The tumor suppressor HIC1 (hypermethylated in cancer 1) is O-GlcNAc glycosylated

European Journal of Biochemistry

Volumn 271, Issue 19, 2004, Pages 3843-3854

  Lefebvre, Tony ^a,b   Pinte, Sébastien ^a   Guérardel, Cateline ^a   Deltour, Sophie ^a,c   Martin Soudant, Nathalie ^a   Slomianny, Marie Christine ^b   Michalski, Jean Claude ^b   Leprince, Dominique ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BTB POZ; DNA binding; HIC1; O GlcNAc; Transcriptional repression

Indexed keywords

N ACETYLGLUCOSAMINE; PROTEIN HIC1; REPRESSOR PROTEIN; UNCLASSIFIED DRUG; WHEAT GERM AGGLUTININ; ZINC FINGER PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BTB POZ DOMAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DELETION MUTANT; DIMERIZATION; GEL MOBILITY SHIFT ASSAY; GLYCOSYLATION; HYPERMETHYLATED IN CANCER 1 GENE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MODIFICATION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

ACETYLGLUCOSAMINE; ANIMALS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; CHO CELLS; CHROMATOGRAPHY, AFFINITY; COS CELLS; CRICETINAE; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENES, TUMOR SUPPRESSOR; GLYCOCONJUGATES; GLYCOSYLATION; NEOPLASMS; PEPTIDE FRAGMENTS; PROTEIN CONFORMATION; TRANSCRIPTION FACTORS; TRYPSIN; WHEAT GERM AGGLUTININS;

ANIMALIA; EUKARYOTA; TRITICUM AESTIVUM;

EID: 4944257244     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04316.x     Document Type: Article

References (42)

