauri L., Casellato R., Tettamanti G., Sonnino S. Association of Src-family protein tyrosine kinases with sphingolipids in rat cerebellar granule cells differentiated in culture. Glycoconj J. 2000, 17:223-232.
77. Palestini P., Pitto M., Tedeschi G., Ferraretto A., Parenti M., Brunner J., Masserini M. Tubulin anchoring to glycolipid-enriched, detergent-resistant domains of the neuronal plasma membrane. J. Biol. Chem. 2000, 275:9978-9985.