Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains

Biochimica et Biophysica Acta - General Subjects

Volumn 1780, Issue 3, 2008, Pages 421-433

  Regina Todeschini, Adriane ^a   Hakomori, Sen itiroh ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Ganglioside; Glycosphingolipids microdomain; Glycosylation; Glycosynapse; Integrin; Tetraspanin

Indexed keywords

CD82 ANTIGEN; CD9 ANTIGEN; FIBROBLAST GROWTH FACTOR RECEPTOR; GANGLIOSIDE GM1; GANGLIOSIDE GM2; GANGLIOSIDE GM3; INTEGRIN; PHOSPHOTRANSFERASE; TETRASPANIN;

CAVEOLA; CELL ADHESION; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; ENZYME ACTIVITY; HUMAN; MODULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TUMOR CELL;

ANIMALS; CAVEOLAE; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; GANGLIOSIDES; HUMANS; MEMBRANE MICRODOMAINS;

EID: 40749132024     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2007.10.008     Document Type: Review

References (101)

1. Hakomori S. Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Ann. Rev. Biochem. 50 (1981) 733-764
2. Hakomori S. Cancer-associated glycosphingolipid antigens: their structure, organization, and function. Acta Anat. 161 (1998) 79-90
3. Hakomori S., Handa K., Iwabuchi K., Yamamura S., and 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 8 (1998) xi-xviii
4. Pascher I. Molecular arrangements in sphingolipids: conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta 455 (1976) 433-451
5. Okada Y., Mugnai G., Bremer E.G., and Hakomori S. Glycosphingolipids in detergent-insoluble substrate attachment matrix (DISAM) prepared from substrate attachment material (SAM): their possible role in regulating cell adhesion. Exp. Cell Res. 155 (1984) 448-456
6. Brown D.A., and London E. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes?. Biochem. Biophys. Res. Commun. 240 (1997) 1-7
7. Hakomori S., and Handa K. Glycosphingolipid-dependent cross-talk between glycosynapses interfacing tumor cells with their host cells: Essential basis to define tumor malignancy. FEBS Lett. 531 (2002) 88-92
8. Hakomori S. Glycosynapses: microdomains controlling carbohydrate-dependent cell adhesion and signaling. Ann. Braz Acad. Sci. 76 (2004) 553-572
9. Hakomori S. Organization and function of glycosphingolipids in membrane. Proc. Jpn. Acad., Ser. B Phys. Biol. Sci. 81 (2005) 189-203
10. Singer S.J., and Nicolson G. The fluid mosaic model of the structure of cell membrane. Science 185 (1972) 720-731
11. Jain M.K., and White H.B. Long-range order in biomembranes. Adv. Lipid Res. 15 (1977) 1-60
12. Forstner G.G., Tanaka K., and Isselbacher K.J. Lipid composition of the isolated rat intestinal microvillus membrane. Biochem. J. 109 (1968) 51-59
13. Forstner G.G., and Wherrett J.R. Plasma membrane and mucosal glycosphingolipids in the rat intestine. Biochim. Biophys. Acta 306 (1973) 446-459
14. Hansson G.C., Simons K., and van Meer G. Two strains of the Madin-Darby canine kidney (MDCK) cell line have distinct glycosphingolipid compositions. EMBO J. 5 (1986) 483-489
15. Matlin K., Bainton D.F., Pesonen M., Louvard D., Genty N., and Simons K. Transepithelial transport of a viral membrane glycoprotein implanted into the apical plasma membrane of Madin-Darby canine kidney cells. I. Morphological evidence. J. Cell Biol. 97 (1983) 627-637
16. Matlin K.S., and Simons K. Sorting of an apical plasma membrane glycoprotein occurs before it reaches the cell surface in cultured epithelial cells. J. Cell Biol. 99 (1984) 2131-2139
