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PMID: 10801981 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny.

Shafi R, Iyer SP, Ellies LG, O'Donnell N, Marek KW, Chui D, Hart GW, Marth JD

Abstract

Nuclear and cytoplasmic protein glycosylation is a widespread and reversible posttranslational modification in eukaryotic cells. Intracellular glycosylation by the addition of N-acetylglucosamine (GlcNAc) to serine and threonine is catalyzed by the O-GlcNAc transferase (OGT). This "O-GlcNAcylation" of intracellular proteins can occur on phosphorylation sites, and has been implicated in controlling gene transcription, neurofilament assembly, and the emergence of diabetes and neurologic disease. To study OGT function in vivo, we have used gene-targeting approaches in male embryonic stem cells. We find that OGT mutagenesis requires a strategy that retains an intact OGT gene as accomplished by using Cre-loxP recombination, because a deletion in the OGT gene results in loss of embryonic stem cell viability. A single copy of the OGT gene is present in the male genome and resides on the X chromosome near the centromere in region D in the mouse spanning markers DxMit41 and DxMit95, and in humans at Xq13, a region associated with neurologic disease. OGT RNA expression in mice is comparably high among most cell types, with lower levels in the pancreas. Segregation of OGT alleles in the mouse germ line with ZP3-Cre recombination in oocytes reveals that intact OGT alleles are required for completion of embryogenesis. These studies illustrate the necessity of conditional gene-targeting approaches in the mutagenesis and study of essential sex-linked genes, and indicate that OGT participation in intracellular glycosylation is essential for embryonic stem cell viability and for mouse ontogeny.

