Regulation of epidermal growth factor receptor through interaction of ganglioside GM3 with GlcNAc of N-Linked glycan of the receptor: Demonstration in ldlD cells

Neurochemical Research

Volumn 36, Issue 9, 2011, Pages 1645-1653

  Guan, Feng ^a,b   Handa, Kazuko ^a,b   Hakomori, Sen Itiroh ^a,b  

^a PACIFIC NORTHWEST RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Carbohydrate carbohydrate interaction; Epidermal growth factor receptor (EGFR); Ganglioside GM3; GlcNAc termini; LdlD cells; N linked glycan

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GALACTOSE; GANGLIOSIDE GM3; ISOMERASE; N ACETYLGLUCOSAMINE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE 4 EPIMERASE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL MOTILITY; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACETYLGLUCOSAMINE; ANIMALS; CELL MOVEMENT; CHO CELLS; CRICETINAE; CRICETULUS; EPIDERMAL GROWTH FACTOR; G(M3) GANGLIOSIDE; PHOSPHORYLATION; POLYSACCHARIDES; RECEPTOR, EPIDERMAL GROWTH FACTOR;

EID: 80755163563     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-010-0379-9     Document Type: Article

References (42)

1. Cohen S, Carpenter G, King L (1980) Epidermal growth factor receptor-protein kinase interactions: Co-purification of receptor and epidermal growth factor-enhanced phosphorylation activity. J Biol Chem 255:4834-4842
2. Ushiro H, Cohen S (1980) Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in A431 cell membranes. J Biol Chem 255:8363-8365
3. Hakomori S, Murakami WT (1968) Glycolipids of hamster fibroblasts and derived malignant-transformed cell lines. Proc Natl Acad Sci USA 59:254-261
4. Sakiyama H, Gross SK, Robbins PW (1972) Glycolipid synthesis in normal and virus-transformed hamster cell lines. Proc Natl Acad Sci USA 69:872-876
5. Chandrabose KA, Graham JM, Macpherson IA (1976) Glycolipid glycosyl transferases of a hamster cell line in culture. II. Subcellular distribution and the effect of culture age and density. Biochim Biophys Acta 429:112-122
6. Langenbach R, Kennedy S (1978) Gangliosides and their cell density-dependent changes in control and chemically transformed C3H/10T1/2 cells. Exp Cell Res 112:361-372 (Pubitemid 8314153)
7. Bremer EG, Schlessinger J, Hakomori S (1986) Gangliosidemediated modulation of cell growth: Specific effects of GM3 on tyrosine phosphorylation of the epidermal growth factor receptor. J Biol Chem 261:2434-2440 (Pubitemid 17205183)
8. Bremer EG, Hakomori S, Bowen-Pope DF et al (1984) Ganglioside- mediated modulation of cell growth, growth factor binding, and receptor phosphorylation. J Biol Chem 259:6818-6825 (Pubitemid 14078977)
9. Toledo MS, Suzuki E, Handa K et al (2004) Cell growth regulation through GM3-enriched microdomain (glycosynapse) in human lung embryonal fibroblast WI38 and its oncogenic transformant VA13. J Biol Chem 279:34655-34664 (Pubitemid 39318095)
10. Mutoh T, Tokuda A, Miyada T et al (1995) Ganglioside GM1 binds to the Trk protein and regulates receptor function. Proc Natl Acad Sci USA 92:5087-5091
11. Nojiri H, Stroud MR, Hakomori S (1991) A specific type of ganglioside as a modulator of insulin-dependent cell growth and insulin receptor tyrosine kinase activity: Possible association of ganglioside-induced inhibition of insulin receptor function and monocytic differentiation induction in HL60 cells. J Biol Chem 266:4531-4537 (Pubitemid 21909389)
12. Weis FMB, Davis RJ (1990) Regulation of epidermal growth factor receptor signal transduction: Role of gangliosides. J Biol Chem 265:12059-12066
13. Kingsley DM, Kozarsky KF, Hobbie L et al (1986) Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP-Gal/UDP-GalNAc 4-epimerase deficient mutant. Cell 44:749-759 (Pubitemid 16073971)
14. Yoon S, Nakayama K, Hikita T et al (2006) Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc Natl Acad Sci USA 103:18987-18991 (Pubitemid 350002815)
15. Kawashima N, Yoon SJ, Itoh K et al (2009) Tyrosine kinase activity of epidermal growth factor receptor is regulated by GM3 binding through carbohydrate to carbohydrate interactions. J Biol Chem 284:6147-6155
16. Symington FW, Fenderson BA, Hakomori S (1984) Fine specificity of a monoclonal anti-testicular cell antibody for glycolipids with terminal N-acetyl-D-glucosamine structure. Mol Immunol 21:877-882 (Pubitemid 15202662)
17. Guan F, Handa K, Hakomori S (2009) Specific glycosphingolipids mediate epithelial-to-mesenchymal transition of human and mouse epithelial cell lines. Proc Natl Acad Sci USA 106:7461-7466
18. Mitsuzuka K, Handa K, Satoh M et al (2005) A specific microdomain ("glycosynapse 3") controls phenotypic conversion and reversion of bladder cancer cells throughGM3-mediated interaction of alpha3beta1 integrin with CD9. J Biol Chem 280:35545-35553 (Pubitemid 41532746)