17. Nagai Y., and Iwamori M. Brain and thymus gangliosides: their molecular diversity and its biological implications and a dynamic annular model for their function in cell surface membranes. Mol. Cell. Biochem. 29 (1980) 81-90
18. Tillack T.W., Allietta M., Moran R.E., and Young W.W.J. Localization of globoside and Forssman glycolipids on erythrocyte membranes. Biochim. Biophys. Acta 733 (1983) 15-24
19. Rock P., Allietta M., Young W.W.J., Thompson T.E., and Tillack T.W. Organization of glycosphingolipids in phosphatidylcholine bilayers: use of antibody molecules and Fab fragments as morphologic markers. Biochemistry 29 (1990) 8484-8490
20. M1 at low concentration are preferentially incorporated into the gel phase in two-component, two-phase phosphatidylcholine bilayers. Biochemistry 30 (1991) 19-25
21. Sorice M., Parolini I., Sansolini T., Garofalo T., Dolo V., Sargiacomo M., Tai T., Peschle C., Torrisi M.R., and Pavan A. Evidence for the existence of ganglioside-enriched plasma membrane domains in human peripheral lymphocytes. J. Lipid Res. 38 (1997) 969-980
22. Yamamura S., Handa K., and Hakomori S. A close association of GM3 with c-Src and Rho in GM3-enriched microdomains at the B16 melanoma cell surface membrane: a preliminary note. Biochem. Biophys. Res. Commun. 236 (1997) 218-222
23. Anderson R.G.W. The caveolae membrane system. Ann. Rev. Biochem. 67 (1998) 199-225
24. Rothberg K.G., Heuser J.E., Donzell W.C., Ying Y.-S., Glenney J.R., and Anderson R.G.W. Caveolin, a protein component of caveolae membrane coats. Cell 68 (1992) 673-682
25. Liu P., Rudick M., and Anderson R.G. Multiple functions of caveolin-1. J. Biol. Chem. 277 (2002) 41295-41298
26. 2+-ganglioside interaction in neuronal differentiation and development. In: Svennerholm L., Asbury A.K., Reisfeld R.A., Sandhoff K., Suzuki K., Tettamanti G., and Toffano G. (Eds). Biological function of gangliosides. Progress in Brain Research vol. 101 (1994), Elsevier, Amsterdam 127-145
27. Simons K., and Ikonen E. Functional rafts in cell membranes. Nature 387 (1997) 569-572
28. Bremer E.G., Hakomori S., Bowen-Pope D.F., Raines E.W., and Ross R. Ganglioside-mediated modulation of cell growth, growth factor binding, and receptor phosphorylation. J. Biol. Chem. 259 (1984) 6818-6825
29. 3 on tyrosine phosphorylation of the epidermal growth factor receptor. J. Biol. Chem. 261 (1986) 2434-2440
30. Stefanova I., Horejsi V., Ansotegui I.J., Knapp W., and Stockinger H. GPI-anchored cell-surface molecules complexed to protein tyrosine kinases. Science 254 (1991) 1016-1019
31. Krummel M.F., and Davis M.M. Dynamics of the immunological synapse: finding, establishing and solidifying a connection. Curr. Opin. Immunol. 14 (2002) 66-74
32. Hakomori S. The glycosynapse. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 225-232
33. Fenderson B.A., Zehavi U., and Hakomori S. A multivalent lacto-N-fucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J. Exp. Med. 160 (1984) 1591-1596
34. x determinants: a possible basis for cell recognition in preimplantation embryos and in embryonal carcinoma cells. J. Biol. Chem. 264 (1989) 9476-9484
35. x interaction, with new approaches: embryoglycan aggregation of F9 teratocarcinoma cells, and adhesion of various tumour cells based on Lex expression. Glycoconj. J. 11 (1994) 238-248
36. Peyrieras N., Hyafil F., Louvard D., Ploegh H.L., and Jacob F. Uvomorulin: a nonintegral membrane protein of early mouse embryo. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 6274-6277
