Implication of N-acetylglucosaminyltransferases III and V in cancer: Gene regulation and signaling mechanism

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1455, Issue 2-3, 1999, Pages 287-300

  Taniguchi, Naoyuki ^a   Miyoshi, Eiji ^a   Ko, Jeong Heon ^a   Ikeda, Yoshitaka ^a   Ihara, Yoshito ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Cancer; Gene regulation; N Acetylglucosaminyltransferase III; N Acetylglucosaminyltransferase V; Signaling

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOPROTEIN; ISOENZYME; N ACETYLGLUCOSAMINYLTRANSFERASE; NERVE GROWTH FACTOR RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

ANGIOGENESIS; CANCER; CANCER INVASION; GENE CONTROL; GENE EXPRESSION; HUMAN; LIVER; LIVER CARCINOGENESIS; LUNG METASTASIS; MELANOMA CELL; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CARBOHYDRATE SEQUENCE; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR SEQUENCE DATA; N-ACETYLGLUCOSAMINYLTRANSFERASES; NEOPLASM METASTASIS; NEOPLASMS; PROTO-ONCOGENE PROTEIN C-ETS-1; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; REGULATORY SEQUENCES, NUCLEIC ACID; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 0032869011     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4439(99)00066-6     Document Type: Review

References (67)

1. Hakomori S.I. Aberrant glycosylation in tumors and tumor-associated carbohydrate antigens. Adv. Cancer Res. 52:1989;257-331.
2. Rademacher T.W., Parekh R.B., Dwek R.A. Glycobiology. Annu. Rev. Biochem. 57:1988;785-838.
3. Yamashita K., Ohkura T., Tachibana Y., Takasuki S., Kobata A. Comparative study of the oligosaccharides released from baby hamster kidney cells and their polyoma transformant by hydrazinolysis. J. Biol. Chem. 259:1984;10834-10840.
4. Collard J.G., Van Beek W.P., Janssen J.W.G., Schijven J.F. Transfection by human oncogenes: concomitant induction of tumorigenicity and tumor-associated membrane alterations. Int. J. Cancer. 35:1985;207-214.
5. Dennis J.W., Laferte S. Oncodevelopmental expression of GlcNAcβ1-6Manα1-6Manβ1-branched asparagine-linked oligosaccharides in murine tissues and human breast carcinomas. Cancer Res. 49:1989;945-950.
6. Dennis J.W., Laferte S., Waghorne C., Breitman M.L., Kerbel R.S. β1-6 branching of Asn-linked oligosaccharides is directly associated with metastasis. Science. 236:1987;582-585.
7. Humphries M.J., Matsumoto K., White S.L., Olden K. Inhibition of experimental metastasis by castanospermine in mice: blockage of two distinct stages of tumor colonization by oligosaccharide processing inhibitors. Cancer Res. 46:1986;5215-5222.
8. Dennis J.W. Effects of swainsonine and polycytidylic acid on murine tumor cell growth and metastasis. Cancer Res. 46:1986;5131-5136.
9. Pierce M., Arango J. Rous sarcoma virus-transformed baby hamster kidney cells express higher levels of asparagine-linked tri- and tetraantennary glycopeptides containing GlcNAc-β(1,6)Man-α(1,6)Man and poly-N-acetyllactosamine sequences than baby hamster kidney cells. J. Biol. Chem. 261:1986;10772-10777.
10. Miyoshi E., Nishikawa A., Ihara Y., Gu J., Sugiyama T., Hayashi N., Fusamoto H., Kamada T., Taniguchi N. N-Acetylglucosaminyltransferase III and V messenger RNA levels in LEC rats during hepatocarcinogenesis. Cancer Res. 53:1993;3899-3902.
11. Yao M., Zhou D.-P., Jiang S.-M., Wang Q.-H., Zhou X.-D., Tang Z.-Y., Gu J.-X. Elevated activity of N-acetylglucosaminyltransferase V in human hepatocellular carcinoma. J. Cancer Res. Clin. Oncol. 124:1988;27-30.
12. Miyoshi E., Nishikawa A., Ihara Y., Saito H., Uozumi N., Hayashi N., Fusamoto H., Kamada T., Taniguchi N. Transforming growth factor β up-regulates expression of the N-acetylglucosaminyltransferase V gene in mouse melanoma cells. J. Biol. Chem. 270:1995;6216-6220.
13. Shoreibah M.G., Perng G.S., Adler B., Weinstein J., Basu R., Cupples R., Wen D., Browne J.K., Buckhaults P., Fregien N., Pierce M. Isolation, characterization and expression of a cDNA encoding N-acetylglucosaminyltransferase V. J. Biol. Chem. 268:1993;15381-15385.