MeSH Terms
Acetylglucosamine/metabolism Animals Cell Survival Chimera Chromosome Mapping Embryonic and Fetal Development/genetics Female Gene Targeting Genes, Lethal Glucosyltransferases/genetics,physiology Glycosylation Humans Hybrid Cells In Situ Hybridization, Fluorescence Male Mice/embryology,genetics Mice, Inbred C57BL Mutagenesis Protein Processing, Post-Translational Recombination, Genetic Stem Cells/cytology X Chromosome/genetics
Chemicals
Glucosyltransferases UDPacetylglucosamine-protein acetylglucosaminyltransferase Acetylglucosamine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Shafi R
The Howard Hughes Medical Institute, Glycobiology Research and Training Center, Department of Cellular and Molecular Medicine, 9500 Gilman Drive-0625, University of California San Diego, La Jolla, CA 92093, USA.
Iyer S P
Ellies L G
O'Donnell N
Marek K W
Chui D
Hart G W
Marth J D
References (37)
37 references, click to expand
  1. O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation.
    Cell. 1988 Oct 7;55(1):125-33 PMID: 3139301
  2. Reduced O-glycosylated clathrin assembly protein AP180: implication for synaptic vesicle recycling dysfunction in Alzheimer's disease.
    Neurosci Lett. 1998 Aug 7;252(1):33-6 PMID: 9756352
  3. Enzymatic addition of O-GlcNAc to nuclear and cytoplasmic proteins. Identification of a uridine diphospho-N-acetylglucosamine:peptide beta-N-acetylglucosaminyltransferase.
    J Biol Chem. 1990 Feb 15;265(5):2563-8 PMID: 2137449
  4. Glycosylation of nuclear pore protein p62. Reticulocyte lysate catalyzes O-linked N-acetylglucosamine addition in vitro.
    J Biol Chem. 1990 Apr 25;265(12):6868-73 PMID: 2182631
  5. Lymphocyte activation induces rapid changes in nuclear and cytoplasmic glycoproteins.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1701-5 PMID: 2000378
  6. Characterization and dynamics of O-linked glycosylation of human cytokeratin 8 and 18.
    J Biol Chem. 1992 Feb 25;267(6):3901-6 PMID: 1371281
  7. Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide beta-N-acetylglucosaminyltransferase.
    J Biol Chem. 1992 May 5;267(13):9005-13 PMID: 1533623
  8. Tissue- and site-specific DNA recombination in transgenic mice.
    Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6861-5 PMID: 1495975
  9. RNA polymerase II is a glycoprotein. Modification of the COOH-terminal domain by O-GlcNAc.
    J Biol Chem. 1993 May 15;268(14):10416-24 PMID: 8486697
  10. Glycosylation of mammalian neurofilaments. Localization of multiple O-linked N-acetylglucosamine moieties on neurofilament polypeptides L and M.
    J Biol Chem. 1993 Aug 5;268(22):16679-87 PMID: 8344946
  11. Purification and characterization of an O-GlcNAc selective N-acetyl-beta-D-glucosaminidase from rat spleen cytosol.
    J Biol Chem. 1994 Jul 29;269(30):19321-30 PMID: 8034696
  12. Clathrin assembly protein AP-3 is phosphorylated and glycosylated on the 50-kDa structural domain.
    J Biol Chem. 1994 Aug 19;269(33):21346-52 PMID: 8063760
  13. Site-specific glycosylation of the human cytomegalovirus tegument basic phosphoprotein (UL32) at serine 921 and serine 952.
    J Virol. 1994 Dec;68(12):8339-49 PMID: 7966627
  14. Glycosylation of the c-Myc transactivation domain.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4417-21 PMID: 7753821
  15. c-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas.
    J Biol Chem. 1995 Aug 11;270(32):18961-5 PMID: 7642555
  16. Beta-amyloid precursor protein is modified with O-linked N-acetylglucosamine.
    J Neurosci Res. 1995 Jun 1;41(2):270-8 PMID: 7650762
  17. Plant nuclear pore complex proteins are modified by novel oligosaccharides with terminal N-acetylglucosamine.
    Plant Cell. 1995 Sep;7(9):1459-71 PMID: 8589629
  18. Glycosylation sites flank phosphorylation sites on synapsin I: O-linked N-acetylglucosamine residues are localized within domains mediating synapsin I interactions.
    J Neurochem. 1999 Jul;73(1):418-28 PMID: 10386995
  19. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells.
    Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8424-8 PMID: 8378314
  20. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes. Evidence for O-linked GlcNAc.
    J Biol Chem. 1984 Mar 10;259(5):3308-17 PMID: 6421821
  21. The subcellular distribution of terminal N-acetylglucosamine moieties. Localization of a novel protein-saccharide linkage, O-linked GlcNAc.
    J Biol Chem. 1986 Jun 15;261(17):8049-57 PMID: 3086323
  22. O-linked N-acetylglucosamine is attached to proteins of the nuclear pore. Evidence for cytoplasmic and nucleoplasmic glycoproteins.
    J Biol Chem. 1987 Jul 15;262(20):9887-94 PMID: 3110163
  23. Regulation of specific DNA binding by p53: evidence for a role for O-glycosylation and charged residues at the carboxy-terminus.
    Oncogene. 1996 Feb 15;12(4):921-30 PMID: 8632915
  24. Recent advances in gene mutagenesis by site-directed recombination.
    J Clin Invest. 1996 May 1;97(9):1999-2002 PMID: 8621787
  25. Dynamic O-GlcNAcylation of the small heat shock protein alpha B-crystallin.
    Biochemistry. 1996 Mar 19;35(11):3578-86 PMID: 8639509
  26. Cytoplasmic O-GlcNAc modification of the head domain and the KSP repeat motif of the neurofilament protein neurofilament-H.
    J Biol Chem. 1996 Aug 23;271(34):20845-52 PMID: 8702840
  27. The microtubule-associated protein tau is extensively modified with O-linked N-acetylglucosamine.
    J Biol Chem. 1996 Nov 15;271(46):28741-4 PMID: 8910513
  28. O-GlcNAcylation of key nuclear and cytoskeletal proteins: reciprocity with O-phosphorylation and putative roles in protein multimerization.
    Glycobiology. 1996 Oct;6(7):711-6 PMID: 8953283
  29. A subpopulation of estrogen receptors are modified by O-linked N-acetylglucosamine.
    J Biol Chem. 1997 Jan 24;272(4):2421-8 PMID: 8999954
  30. Zp3-cre, a transgenic mouse line for the activation or inactivation of loxP-flanked target genes specifically in the female germ line.
    Curr Biol. 1997 Feb 1;7(2):148-51 PMID: 9016703
  31. Isolation, characterization and inactivation of the mouse Mgat3 gene: the bisecting N-acetylglucosamine in asparagine-linked oligosaccharides appears dispensable for viability and reproduction.
    Glycobiology. 1997 Feb;7(1):45-56 PMID: 9061364
  32. Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats.
    J Biol Chem. 1997 Apr 4;272(14):9308-15 PMID: 9083067
  33. O-Linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats.
    J Biol Chem. 1997 Apr 4;272(14):9316-24 PMID: 9083068
  34. Dynamic O-linked glycosylation of nuclear and cytoskeletal proteins.
    Annu Rev Biochem. 1997;66:315-35 PMID: 9242909
  35. Reduction of O-linked N-acetylglucosamine-modified assembly protein-3 in Alzheimer's disease.
    J Neurosci. 1998 Apr 1;18(7):2399-411 PMID: 9502801
  36. Streptozotocin, an analog of N-acetylglucosamine, blocks the removal of O-GlcNAc from intracellular proteins.
    Proc Assoc Am Physicians. 1998 Sep-Oct;110(5):422-32 PMID: 9756093
  37. Nucleotide sequence of the gene encoding zona pellucida glycoprotein ZP3--the mouse sperm receptor.
    Nucleic Acids Res. 1989 Apr 11;17(7):2861-3 PMID: 2541416
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-05-23
Pages
5735-9
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC18502
Subset
IM
Grants
NIDDK NIH HHS · R01 DK048247 · United States
NICHD NIH HHS · R37 HD013563 · United States
NIDDK NIH HHS · DK 48247 · United States
NICHD NIH HHS · HD 13563 · United States
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