37. Takeichi M. Cadherins: a molecular family essential for selective cell-cell adhesion and animal morphogenesis. Trends Genet. 3 (1987) 213-217
38. Siebert H.C., Born K., Andre S., Frank M., Kaltner H., von der Lieth C.W., Heck A.J., Jimenez-Barbero J., Kopitz J., and Gabius H.J. Carbohydrate chain of ganglioside GM1 as a ligand: identification of the binding strategies of three 15 mer peptides and their divergence from the binding modes of growth-regulatory galectin-1 and cholera toxin. Chemistry 12 (2005) 388-402
39. Elola M.T., Chiesa M.E., Alberti A.F., Mordoh J., and Fink N.E. Galectin-1 receptors in different cell types. J. Biomed. Sci. 12 (2005) 13-29
40. Geyer A., Gege C., and Schmidt R.R. Calcium-dependent carbohydrate-carbohydrate recognition between Lewis(X) blood group antigens. Angew. Chem., Int. Ed. Engl. 39 (2000) 3245-3249
41. de la Fuente J.M., and Penades S. Understanding carbohydrate-carbohydrate interactions by means of glyconanotechnology. Glycoconj. J. 21 (2004) 149-163
42. de la Fuente J.M., Eaton P., Barrientos A.G., Menendez M., and Penades S. Thermodynamic evidence for Ca2+-mediated self-aggregation of Lewis X gold glyconanoparticles. A model for cell adhesion via carbohydrate-carbohydrate interaction. J. Am. Chem. Soc. 127 (2005) 6192-6197
43. x glycan mediates homotypic adhesion of embryonal cells independently from E cadherin: a preliminary note. Biochem. Biophys. Res. Commun. 358 (2007) 247-252
44. Hakomori S. Carbohydrate-to-carbohydrate interaction in basic cell biology: a brief overview. Arch. Biochem. Biophys. 426 (2004) 173-181
45. Carvalho de Souza A., and Kamerling J.P. Analysis of carbohydrate-carbohydrate interactions using gold glyconanoparticles and oligosaccharide self-assembling monolayers. Methods Enzymol. 417 (2006) 221-243
46. Gourier C., Pincet F., Perez E., Zhang Y., Zhu Z., Mallet J.M., and Sinay P. The natural LewisX-bearing lipids promote membrane adhesion: influence of ceramide on carbohydrate-carbohydrate recognition. Angew. Chem., Int. Ed. Engl. 44 (2005) 1683-1687
47. Spillmann D. Carbohydrates in cellular recognition: from leucine-zipper to sugar-zipper?. Glycoconj. J. 11 (1994) 169-171
48. Tosin M., Muller-Bunz H., and Murphy P.V. Synthesis and X-ray single crystal structure of a bivalent glycocluster. Chem. Commun. (Camb.) (2004) 494-495
49. Murphy P.V., Muller-Bunz H., and Velasco-Torrijos T. The crystal structure of a cyclic glycolipid reveals a carbohydrate-carbohydrate interaction interface. Carbohydr. Res. 340 (2005) 1437-1440
50. Bird J.M., and Kimber S.J. Oligosaccharides containing fucose linked α(1,3) and α(1,4) to N-acetylglucosamine cause decompaction of mouse morulae. Dev. Biol. 104 (1984)
51. Misevic G.N., and Burger M.M. The species-specific cell-binding site of the aggregation factor from the sponge Microciona prolifera is a highly repetitive novel glycan containing glucuronic acid, fucose, and mannose. J. Biol. Chem. 265 (1990) 20577-20584
52. Spillmann D., Hard K., Thomas-Oates J., Vliegenthart J.F.G., Misevic G., Burger M.M., and Finne J. Characterization of a novel pyruvylated carbohydrate unit implicated in the cell aggregation of the marine sponge Microciona prolifera. J. Biol. Chem. 268 (1993) 13378-13387
53. Spillmann D., Thomas-Oates J.E., van Kuik J.A., Vliegenthart J.F.G., Misevic G., Burger M.M., and Finne J. Characterization of a novel sulfated carbohydrate unit implicated in the carbohydrate-carbohydrate-mediated cell aggregation of the marine sponge Microciona prolifera. J. Biol. Chem. 270 (1995) 5089-5097