14. Gu J., Nishikawa A., Tsuruoka N., Ohno M., Yamaguchi N., Kangawa K., Taniguchi N. Purification and characterization of UDP-N-acetylglucosamine:α-6-D-mannoside β-1,6-N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113:1993;614-619.
15. Saito H., Gu J., Nishikawa A., Ihara Y., Fujii J., Kohgo Y., Taniguchi N. cDNA cloning and chromosomal mapping of human N-acetylglucosaminyltransferase V. Eur. J. Biochem. 233:1995;18-26.
16. Kang R., Saito H., Ihara Y., Miyoshi E., Koyama N., Sheng Y., Taniguchi N. Transcriptional regulation of the N-acetylglucosaminyltransferase V gene in human bile duct carcinoma cells (HuCC-T1) is mediated by ets-1. J. Biol. Chem. 271:1996;26706-26712.
17. Wasylyk B., Hahn S.L., Giovane A. The Ets family of transcription factors. Eur. J. Biochem. 211:1993;7-18.
18. Ho I.C., Bhat N.K., Gottschalk L.R., Lindsten T., Thompson C.B., Papas T.S., Leiden J.M. Sequence-specific binding of human Ets-1 to the T cell receptor alpha gene enhancer. Science. 250:1990;814-818.
19. Prosser H.M., Wotton D., Gegonne A., Ghysdael J., Wang S., Speck N.A., Owen M.J. A phorbol ester response element within the human T-cell receptor beta-chain enhancer. Proc. Natl. Acad. Sci. USA. 89:1992;9934-9938.
20. Thompson C.B., Wang C.Y., Ho I.C., Bohjanen P.R., Petryniak B., June C.H., Miesfeldt S., Zhang L., Nabel G.J., Karpinski B., Leiden J.M. Mol. Cell. Biol. 12:1992;1043-1053.
21. Wu H., Monlton K., Horvai A., Parik S., Glass C.K. Chinese hamster ovary cell mutants defective in the internalization of ricin. Mol. Cell. Biol. 14:1994;2129-2139.
22. Wasylyk C., Gutman A., Nicholson R., Wasylyk K. The c-Ets oncoprotein activates the stromelysin promoter through the same elements as several non-nuclear oncoproteins. EMBO J. 10:1991;1127-1134.
23. Nakajima K., Kusafuka T., Takeda T., Fujitani Y., Nakae K., Hirano T. Identification of a novel interleukin-6 response element containing an Ets-binding site and a CRE-like site in the junB promoter. Mol. Cell. Biol. 13:1993;3027-3041.
24. Wasylyk C., Flores P., Gutman A., Wasylyk B. PEA3 is a nuclear target for transcription activation by non-nuclear oncogenes. EMBO J. 8:1989;3371-3378.
25. Salmon P., Giovane A., Wasylyk B., Klatzmann D. Characterization of the human CD4 gene promoter: transcription from the CD4 gene core promoter is tissue-specific and is activated by Ets proteins. Proc. Natl. Acad. Sci. USA. 90:1993;7739-7743.
26. Seth A., Robinson L., Panayiotaskis A., Thompson D.M., Hodge D.R., Zhang X.K., Watson D.K., Ozato K., Papas T.S. The EndoA enhancer contains multiple ETS binding site repeats and is regulated by ETS proteins. Oncogene. 9:1994;469-477.
27. Klaes A., Menne T., Stollewerk A., Scholz H., Klambt C. The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell. 78:1994;149-160.
28. Sumarsono S.H., Wilson T.J., Tymms M.J., Venter D.J., Corrick C.M., Kola R., Lahoud M.H., Papas T.S., Seth A., Kola I. Down's syndrome-like skeletal abnormalities in Ets2 transgenic mice. Nature. 379:1996;534-537.
29. Vandenbunder B., Queva C., Desbiens X., Wernert N., Stehelin D. Expression of the transcription factor c-Ets1 correlates with the occurrence of invasive processes during normal and pathological development. Invasion Metastasis. 14:1994;198-209.
30. N. Wernert, M.B. Raes, P. Lassalle, M.P. Dehouclr, B. Gosselin, B. Vandenbunder, D. Stehelin, c-ets1 proto-oncogene is a transcription factor expressed in endothelial cells during tumor vascularization and other forms of angiogenesis in humans, Am. J. Pathol. 140 (1992).
31. Liabakk N.B., Talbot I., Smith R.A., Wilkinson K., Balkwill F. Matrix metalloprotease 2 (MMP-2) and matrix metalloprotease 9 (MMP-9) type IV collagenases in colorectal cancer. Cancer Res. 56:1996;190-196.
