Knockdown of GnT-Va expression inhibits ligand-induced downregulation of the epidermal growth factor receptor and intracellular signaling by inhibiting receptor endocytosis

Glycobiology

Volumn 19, Issue 5, 2009, Pages 547-559

  Guo, Hua Bei ^a   Johnson, Heather ^a   Randolph, Matthew ^a   Lee, Intaek ^b   Pierce, Michael ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EGFR; Endocytosis; GnT V; N glycan

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GALECTIN; N ACETYLGLUCOSAMINYLTRANSFERASE; SMALL INTERFERING RNA;

ARTICLE; ATTENUATION; CANCER CELL CULTURE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UBIQUITINATION;

CELL LINE, TUMOR; DISACCHARIDES; DOWN-REGULATION; ENDOCYTOSIS; GALECTINS; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROTEIN MULTIMERIZATION; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 64549101115     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp023     Document Type: Article

References (70)

1. Abbott KL, Troupe K, Lee I, Pierce M. 2006. Integrin-dependent neuroblastoma cell adhesion and migration on laminin is regulated by expression levels of two enzymes in the O-mannosyl-linked glycosylation pathway, PomGnT1 and GnT-Vb. Exp Cell Res. 312:2837-2850.
2. Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, et al. 1994. Galectins: A family of animal beta-galactoside-binding lectins. Cell. 76:597-598.
3. Brewer CF, Miceli MC, Baum LG. 2002. Clusters, bundles, arrays and lattices: Novel mechanisms for lectin-saccharide-mediated cellular interactions. Curr Opin Struct Biol. 12:616-623.
4. Brockhausen I, Carver JP, Schachter H. 1988. Control of glycoprotein synthesis. The use of oligosaccharide substrates and HPLC to study the sequential pathway for N-acetylglucosaminyltransferases I, II, III, IV, V, and VI in the biosynthesis of highly branched N glycans by hen oviduct membranes. Biochem Cell Biol. 66:1134-1151.
5. Camby I, Le Mercier M, Lefranc F, Kiss R. 2006. Galectin-1: A small protein with major functions. Glycobiology. 16:137R-157R.
6. Ceresa BP, Schmid SL. 2000. Regulation of signal transduction by endocytosis. Curr Opin Cell Biol. 12:204-210.
7. Clague MJ, Urbe S. 2001. The interface of receptor trafficking and signalling. J Cell Sci. 114:3075-3081.
8. Demetriou M, Nabi IR, Coppolino M, Dedhar S, Dennis JW. 1995. Reduced contact-inhibition and substratum adhesion in epithelial cells expressing GlcNAc-transferase V. J Cell Biol. 130:383-392.
9. Di Fiore PP, De Camilli P. 2001. Endocytosis and signaling. An inseparable partnership. Cell. 106:1-4.
10. Di Fiore PP, Gill GN. 1999. Endocytosis and mitogenic signaling. Curr Opin Cell Biol. 11:483-488.
11. Di Guglielmo GM, Baass PC, Ou WJ, Posner BI, Bergeron JJ. 1994. Compartmentalization of SHC, GRB2 and mSOS, and hyperphosphorylation of Raf-1 by EGF but not insulin in liver parenchyma. Embo J. 13:4269-4277.
12. Dikic I, Giordano S. 2003. Negative receptor signalling. Curr Opin Cell Biol. 15:128-135.
13. Dumic J, Dabelic S, Flogel M. 2006. Galectin-3: An open-ended story. Biochim Biophys Acta. 1760:616-635.
14. Grandal MV, Madshus IH. 2008. Epidermal growth factor receptor and cancer: Control of oncogenic signalling by endocytosis. J Cell Mol Med.
15. Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW. 2000. Suppression of tumor growth and metastasis in Mgat5-deficient mice. Nat Med. 6:306-312.