1. Wells, L., Whelan, S.A. & Hart, G.W. (2003) O-GlcNAc: a regulatory post-translational modification. Biochem. Biophys. Res. Commun. 302, 435-441.
2. Omary, M.B., Ku, N.O., Liao, J. & Price, D. (1998) Keratin modifications and solubility properties in epithelial cells and in vitro. Subcell. Biochem. 31, 105-140.
3. Dong, D.L., Xu, Z.S., Hart, G.W. & Cleveland, D.W. (1996) Cytoplasmic O-GlcNAc modification of the head domain and the KSP repeat motif of the neurofilament protein neurofilament-H. J. Biol. Chem. 271, 20845-20852.
4. Cole, R.N. & Hart, G.W. (1999) Glycosylation sites flank phosphorylation sites on synapsin I: O-linked N-acetylglucosamine residues are localized within domains mediating synapsin I interactions. J. Neurochem. 73, 418-428.
5. Lefebvre, T., Ferreira, S., Dupont-Wallois, L., Bussiere, T., Dupire, M.-J., Delacourte, A., Michalski, J.-C. & Caillet-Boudin, M.-L. (2003) Evidence of a balance between phosphorylation and O-GlcNAc glycosylation of Tau proteins: a role in nuclear localization. Biochim. Biophys. Acta 1619, 167-176.
6. Comer, F.I. & Hart, G.W. (2001) Reciprocity between O-GlcNAc and O-phosphate on the carboxyl terminal domain of RNA polymerase II. Biochemistry 40, 7845-7852.
7. Juang, Y.T., Solomou, E.E., Rellahan, B. & Tsokos, G.C. (2002) Phosphorylation and O-linked glycosylation of Elf-1 leads to its translocation to the nucleus and binding to the promoter of the TCR zeta-chain. J. Immunol. 168, 2865-2871.
8. Kamemura, K., Hayes, B.K., Comer, F.I. & Hart, G.W. (2002) Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens. J. Biol. Chem. 277, 19229-19235.
9. Lefebvre, T., Planque, N., Leleu, D., Bailly, M., Caillet-Boudin, M.-L., Saule, S. & Michalski, J.-C. (2002) O-Glycosylation of the nuclear forms of Pax-6 products in quail neuroretina cells. J. Cell. Biochem. 85, 208-218.
10. Lamarre-Vincent, N. & Hsieh-Wilson, L.C. (2003) Dynamic glycosylation of the transcription factor CREB: a potential role in gene regulation. J. Am. Chem. Soc. 125, 6612-6613.
11. Yang, X., Zhang, F. & Kudlow, J.E. (2002) Recruitment of O-GIcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell 110, 69-80.
12. Kreppel, L.K., Blomberg, M.A. & Hart, G.W. (1997) Dynamic glycosylation of nuclear and cytosolic proteins: cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 272, 9308-9315.
13. Gao, Y., Wells, L., Comer, F.I., Parker, G.J. & Hart, G.W. (2001) Dynamic O-glycosylation of nuclear and cytosolic proteins: cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276, 9838-9845.
14. Iyer, S.P. & Hart, G.W. (2003) Dynamic nuclear and cytoplasmic glycosylation: enzymes of O-GlcNAc cycling, Biochemistry 42, 2493-2499.
15. O'Donnell, N. (2002) Intracellular glycosylation and development. Biochim. Biophys. Acta 1573, 336-345.
16. Han, I. & Kudlow, J.E. (1997) Reduced O-glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17, 2550-2558.
17. Cheng, X. & Hart, G.W. (2001) Alternate O-glycosylation/O- phosphorylation of serine 16 in the murine estrogen receptor-Beta. J. Biol. Chem. 276, 10570-10575.
18. Roos, M.D., Su, K., Baker, J.R. & Kudlow, J.E. (1997) O-Glycosylation of an Sp1-derived peptide blocks known Sp1 protein interactions. Mol. Cell Biol. 17, 6472-6480.
19. Shaw, P., Freeman, J., Bovey, R. & Iggo, R. (1996) Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus. Oncogene 12, 921-930.
20. Weigert, C., Klopfer, K., Kausch, C., Brodbeck, K., Stumvoll, M., Haring, H.U. & Schleicher, E.D. (2003) Palmitate-induced activation of the hexosamine pathway in human myotubes: increased expression of glutamine: fructose-6-phosphate aminotransferase. Diabetes 52, 650-656.
21. Wales, M.M., Biel, M.A., el Deiry, W., Nelkin, B.D., Issa, J.P., Cavenee, W.K., Kuerbitz, S.J. & Baylin, S.B. (1995) p53 activates expression of HIC1, a new candidate tumour suppressor gene on 17p13.3. Nat. Med. 1, 570-577.
22. Baylin, S.B. & Herman, J.G. (2001) Promoter hypermethylation: can this change alone ever designate true tumor suppressor gene function? J. Natl Cancer Inst. 93, 664-665.
23. Herman, J.G. & Baylin, S.B. (2003) Gene silencing in cancer in association with promoter hypermethylation. N. Engl. J. Med. 349, 2042-2054.