32. Higashino F., Yoshida K., Noumi T., Seiki M., Fujinaga K. Ets-related protein E1A-F can activate three different matrix metalloproteinase gene promoters. Oncogene. 10:1996;1461-1463.
33. Suzuki H., Romano-Spica V., Papas T.S., Bhat N.K. ETS1 suppresses tumorigenicity of human colon cancer cells. Proc. Natl. Acad. Sci. USA. 92:1995;4442-4446.
34. Demetriou M., Nabi I.R., Coppolino M., Dedhar S., Dennis J.W. Reduced contact-inhibition and substratum adhesion in epithelial cells expressing GlcNAc-transferase V. J. Cell Biol. 130:1995;383-392.
35. Thompson C.B., Wang C.Y., Ho I.C., Bohjanen P.R., Petryniak B., June C.H., Miesfeldt S., Zhang L., Nabel G.J., Karpinski B., et al. cis-Acting sequences required for inducible interleukin-2 enhancer function bind a novel Ets-related protein, Elf-1. Mol. Cell. Biol. 12:1992;1043-1053.
36. Auble D.T., Brinckerhoff C.E. The AP-1 sequence is necessary but not sufficient for phorbol induction of collagenase in fibroblasts. Biochemistry. 30:1991;4629-4635.
37. Kramer B., Wiegmann K., Kronke M. Regulation of the human TNF promoter by the transcription factor ets. J. Biol. Chem. 270:1995;6577-6583.
38. Wang Q., Zhou D., Shao D., Shen Z., Gu J. Effects of epidermal growth factor and insulin on the activity of N-acetylglucosaminyltransferase V. Biochem. J. 324:1997;543-545.
39. Buckhaults P., Chen L., Fregien N., Pierce M. Transcriptional regulation of N-acetylglucosaminyltransferase V by the src oncogene. J. Biol. Chem. 272:1997;19575-19581.
40. Chen L., Zhang W., Fregien N., Pierce M. The her-2/neu oncogene stimulates the transcription of N-acetylglucosaminyltransferase V and expression of its cell surface oligosaccharide products. Oncogene. 17:1998;2087-2093.
41. J.W. Dennis et al., personal communication.
42. Narasimhan S. Control of glycoprotein synthesis. J. Biol. Chem. 257:1982;10235-10242.
43. Schachter H. Biosynthetic controls that determine the branching and microheterogeneity of protein-bound oligosaccharides. Biochem. Cell Biol. 64:1986;163-181.
44. Gu J., Nishikawa A., Tsuruoka N., Ohno M., Yamaguchi N., Kangawa K., Taniguchi N. Purification and characterization of UDP-N-acetylglucosamine: alpha-6-D-mannoside beta 1-6N-acetylglucosaminyltransferase (N-acetylglucosaminyltransferase V) from a human lung cancer cell line. J. Biochem. 113:1993;614-619.
45. Brisson J.R., Carver J.P. Solution conformation of asparagine-linked oligosaccharides: α(1-6)-linked moiety. Biochemistry. 22:1983;3680-3686.
46. Nishikawa A., Fujii S., Sugiyama T., Hayashi N., Taniguchi N. High expression of an N-acetylglucosaminyltransferase III in 3′-methyl DAB-induced hepatoma and ascites hepatoma. Biochem. Biophys. Res. Commun. 152:1988;107-112.
47. Taniguchi N., Yokosawa N., Iizuka S., Tsukada Y., Sako F., Miyazawa N. Gann Monogr. Cancer Res. 29:1983;263-272.
48. Taniguchi N., Ikeda Y. γ-Glutamyl transpeptidase: catalytic mechanism and gene expression. Adv. Enzymol. 72:1998;239-278.
49. Yamashita K., Hitoi A., Taniguchi N., Yokosawa N., Tsukada Y., Kobata A. Comparative study of the sugar chains of gamma-glutamyltranspeptidases purified from rat liver and rat AH-66 hepatoma cells. Cancer Res. 43:1983;5059-5063.
50. Nishikawa A., Ihara Y., Hatakeyama M., Kangawa K., Taniguchi N. Purification, cDNA cloning, and expression of UDP-N-acetylglucosamine: β-D-mannoside β-1,4N-acetylglucosaminyltransferase III from rat kidney. J. Biol. Chem. 267:1992;18199-18204.
51. Yoshimura M., Nishikawa A., Ihara Y., Nishiura T., Nakao H., Kanayama Y., Matsuzawa Y., Taniguchi N. High expression of UDP-N-acetylglucosamine: β-D-mannoside β-1,4-N-acetylglucosaminyltransferase III (GnT-III) in chronic myelogenous leukemia in blast crisis. Int. J. Cancer. 60:1995;443-449.