16. Greenfield C, Hiles I, Waterfield MD, Federwisch M, Wollmer A, Blundell TL, McDonald N. 1989. Epidermal growth factor binding induces a conformational change in the external domain of its receptor. Embo J 8:4115-4123.
17. Guo HB, Lee I, Bryan BT, Pierce M. 2005. Deletion of mouse embryo fibroblast N-acetylglucosaminyltransferase V stimulates alpha5beta1 integrin expression mediated by the protein kinase C signaling pathway. J Biol Chem. 280:8332-8342.
18. Guo HB, Lee I, Kamar M, Akiyama SK, Pierce M. 2002. Aberrant N lycosylation of beta1 integrin causes reduced alpha5beta1 integrin clustering and stimulates cell migration. Cancer Res. 62:6837-6845.
19. Guo HB, Lee I, Kamar M, Pierce M. 2003. N Acetylglucosaminyltransferase V expression levels regulate cadherin-associated homotypic cell-cell adhesion and intracellular signaling pathways. J Biol Chem. 278:52412-52424.
20. Guo HB, Nairn A, Harris K, Randolph M, Alvarez-Manilla G, Moremen K, Pierce M. 2008. Loss of expression of N acetylglucosaminyltransferase Va results in altered gene expression of glycosyltransferases and galectins. FEBS Lett. 582:527-535.
21. Guo HB, Randolph M, Pierce M. 2007. Inhibition of a specific N glycosylation activity results in attenuation of breast carcinoma cell invasiveness-related phenotypes: Inhibition of epidermal growth factor-induced dephosphorylation of focal adhesion kinase. J Biol Chem. 282:22150-22162.
22. Guo P, Wang QY, Guo HB, Shen ZH, Chen HL. 2004. N cetylglucosaminyltransferase V modifies the signaling pathway of epidermal growth factor receptor. Cell Mol Life Sci. 61:1795-1804.
23. Haglund K, Sigismund S, Polo S, Szymkiewicz I, Di Fiore PP, Dikic I. 2003. Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol. 5:461-466.
24. Hakomori S. 2002. Glycosylation defining cancer malignancy: New wine in an old bottle. Proc Natl Acad Sci USA. 99:10231-10233.
25. Handerson T, Camp R, Harigopal M, Rimm D, Pawelek J. 2005. Beta1,6branched oligosaccharides are increased in lymph node metastases and predict poor outcome in breast carcinoma. Clin Cancer Res. 11:2969-2973.
26. Huang F, Goh LK, Sorkin A. 2007. EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA. 104:16904-16909.
27. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. 2006. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell. 21:737-748.
28. Isaji T, Gu J, Nishiuchi R, Zhao Y, Takahashi M, Miyoshi E, Honke K, Sekiguchi K, Taniguchi N. 2004. Introduction of bisecting GlcNAc into integrin alpha5beta1 reduces ligand binding and down-regulates cell adhesion and cell migration. J Biol Chem. 279:19747-19754.
29. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, Liu YC. 1999. The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science. 286:309-312.
30. Kotani N, Gu J, Isaji T, Udaka K, Taniguchi N, Honke K. 2008. Biochemical visualization of cell surface molecular clustering in living cells. Proc Natl Acad Sci USA. 105:7405-7409.
31. Lajoie P, Partridge EA, Guay G, Goetz JG, Pawling J, Lagana A, Joshi B, Dennis JW, Nabi IR. 2007. Plasma membrane domain organization regulates EGFR signaling in tumor cells. J Cell Biol. 179:341-356.
32. Lemmon MA, Bu Z, Ladbury JE, Zhou M, Pinchasi D, Lax I, Engelman DM, Schlessinger J. 1997. Two EGF molecules contribute additively to stabilization of the EGFR dimer. Embo J. 16:281-294.
33. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, Alroy I, Lavi S, Iwai K, Reiss Y, Ciechanover A, et al. 1999. Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell. 4:1029-1040.
34. Lua BL, Low BC. 2005. Activation of EGF receptor endocytosis and ERK1/2 signaling by BPGAP1 requires direct interaction with EEN/endophilin II and a functional RhoGAP domain. J Cell Sci. 118:2707-2721.
35. Marmor MD, Yarden Y. 2004. Role of protein ubiquitylation in regulating endocytosis of receptor tyrosine kinases. Oncogene. 23:2057-2070.
36. Mosesson Y, Shtiegman K, Katz M, Zwang Y, Vereb G, Szollosi J, Yarden Y. 2003. Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J Biol Chem. 278:21323-21326.
37. Ohtsubo K, Takamatsu S, Minowa MT, Yoshida A, Takeuchi M, Marth JD. 2005. Dietary and genetic control of glucose transporter 2 glycosylation promotes insulin secretion in suppressing diabetes. Cell. 123:1307-1321.
38. Padron D, Sato M, Shay JW, Gazdar AF, Minna JD, Roth MG. 2007. Epidermal growth factor receptors with tyrosine kinase domain mutations exhibit reduced Cbl association, poor ubiquitylation, and down-regulation but are efficiently internalized. Cancer Res. 67:7695-7702.
39. Palmieri D, Bouadis A, Ronchetti R, Merino MJ, Steeg PS. 2006. Rab11a differentially modulates epidermal growth factor-induced proliferation and motility in immortal breast cells. Breast Cancer Res Treat. 100:127-137.
40. Partridge EA, Le Roy C, Di Guglielmo GM, Pawling J, Cheung P, Granovsky M, Nabi IR, Wrana JL, Dennis JW. 2004. Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis. Science. 306:120-124.
41. Pawson T. 1995. Protein modules and signalling networks. Nature. 373: 573-580.
42. Pawson T. 1997. New impressions of Src and Hck. Nature. 385:582-583, 585.
43. Pennock S, Wang Z. 2003. Stimulation of cell proliferation by endosomal epidermal growth factor receptor as revealed through two distinct phases of signaling. Mol Cell Biol. 23:5803-5815.
44. Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. 2007. Functions of cell surface galectin-glycoprotein lattices. Curr Opin Struct Biol. 17:513-520.
45. Ramasamy S, Duraisamy S, Barbashov S, Kawano T, Kharbanda S, Kufe D. 2007. The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop. Mol Cell. 27:992-1004.
46. Ravid T, Heidinger JM, Gee P, Khan EM, Goldkorn T. 2004. c-Cbl-mediated ubiquitinylation is required for epidermal growth factor receptor exit from the early endosomes. J Biol Chem. 279:37153-37162.
47. Ren Y, Cheng L, Rong Z, Li Z, Li Y, Zhang X, Xiong S, Hu J, Fu XY, Chang Z. 2008. hSef potentiates EGF-mediated MAPK signaling through affecting EGFR trafficking and degradation. Cell Signal. 20:518-533.
48. Sato Y, Takahashi M, Shibukawa Y, Jain SK, Hamaoka R, Miyagawa J, Yaginuma Y, Honke K, Ishikawa M, Taniguchi N. 2001. 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.
49. Seales EC, Jurado GA, Brunson BA, Wakefield JK, Frost AR, Bellis SL. 2005. Hypersialylation of beta1 integrins, observed in colon adenocarcinoma, may contribute to cancer progression by up-regulating cell motility. Cancer Res. 65:4645-4652.
50. Sebastian S, Settleman J, Reshkin SJ, Azzariti A, Bellizzi A, Paradiso A. 2006. The complexity of targeting EGFR signalling in cancer: From expression to turnover. Biochim Biophys Acta. 1766:120-139.
51. Seelentag WK, Li WP, Schmitz SF, Metzger U, Aeberhard P, Heitz PU, Roth J. 1998. Prognostic value of beta1,6-branched oligosaccharides in human colorectal carcinoma. Cancer Res. 58:5559-5564.