54. Bucior I., Scheuring S., Engel A., and Burger M.M. Carbohydrate-carbohydrate interaction provides adhesion force and specificity for cellular recognition. J. Cell Biol. 165 (2004) 529-537
55. Bucior I., and Burger M.M. Carbohydrate-carbohydrate interaction as a major force initiating cell-cell recognition. Glycoconj. J. 21 (2004) 111-123
56. Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9 (1993) 317-321
57. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251 (1991) 1451-1455
58. x determinant antigens as measured by atomic force microscopy. Angew. Chem., Int. Ed. Engl. 40 (2001) 3052-3055
59. de la Fuente J.M., Barrientos A.G., Rojas T.C., Rojo J., Canada J., Fernandez A., and Penades S. Gold glyconanoparticles as water-soluble polyvalent models to study carbohydrate interactions. Angew. Chem., Int. Ed. Engl. 40 (2001) 2259-2261
60. Yoon S., Nakayama K., Takahashi N., Yagi H., Utkina N., Wang H.Y., Kato K., Sadilek M., and Hakomori S. Interaction of N-linked glycans, having multivalent GlcNAc termini, with GM3 ganglioside. Glycoconj. J. 23 (2006) 639-649
61. Yoon S., Nakayama K., Hikita T., Handa K., and Hakomori S. Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 18987-18991
62. Fernandes H., Cohen S., and Bishayee S. Glycosylation-induced conformational modification positively regulates receptor-receptor association: a study with an aberrant epidermal growth factor receptor (EGFRvIII/DEGFR) expressed in cancer cells. J. Biol. Chem. 276 (2001) 5375-5383
63. Kaida K., Morita D., Kanzaki M., Kamakura K., Motoyoshi K., Hirakawa M., and Kusunoki S. Ganglioside complexes as new target antigens in Guillain-Barre syndrome. Ann. Neurol. 56 (2004) 567-571
64. Kaida K., Morita D., Kanzaki M., Kamakura K., Motoyoshi K., Hirakawa M., and Kusunoki S. Anti-ganglioside complex antibodies associated with severe disability in GBS. J. Neuroimmunol. 182 (2007) 212-218
65. Ono M., Handa K., Withers D.A., and Hakomori S. Motility inhibition and apoptosis are induced by metastasis-suppressing gene product CD82 and its analogue CD9, with concurrent glycosylation. Cancer Res. 59 (1999) 2335-2339
66. Ono M., Handa K., Sonnino S., Withers D.A., Nagai H., and Hakomori S. GM3 ganglioside inhibits CD9-facilitated haptotactic cell motility: co-expression of GM3 and CD9 is essential in down-regulation of tumor cell motility and malignancy. Biochemistry 40 (2001) 6414-6421
67. Kawakami Y., Kawakami K., Steelant W.F.A., Ono M., Baek R.C., Handa K., Withers D.A., and Hakomori S. Tetraspanin CD9 is a "proteolipid", and its interaction with a3 integrin in microdomain is promoted by GM3 ganglioside, leading to inhibition of laminin-5-dependent cell motility. J. Biol. Chem. 277 (2002) 34349-34358
68. Hehlgans S., Haase M., and Cordes N. Signalling via integrins: implications for cell survival and anticancer strategies. Biochim. Biophys. Acta 1775 (2007) 163-180
69. Gu J., and Taniguchi N. Regulation of integrin functions by N-glycans. Glycoconj. J. 21 (2004) 9-15
70. Hemler M.E. Tetraspanin functions and associated microdomains. Nat. Rev., Mol. Cell Biol. 6 (2005) 801-811
71. Miyake M., Koyama M., Seno M., and Ikeyama S. Identification of the motility-related protein (MRP-1), recognized by monoclonal antibody M31-15, which inhibits cell motility. J. Exp. Med. 174 (1991) 1347-1354