19. Krieger M (1983) Complementation of mutations in the LDL pathway of receptor-mediated endocytosis by cocultivation of LDL receptor-defective hamster cell mutants. Cell 33:413-422 (Pubitemid 13062493)
20. Ono M, Handa K, Withers DA et al (1999) Motility inhibition and apoptosis are induced by metastasis-suppressing gene product CD82 and its analogue CD9, with concurrent glycosylation. Cancer Res 59:2335-2339 (Pubitemid 29242279)
21. Ono M, Handa K, Sonnino S et al (2001) 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 40:6414-6421 (Pubitemid 32472731)
22. Kawakami Y, Kawakami K, Steelant WFA et al (2002) 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 277:34349-34358
23. Kobata A (1996) Cancer cells and metastasis: The Warren-Glick phenomenon: Basis of tumorigenesis and metastasis. In: Montreuil J, Vliegenthart JFG, Schachter H (eds) Glycoproteins and disease. Elsevier Science, Amsterdam, pp 211-227
24. Yamashita K, Kamerling JP, Kobata A (1982) Structural study of the carbohydrate moiety of hen ovomucoid: Occurrence of a series of pentaantennary complex-type asparagine-linked sugar chains. J Biol Chem 257:12809-12814
25. Shankar Iyer PN, Wilkinson KD, Goldstein IJ (1976) An N-acetyl-D-glycosamine binding lectin from Bandeiraea simplicifolia seeds. Arch Biochem Biophys 177:330-333
26. Eggens I, Fenderson BA, Toyokuni T et al (1989) Specific interaction between Lex and Lex determinants: A possible basis for cell recognition in preimplantation embryos and in embryonal carcinoma cells. J Biol Chem 264:9476-9484 (Pubitemid 19157590)
27. Kojima N, Fenderson BA, Stroud MR et al (1994) Further studies on cell adhesion based on Lex-Lex interaction, with new approaches: Embryoglycan aggregation of F9 teratocarcinoma cells, and adhesion of various tumour cells based on Lex expression. Glycoconj J 11:238-248 (Pubitemid 24300506)
28. Handa K, Kojima N, Hakomori S (2000) Analysis of glycolipiddependent cell adhesion based on carbohydrate-carbohydrate interaction. Meth Enzymol 312:447-458
29. Yoon S, Nakayama K, Takahashi N et al (2006) Interaction of N-linked glycans, having multivalent GlcNAc termini, with GM3 ganglioside. Glycoconj J 23:639-649 (Pubitemid 44934188)
30. Schlessinger J (1988) Signal transduction by allosteric receptor oligomerization. Trends Biochem Sci (TIBS) 13:443-447 (Pubitemid 18264445)
31. Ullrich A, Schlessinger J (1990) Signal transduction by receptors with tyrosine kinase activity. Cell 61:203-212
32. Zhou Q, Hakomori S, Kitamura K et al (1994) GM3 directly inhibits tyrosine phosphorylation and de-N-acetyl-GM3 directly enhances serine phosphorylation of epidermal growth factor receptor, independently of receptor-receptor interaction. J Biol Chem 269:1959-1965
33. Lee L, Abe A, Shayman JA (1999) Improved inhibitors of glucosylceramide synthase. J Biol Chem 274:14662-14669
34. Park S-Y, Yoon S-J, Freire-de-Lima L et al (2009) Control of cell motility by interaction of gangliosides, tetraspanins, and epidermal growth factor receptor in A431 vs. Kb epidermoid tumor cells. Carbohydr Res 344:1479-1486
35. Rebbaa A, Yamamoto H, Moskal JR et al (1996) Binding of erythroagglutinating phytohemagglutinin lectin from Phaseolus vulgaris to the epidermal growth factor receptor inhibits receptor function in the human glioma cell line, U373 MG. J Neurochem 67:2265-2272 (Pubitemid 26392495)
36. Rebbaa A, Yamamoto H, Saito T et al (1997) Gene transfectionmediated overexpression of b1,4 GlcNAc bisecting oligosaccharide structure in a glioma cell line, U373MG, inhibits EGF receptor function. J Biol Chem 272:9275-9280
37. Schachter H (1986) Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem Cell Biol 64:163-181 (Pubitemid 16036405)
38. Kang R, Saito H, Ihara Y et al (1996) Transcriptional regulation of the N-acetylglucosaminyltransferase V gene in human bile duct carcinoma cells (HuCC-T1) is mediated by Ets-1. J Biol Chem 271:26706-26712 (Pubitemid 26359077)
39. Buckhaults P, Chen L, Freigen N et al (1997) Transcriptional regulation of N-acetylglucosaminyltransferase V by the src oncogene. J Biol Chem 272:19575-19581 (Pubitemid 27337760)
40. Yoshimura M, Nishikawa A, Ihara Y et al (1995) Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA 92:8754-8758
41. Yoshimura M, Ihara Y, Matsuzawa Y et al (1996) Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J Biol Chem 271:13811-13815 (Pubitemid 26185425)
42. Cummings RD, Kornfeld S (1982) Characterization of structural determinants required for the high-affinity interaction of asparagine- linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem 257:11230-11234