52. Shen Y, Xu L, Foster DA. 2001. Role for phospholipase D in receptor-mediated endocytosis. Mol Cell Biol. 21:595-602.
53. Sigismund S, Argenzio E, Tosoni D, Cavallaro E, Polo S, Di Fiore PP. 2008. Clathrin-mediated internalization is essential for sustained EGFR signaling but dispensable for degradation. Dev Cell. 15:209-219.
54. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S. 2005. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA. 102:2760-2765.
55. Sorkin A, Carpenter G. 1991. Dimerization of internalized epidermal growth factor receptors. J Biol Chem. 266:23453-23460.
56. Sorkin A, Von Zastrow M. 2002. Signal transduction and endocytosis: Close encounters of many kinds. Nat Rev Mol Cell Biol. 3:600-614.
57. Suyama K, Shapiro I, Guttman M, Hazan RB. 2002. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell. 2:301-314.
58. Tanos B, Pendergast AM. 2006. Abl tyrosine kinase regulates endocytosis of the epidermal growth factor receptor. J Biol Chem. 281:32714-32723.
59. Tsuda T, Ikeda Y, Taniguchi N. 2000. The Asn-420-linked sugar chain in human epidermal growth factor receptor suppresses ligand-independent spontaneous oligomerization. Possible role of a specific sugar chain in controllable receptor activation. J Biol Chem. 275:21988-21994.
60. Ullrich A, Coussens L, Hayflick JS, Dull TJ, Gray A, Tam AW, Lee J, Yarden Y, Libermann TA, Schlessinger J, et al. 1984. Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells. Nature. 309:418-425.
61. Vagin O, Tokhtaeva E, Yakubov I, Shevchenko E, Sachs G. 2008. Inverse correlation between the extent of N-glycan branching and intercellular adhesion in epithelia. Contribution of the Na,K-ATPase beta1 subunit. J Biol Chem. 283:2192-2202.
62. V ieira AV, L amaze C, Schmid SL. 1996. Control of EGF receptor signaling by clathrin-mediated endocytosis. Science. 274:2086-2089.
63. Wang Q, Villeneuve G, Wang Z. 2005. Control of epidermal growth factor receptor endocytosis by receptor dimerization, rather than receptor kinase activation. EMBO Rep. 6:942-948.
64. Wang Y, Pennock S, Chen X,Wang Z. 2002. Endosomal signaling of epidermal growth factor receptor stimulates signal transduction pathways leading to cell survival. Mol Cell Biol. 22:7279-7290.
65. Waterman H, Katz M, Rubin C, Shtiegman K, Lavi S, Elson A, Jovin T, Yarden Y. 2002. Amutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling. Embo J. 21:303-313.
66. Wong A, Lamothe B, Lee A, Schlessinger J, Lax I. 2002. FRS2 alpha attenuates FGF receptor signaling byGrb2-mediated recruitment of the ubiquitin ligase Cbl. Proc Natl Acad Sci USA. 99:6684-6689.
67. Wu Y, Chen L, Cao L, Sheng W, Yang BB. 2004. Overexpression of the C-terminal PG-M/versican domain impairs growth of tumor cells by intervening in the interaction between epidermal growth factor receptor and beta1-integrin. J Cell Sci. 117:2227-2237.
68. Yamamoto H, Swoger J, Greene S, Saito T, Hurh J, Sweeley C, Leestma J, Mkrdichian E, Cerullo L, Nishikawa A, et al. 2000. Beta1,6-N acetylglucosamine -bearing N-glycans in human gliomas: Implications for a role in regulating invasivity. Cancer Res. 60:134-142.
69. Yarden Y, Sliwkowski MX. 2001. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol. 2:127-137.
70. Yoshimura M, Ihara Y, Matsuzawa Y, Taniguchi N. 1996. Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J Biol Chem. 271:13811-13815.