72. Cajot J.-F., Sordat I., Silvestre T., and Sordat B. Differential display cloning identifies motility-related protein (MRP1/CD9) as highly expressed in primary compared to metastatic human colon carcinoma cells. Cancer Res. 57 (1997) 2593-2597
73. Kingsley D.M., Kozarsky K.F., Hobbie L., and Krieger M. Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase deficient mutant. Cell 44 (1986) 749-759
74. Krieger M., Reddy P., Kozarsky K., Kingsley D., Hobbie L., and Penman M. Analysis of the synthesis, intracellular sorting, and function of glycoproteins using a mammalian cell mutant with reversible glycosylation defects. Methods Cell Biol. 32 (1989) 57-84
75. Folch J., and Lees M.B. Proteolipides, a new type of tissue lipoproteins: their isolation from brain. J. Biol. Chem. 191 (1951) 807-817
76. Lee M., and Pope A. Jordi Folch-Pi. National Academy of Sciences Online Memoirs (2004) 1-12. http://www.nap.edu/readingroom/books/biomems/jfolch-pi.html www.nap.edu/readingroom/books/biomems/jfolch-pi.html
77. Miura Y., Kainuma M., Jiang H., Velasco H., Vogt P.K., and Hakomori S. Reversion of the Jun-induced oncogenic phenotype by enhanced synthesis of sialosyllactosylceramide (GM3 ganglioside). Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16204-16209
78. Toledo M.S., Suzuki E., Handa K., and Hakomori S. Cell growth regulation through GM3-enriched microdomain (glycosynapse) in human lung embryonal fibroblast WI38 and its oncogenic transformant VA13. J. Biol. Chem. 279 (2004) 34655-34664
79. Mitsuzuka K., Handa K., Satoh M., Arai Y., and Hakomori S. A specific microdomain ("glycosynapse 3") controls phenotypic conversion and reversion of bladder cancer cells through GM3-mediated interaction of alpha3beta1 integrin with CD9. J. Biol. Chem. 280 (2005) 35545-35553
80. Satoh M., Ito A., Nojiri H., Handa K., Numahata K., Ohyama C., Saito S., Hoshi S., and Hakomori S. Enhanced GM3 expression, associated with decreased invasiveness, is induced by brefeldin A in bladder cancer cells. Int. J. Oncol. 19 (2001) 723-731
81. Dong J.-T., Lamb P.W., Rinker-Schaeffer C.W., Vukanovic J., Ichikawa T., Isaacs J.T., and Barrett J.C. KAI1, a metastasis suppressor gene for prostate cancer on human chromosome 11p11.2. Science 268 (1995) 884-886
82. Dong J.T., Suzuki H., Pin S.S., Bova S., Schalken J.A., Isaacs W.B., Barrett J.C., and Isaacs J.T. Down-regulation of the KAI1 metastasis suppressor gene during the progression of human prostatic cancer infrequently involves gene mutation or allelic loss. Cancer Res. 56 (1996) 4387-4390
83. Adachi M., Taki T., Ieki Y., Huang C., Higashiyama M., and Miyake M. Correlation of KAII/CD82 gene expression with good prognosis in patients with non-small cell lung cancer. Cancer Res. 56 (1996) 1751-1755
84. Sridhar S.C., and Miranti C.K. Tetraspanin KAI1/CD82 suppresses invasion by inhibiting integrin-dependent crosstalk with c-Met receptor and Src kinases. Oncogene 25 (2006) 2367-2378
85. Birchmeier C., Birchmeier W., Gherardi E., and Vande Woude G.F. Met, metastasis, motility and more. Nat. Rev., Mol. Cell Biol. 4 (2003) 915-925
86. Todeschini A.R., Dos Santos J.N., Handa K., and Hakomori S. Ganglioside GM2-tetraspanin CD82 complex inhibits Met and its cross-talk with integrins, providing a basis for control of cell motility through glycosynapse. J. Biol. Chem. 282 (2007) 8123-8133
87. A.R. Todeschini, J.N. Dos Santos, K. Handa, S. Hakomori, Ganglioside GM2/GM3 complex affixed on silica nanospheres inhibits cell motility strongly through CD82/Met/integrin-mediated processes. Proc. Natl. Acad. Sci. U. S. A. (submited for publication).