24. Guérardel, C., Deltour, S., Pinte, S., Monte, D., Begue, A., Godwin, A.K. & Leprince, D. (2001) Identification in the human candidate tumor suppressor gene HIC1 of a new major alternative TATA-less promoter positively regulated by p53. J. Biol. Chem. 276, 3078-3089.
25. Carter, M.G., Johns, M.A., Zeng, X., Zhou, L., Zink, M.C., Mankowski, J.L., Donovan, D.M. & Baylin, S.B. (2000) Mice deficient in the candidate tumor suppressor gene Hic1 exhibit developmental defects of structures affected in the Miller-Dieker syndrome. Hum. Mol. Genet. 9, 413-419.
26. Chen, W.Y., Zeng, X., Carter, M.G., Morrell, C.N., Chiu Yen, R.W., Esteller, M., Watkins, D.N., Herman, J.G., Mankowski, J.L. & Baylin, S.B. (2003) Heterozygous disruption of Hic1 predisposes mice to a gender-dependent spectrum of malignant tumors. Nat. Genet. 33, 197-202.
27. Deltour, S., Guerardel, C. & Leprince, D. (1999) Recruitment of SMRT/N-CoR-mSin3A-HDAC-repressing complexes is not a general mechanism for BTB/POZ transcriptional repressors: the case of HIC-1 and γFBP-B. Proc. Natl Acad. Sci. USA 96, 14831-14836.
28. Deltour, S., Pinte, S., Guerardel, C., Wasylyk, B. & Leprince, D. (2002) The human candidate tumor suppressor gene HIC1 recruits CtBP through a degenerate GLDLSKK motif. Mol. Cell. Biol. 22, 4890-4901.
29. Pinte, S., Stankovic-Valentin, N., Deltour, S., Rood, B.R. & Guerardel and Leprince, D. (2004) The tumor suppressor gene HIC1 (hypermethylated in cancer 1) is a sequence-specific transcriptional rerpressor: definition of its consensus binding sequence and analysis of its DNA-binding and repressive properties. J. Biol. Chem. in press.
30. Bertrand, S., Pinte, S., Stankovic-Valentin, N., Deltour-Balerdi, Guérardel, C., Begue, A., Laudet, V. & Leprince, D. (2004) Identification and developmental expression of the zebrafish orthologue of the tumor suppressor gene HIC1. Bioch. Biophys. Acta 1678, 57-66.
31. Han, I., Oh, E.S. & Kudlow, J.E. (2000) Responsiveness of the state of O-linked N-acetylglucosamine modification of nuclear pore protein p62 to the extracellular glucose concentration. Biochem. J. 350, 109-114.
32. Gao, Y., Miyazaki, J. & Hart, G.W. (2003) The transcription factor PDX-1 is post-translationally modified by O-linked N-acetylglucosamine and this modification is correlated with its DNA binding activity and insulin secretion in min6 beta-cells. Arch. Biochem. Biophys. 415, 155-163.
33. Starr, C.M. & Hanover, J.A. (1990) Glycosylation of nuclear pore protein p62: reticulocyte lysate catalyzes O-linked N-acetylglucosamine addition in vitro. J. Biol. Chem. 265, 6868-6873.
34. Torres, C.R. & Hart, G.W. (1984) Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes: evidence for O-linked GlcNAc. J. Biol. Chem. 259, 3308-3317.
35. Hanover, J.A., Cohen, C.K., Willingham, M.C. & Park, M.K. (1987) O-Linked N-acetylglucosamine is attached to proteins of the nuclear pore: evidence for cytoplasmic and nucleoplasmic glycoproteins. J. Biol. Chem. 262, 9887-9894.
36. Wells, L., Vosseller, K. & Hart, G.W. (2003) A role for N-acetylglucosamine as a nutrient sensor and mediator of insulin resistance. Cell. Mol. Life Sci. 60, 222-228.
37. Li, J.-Y., English, M.A., Ball, H.J., Yeyati, P.L., Waxman, S. & Licht, J.L. (1997) Sequence-specific DNA binding and transcriptional regulation by the promyelocytic leukemia zinc finger protein. J. Biol. Chem. 272, 22447-22455.
38. Ivins, S., Pemberton, K., Guidez, F., Howell, L., Krumlauf, R. & Zelent, A. (2003) Regulation of Hoxb2 by APL-associated PLZF protein. Oncogene 22, 3685-3697.
39. Hiromura, M., Choi, C.H., Sabourin, N.A., Jones, H., Bachvarov, D. & Usheva, A. (2003) YY1 is regulated by O-linked N-acetylglucosaminylation (O-GlcNAcylation). J. Biol. Chem. 278, 14046-14052.
40. Yang, X., Su, K., Roos, M.D., Chang, Q., Paterson, A.J. & Kudlow, J.E. (2001) O-Linkage of N-acetylglucosamine to Sp1 activation domain inhibits its transcriptional capability. Proc. Natl Acad. Sci. USA 98, 6611-6616.
41. Gewinner, C., Hart, G., Zachara, N., Cole, R., Beisenherz-Huss, C. & Groner, B. (2004) The coactivator of transcription CREB binding protein interacts preferentially with the glycosylated form of Stat5. J. Biol. Chem. 279, 3563-3572.
42. Lemercier, C., Brocard, M.P., Puvion-Dutilleul, F., Kao, H.Y., Albagli, O. & Khochbin, S. (2002) Class II histone deacetylases are directly recruited by BCL6 transcriptional repressor. J. Biol. Chem. 277, 22045-22052.