52. Yoshimura M., Nishikawa A., Ihara Y., Taniguchi S., Taniguchi N. Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc. Natl. Acad. Sci. USA. 92:1995;8754-8758.
53. Taniguchi N., Yoshimura M., Miyoshi E., Ihara Y., Nishikawa A., Fujii S. Remodeling of cell surface glycoproteins by N-acetylglucosaminyltransferase III gene transfection: modulation of metastatic potentials and down regulation of hepatitis B virus replication. Glycobiology. 6:1996;691-694.
54. Yoshimura M., Ihara Y., Matsuzawa Y., Taniguchi N. Aberrant glycosylation of E-cadherin enhances cell-cell binding to suppress metastasis. J. Biol. Chem. 271:1996;13811-13815.
55. Ihara Y., Sakamoto Y., Mihara M., Shimizu K., Taniguchi N. Overexpression of N-acetylglucosaminyltransferase III disrupts the tyrosine phosphorylation of Trk with resultant signaling dysfunction in PC12 cells treated with nerve growth factor. J. Biol. Chem. 272:1997;9629-9634.
56. Rebbaa A., Yamamoto H., Moskal J.R., Bremer E.G. 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. 67:1997;2265-2272.
57. Rebbaa A., Yamamoto H., Saito T., Meuillet E., Kim P., Kersey D.S., Bremer E.G., Taniguchi N., Moskal J.R. 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. 272:1997;9275-9279.
58. Miyoshi E., Ihara Y., Nishikawa A., Saito H., Uozumi N., Hayashi N., Fusamoto H., Kamada T., Taniguchi N. Gene expression of N-acetylglucosaminyltransferases III and V: a possible implication for liver regeneration. Hepatology. 22:1995;1847-1855.
59. Ihara Y., Yoshimura M., Miysohi E., Nishikawa A., Sulutan A.S., Toyosawa S., Ohnishi A., Suzuki M., Yamamura K., Ijuhin N., Taniguchi N. Ectopic expression of N-acetylglucosaminyltransferase III in transgenic hepatocytes disrupts apolipoprotein B secretion and induces aberrant cellular morphology with lipid storage. Proc. Natl. Acad. Sci. USA. 95:1998;2526-2530.
60. Priatel J.J., Sarkar M., Schachter H., Marth J.D. Isolation, characterization and inactivation of the mouse Mgat3 gene: the bisecting N-acetylglucosamine in asparagine-linked oligosaccharides appears dispensable for viability and reproduction. Glycobiology. 7:1997;45-56.
61. Bhaumik M., Harris T., Sundaram S., Johnson L., Guttenplan J., Rogler C., Stanley P. Progression of hepatic neoplasms is severely retarded in mice lacking the bisecting N-acetylglucosamine on N-glycans: evidence for a glycoprotein factor that facilitates hepatic tumor progression. Cancer Res. 58:1998;2881-2897.
62. Sultan A.S., Miyoshi E., Ihara Y., Nishikawa A., Tsukada Y., Taniguchi N. Bisecting GlcNAc structures act as negative sorting signals for cell surface glycoproteins in forskolin-treated rat hepatoma cells. J. Biol. Chem. 272:1997;2866-2872.
63. Yoshimura M., Ihara Y., Ohnishi A., Ijuhin N., Nishiura T., Kanakura Y., Matuzawa Y., Taniguchi N. Bisecting N-acetylglucosamine on K562 cells suppresses natural killer cytotoxicity and promotes spleen colonization. Cancer Res. 56:1996;412-418.
64. Miyoshi E., Ihara Y., Hayashi N., Fusamoto H., Kamada T., Taniguchi N. Transfection of N-acetylglucosaminyltransferase III gene suppresses expression of hepatitis B virus in a human hepatoma cell line, HB611. J. Biol. Chem. 270:1995;28311-28315.
65. Sheng Y., Yoshimura M., Inoue S., Oritani K., Nishiura T., Yoshida H., Ogawa M., Okajima Y., Matsuzawa Y., Taniguchi N. Remodeling of glycoconjugates on CD44 enhances cell adhesion to hyaluronate, tumor growth and metastasis in B16 melanoma cells expressing β1,4-N-acetylglucosaminyltransferase III. Int. J. Cancer. 73:1997;850-858.
66. Taniguchi N., Ihara Y. Recent progress in the molecular biology of the cloned N-acetylglucosaminyltransferases. Glycoconjugate J. 12:1995;733-738.
67. J.H. Ko, E. Miyoshi, K. Noda, A. Ekuni, R. Kang, Y. Ikeda, N. Taniguchi, Regulation of the GnT-V promotor by transcription factor ets-1 in various cancer cell lines, J. Biol. Chem. (1999) in press.