88. Ono M., Handa K., Withers D.A., and Hakomori S. Glycosylation effect on membrane domain (GEM) involved in cell adhesion and motility: a preliminary note on functional α3, α5-CD82 glycosylation complex in ldlD 14 cells. Biochem. Biophys. Res. Commun. 279 (2000) 744-750
89. Hakomori S. Glycosylation defining cancer malignancy: new wine in an old bottle. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10231-10233
90. Mintz B., and Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc. Natl. Acad. Sci. U. S. A. 72 (1975) 3585-3589
91. Illmensee K., and Mintz B. Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts. Proc. Natl. Acad. Sci. U. S. A. 73 (1976) 549-553
92. Wang F., Hansen R.K., Radisky D., Yoneda T., Barcellos-Hoff M.H., Petersen O.W., Turley E.A., and Bissell M.J. Phenotypic reversion or death of cancer cells by altering signaling pathways in three-dimensional contexts. J. Natl. Cancer Inst. 94 (2002) 1494-1503
93. Kenny P.A., and Bissell M.J. Tumor reversion: correction of malignant behavior by microenvironmental cues. Int. J. Cancer 107 (2003) 688-695
94. Iwabuchi K., Zhang Y., Handa K., Withers D.A., Sinaÿ P., and Hakomori S. Reconstitution of membranes simulating "glycosignaling domain" and their susceptibility to lyso-GM3. J. Biol. Chem. 275 (2000) 15174-15181
95. Murozuka Y., Watanabe N., Hatanaka K., and Hakomori S. Lyso-GM3, its dimer, and multimer: Their synthesis, and their effect on epidermal growth factor-induced receptor tyrosine kinase. Glycoconj. J. 24 (2007) 551-563
96. Gu J., Fujibayashi A., Yamada K.M., and Sekiguchi K. Laminin-10/11 and fibronectin differentially prevent apoptosis induced by serum removal via phosphatidylinositol 3-kinase/Akt- and MEK1/ERK-dependent pathways. J. Biol. Chem. 277 (2002) 19922-19928
97. Hakomori S., and Ishizuka I. Glycolipids: Animal. Encyclopedia of Life Sciences (2001), Nature Publ. Group, London. http://www.els.net http://www.els.net
98. Garcia-Manyes S., Bucior I., Ros R., Anselmetti D., Sanz F., Burger M.M., and Fernàndez-Busquets X. Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans. J. Biol. Chem. 281 (2006) 5992-5999
99. Stewart R.J., and Boggs J.M. Dependence of the surface expression of the glycolipid cerebroside sulfate on its lipid environment: comparison of sphingomyelin and phosphatidylcholine. Biochemistry 29 (1990) 3644-3653
100. Boggs J.M., Wang H., Gao W., Arvanitis D.N., Gong Y., and Min W. A glycosynapse in myelin?. Glycoconj. J. 21 (2004) 97-110
101. Yu S., Kojima N., Hakomori S., Kudo S., Inoue S., and Inoue Y. Binding of rainbow trout sperm to egg is mediated by strong carbohydrate-to-carbohydrate interaction between (KDN)GM3 (deaminated neuraminyl ganglioside) and Gg3-like epitope. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2854-2859