Down-regulation of the epidermal growth factor receptor by altering N-glycosylation: Emerging role of β1,4-Galactosyltransferases

Anticancer Research

Volumn 32, Issue 5, 2012, Pages 1565-1572

  Gabius, Hans J ^a   Van De Wouwer, Marlies ^b,c   André, Sabine ^a   Villalobo, Antonio ^b  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

A431 cells; Autophosphorylation; CHO wild type; ErbB receptors; Galactosyltransferase; Glycosylation; HEK293; Lec1; Lec2; Lec8 and Lec19 mutant cells; Sialylation

Indexed keywords

BETA 1,4 GALACTOSYLTRANSFERASE; EPIDERMAL GROWTH FACTOR RECEPTOR; GALACTOSYLTRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; BIOTRANSFORMATION; CELL MEMBRANE; CELL STRAIN HEK293; CHO CELL; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIALYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; DOWN-REGULATION; GALACTOSYLTRANSFERASES; GLYCOSYLATION; HEK293 CELLS; HUMANS; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFECTION;

EID: 84861492200     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (37)

1. Takahashi M, Yokoe S, Asahi M, Lee SH, Li W, Osumi D, Miyoshi E and Taniguchi N: N-Glycan of ErbB family plays a crucial role in dimer formation and tumor promotion. Biochim Biophys Acta 1780: 520-524, 2008.
2. Zuber C and Roth J: N-Glycosylation. In: The Sugar Code. Fundamentals of Glycosciences. Gabius H-J (ed.). Weinheim, Germany, Wiley-VCH, pp. 87-110, 2009.
3. Hennet T: Diseases of glycosylation. In: The Sugar Code. Fundamentals of Glycosciences. Gabius H-J (ed.). Weinheim, Germany, Wiley-VCH, pp. 365-383, 2009.
4. Honke K and Taniguchi N: Animal models to delineate glycan functionality. In: The Sugar Code. Fundamentals of Glycosciences. Gabius H-J (ed.). Weinheim, Germany, Wiley-VCH, pp. 385-401, 2009.
5. André S, Kozár T, Schuberth R, Unverzagt C, Kojima S and Gabius H-J: Substitutions in the N-glycan core as regulators of biorecognition: the case of core-fucose and bisecting GlcNAc moieties. Biochemistry 46: 6984-6995, 2007. (Pubitemid 46906427)
6. André S, Kozár T, Kojima S, Unverzagt C and Gabius H-J: From structural to functional glycomics: core substitutions as molecular switches for shape and lectin affinity of N-glycans. Biol Chem 390: 557-565, 2009.
7. Gabius HJ, André S, Jiménez-Barbero J, Romero A and Solís D: From lectin structure to functional glycomics: principles of the sugar code. Trends Biochem Sci 36: 298-313, 2011.
8. Soderquist AM and Carpenter G: Glycosylation of the epidermal growth factor receptor in A431 cells. The contribution of carbohydrate to receptor function. J Biol Chem 259: 12586-12594, 1984. (Pubitemid 15203769)
9. Slieker LJ, Martensen TM and Lane MD: Synthesis of epidermal growth factor receptor in human A431 cells. Glycosylation-dependent acquisition of ligand binding activity occurs post-translationally in the endoplasmic reticulum. J Biol Chem 261: 15233-15241, 1986. (Pubitemid 17218102)
10. Gamou S and Shimizu N: Glycosylation of the epidermal growth factor receptor and its relationship to membrane transport and ligand binding. J Biochem 104: 388-396, 1988.
11. Rebbaa A, Yamamoto H, Saito T, Meuillet E, Kim P, Kersey DS, Bremer EG, Taniguchi N and Moskal JR: Gene transfection-mediated overexpression of β1,4-N-acetylglucosamine bisecting oligosaccharides in glioma cell line U373 MG inhibits epidermal growth factor receptor function. J Biol Chem 272: 9275-9279, 1997. (Pubitemid 27154938)
12. Sato Y, Takahashi M, Shibukawa Y, Jain SK, Hamaoka R, Miyagawa J, Yaginuma Y, Honke K, Ishikawa M and Taniguchi N: Overexpression of N-acetylglucosaminyltransferase III enhances the epidermal growth factor-induced phosphorylation of ERK in HeLaS3 cells by up-regulation of the internalization rate of the receptors. J Biol Chem 276: 11956-11962, 2001.
13. Wang X, Gu J, Ihara H, Miyoshi E, Honke K and Taniguchi N: Core fucosylation regulates epidermal growth factor receptor-mediated intracellular signaling. J Biol Chem 281: 2572-2577, 2006. (Pubitemid 43845717)
14. Matsumoto K, Yokote H, Arao T, Maegawa M, Tanaka K, Fujita Y, Shimizu C, Hanafusa T, Fujiwara Y and Nishio K: N-Glycan fucosylation of epidermal growth factor receptor modulates receptor activity and sensitivity to epidermal growth factor receptor tyrosine kinase inhibitor. Cancer Sci 99: 1611-1617, 2008.
15. Liu YC, Yen HY, Chen CY, Chen CH, Cheng PF, Juan YH, Khoo KH, Yu CJ, Yang PC, Hsu TL and Wong CH: Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc Natl Acad Sci USA 108: 11332-11337, 2011.
16. Zeng FY, Benguria A, Kafert S, André S, Gabius H-J and Villalobo A: Differential response of the epidermal growth factor receptor tyrosine kinase activity to several plant and mammalian lectins. Mol Cell Biochem 142: 117-124, 1995.
17. Kaltner H and Gabius H-J: A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol Histopathol 27: 397-416, 2012.
18. Contessa JN, Bhojani MS, Freeze HH, Rehemtulla A and Lawrence TS: Inhibition of N-linked glycosylation disrupts receptor tyrosine kinase signaling in tumor cells. Cancer Res 68: 3803-3809, 2008.
19. Ling YH, Li T, Perez-Soler R and Haigentz M Jr.: Activation of ER stress and inhibition of EGFR N-glycosylation by tunicamycin enhances susceptibility of human non-small cell lung cancer cells to erlotinib. Cancer Chemother Pharmacol 64: 539-548, 2009.
20. Patnaik SK and Stanley P: Lectin-resistant CHO glycosylation mutants. Methods Enzymol 416: 159-182, 2006. (Pubitemid 44750110)
21. Smith KD, Davies MJ, Bailey D, Renouf DV and Hounsell EF: Analysis of the glycosylation patterns of the extracellular domain of the epidermal growth factor receptor expressed in Chinese hamster ovary fibroblasts. Growth Factors 13: 121-132, 1996. (Pubitemid 26193747)
22. Sato C, Kim JH, Abe Y, Saito K, Yokoyama S and Kohda D: Characterization of the N-oligosaccharides attached to the atypical Asn-X-Cys sequence of recombinant human epidermal growth factor receptor. J Biochem 127: 65-72, 2000. (Pubitemid 30094095)
23. Lee J, Park SH, Sundaram S, Raju TS, Shaper NL and Stanley P: A mutation causing a reduced level of expression of six β4-galctosyltransferase genes is the basis of the Lec19 CHO glycosylation mutant. Biochemistry 42: 12349-12357, 2003. (Pubitemid 37296511)
24. Stanley P, Sallustio S, Krag SS and Dunn B: Lectin-resistant CHO cells: selection of seven new mutants resistant to ricin. Somat Cell Mol Genet 16: 211-223, 1990. (Pubitemid 20214469)
25. Guo S, Sato T, Shirane K and Furukawa K: Galactosylation of N-linked oligosaccharides by human β1,4-galactosyltransferases I, II, III, IV, V, and VI expressed in Sf-9 cells. Glycobiology 11: 813-820, 2001. (Pubitemid 32982662)
26. Sato T, Guo S and Furukawa K: Occurrence of poly-N-acetyllactosamine synthesis in Sf-9 cells upon transfection of individual human β1,4-galactosyltransferase I, II, III, IV, V and VI cDNAs. Biochimie 83: 719-725, 2001. (Pubitemid 32821236)
27. Hennet T: The galactosyltransferase family. Cell Mol Life Sci 59: 1081-1095, 2002.
28. INK4a: modulator of glycomic profile and galectin-1 expression to increase susceptibility to carbohydrate-dependent induction of anoikis in pancreatic carcinoma cells. FEBS J 274: 3233-3256, 2007.
29. André S, Kopitz J, Kaltner H, Villalobo A and Gabius H-J: Glycans as functional markers in malignancy? In: The Sugar Code. Fundamentals of Glycosciences. Gabius H-J (ed.). Weinheim, Germany, Wiley-VCH, pp. 419-432, 2009.
30. Xu S, Zhu X, Zhang S, Yin S, Zhou L, Chen C and Gu J: Overexpression of β1,4-galactosyltransferase I, II, and V in human astrocytoma. J Cancer Res Clin Oncol 127: 502-506, 2001.
31. Chen X, Jiang J, Yang J, Chen C, Sun M, Wei Y, Guang X and Gu J: Down-regulation of the expression of β1,4-galactosyltransferase V promotes integrin β1 maturation. Biochem Biophys Res Commun 343: 910-916, 2006. (Pubitemid 46137866)
32. Jiang J, Chen X, Shen J, Wei Y, Wu T, Yang Y, Wang H, Zong H, Yang J, Zhang S, Xie J, Kong X, Liu W and Gu J: β1,4-Galactosyltransferase V functions as a positive growth regulator in glioma. J Biol Chem 281: 9482-9489, 2006. (Pubitemid 43864665)
33. Jiang J, Shen J, Wu T, Wei Y, Chen X, Zong H, Zhang S, Sun M, Xie J, Kong X, Yang Y, Shen A, Wang H and Gu J: Down-regulation of β1,4- galactosyltransferase V is a critical part of etoposide-induced apoptotic process and could be mediated by decreasing SP1 levels in human glioma cells. Glycobiology 16: 1045-1051, 2006. (Pubitemid 44530697)
34. Chen WS, Chang HY, Li CP, Liu JM and Huang TS: Tumor β1,4- galactosyltransferase IV overexpression is closely associated with colorectal cancer metastasis and poor prognosis. Clin Cancer Res 11: 8615-8622, 2005. (Pubitemid 43005908)
35. Li Z, Zong H, Kong X, Zhang S, Wang H, Sun Q and Gu J: Cell surface β1,4-galactosyltransferase 1 promotes apoptosis by inhibiting epidermal growth factor receptor pathway. Mol Cell Biochem 291: 69-76, 2006. (Pubitemid 44725304)
36. Dricu A, Carlberg M, Wang M and Larsson O: Inhibition of N-linked glycosylation using tunicamycin causes cell death in malignant cells: role of down-regulation of the insulin-like growth factor 1 receptor in induction of apoptosis. Cancer Res 57: 543-548, 1997. (Pubitemid 27081677)
37. Asano M, Furukawa K, Kido M, Matsumoto S, Umesaki Y, Kochibe N and Iwakura Y: Growth retardation and early death of β1,4-galactosyltransferase knock-out mice with augmented proliferation and abnormal differentiation of epithelial cells. EMBO J 16: 1850-1857, 1997. (Pubitemid 27170946)