O-linked N-acetylglucosaminyltransferase inhibition prevents G2/M transition in Xenopus laevis oocytes

被引:59
作者
Dehennaut, Vanessa
Lefebvre, Tony
Sellier, Chantal
Leroy, Yves
Gross, Benjamin
Walker, Suzanne
Cacan, Rene
Michalski, Jean-Claude
Vilain, Jean-Pierre
Bodart, Jean-Francois [1 ]
机构
[1] Univ Sci & Technol Lille, EA 4020, Lab Regulat Signaux Div, SN3,IFR147, F-59655 Villeneuve Dascq, France
[2] CNRS, Unite Glycobiol Struct & Fonct, UMR 8576, IFR147, F-59655 Villeneuve Dascq, France
[3] Harvard Univ, Sch Med, Dept Microbiol & Mol Genet, Boston, MA 02115 USA
关键词
D O I
10.1074/jbc.M700444200
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Full-grown Xenopus oocytes are arrested at the prophase of the first meiotic division in a G(2)-like state. Progesterone triggers meiotic resumption also called the G(2)/M transition. This event is characterized by germinal vesicle breakdown ( GVBD) and by a burst in phosphorylation level that reflects activation of M-phase-promoting factor ( MPF) and MAPK pathways. Besides phosphorylation and ubiquitin pathways, increasing evidence has suggested that the cytosolic and nucleus-specific O-GlcNAc glycosylation also contributes to cell cycle regulation. To investigate the relationship between O-GlcNAc and cell cycle, Xenopus oocyte, in which most of the M-phase regulators have been discovered, was used. Alloxan, an O-GlcNAc transferase inhibitor, blocked G(2)/M transition in a concentration-dependent manner. Alloxan prevented GVBD and both MPF and MAPK activations, either triggered by progesterone or by egg cytoplasm injection. The addition of detoxifying enzymes ( SOD and catalase) did not rescue GVBD, indicating that the alloxan effect did not occur through reactive oxygen species production. These results were strengthened by the use of a benzoxazolinone derivative ( XI), a new O-GlcNAc transferase inhibitor. Conversely, injection of O-(2-acetamido-2-deoxy-D-glucopyranosylidene) amino-N-phenylcarbamate, an O-GlcNAcase inhibitor, accelerated the maturation process. Glutamine: fructose-6-phosphate amidotransferase inhibitors, azaserine and 6-diazo-5-ox-onorleucine, failed to prevent GVBD. Such a strategy appeared to be inefficient; indeed, UDP-GlcNAc assays in mature and immature oocytes revealed a constant pool of the nucleotide sugar. Finally, we observed that cyclin B2, the MPF regulatory subunit, was associated with an unknown O-GlcNAc partner. The present work underlines a crucial role for O-GlcNAc in G(2)/M transition and strongly suggests that its function is required for cell cycle regulation.
引用
收藏
页码:12527 / 12536
页数:10
相关论文
共 47 条
  • [1] Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint
    Abrieu, A
    Magnaghi-Jaulin, L
    Kahana, JA
    Peter, M
    Castro, A
    Vigneron, S
    Lorca, T
    Cleveland, DW
    Labbé, JC
    [J]. CELL, 2001, 106 (01) : 83 - 93
  • [2] Xp42Mpk1 activation is not required for germinal vescicle breakdown but for Raf complete phosphorylation in insulin-stimulated Xenopus oocytes
    Baert, F
    Bodart, JF
    Bocquet-Muchembled, B
    Lescuyer-Rousseau, A
    Vilain, JP
    [J]. JOURNAL OF BIOLOGICAL CHEMISTRY, 2003, 278 (50) : 49714 - 49720
  • [3] Differential roles of p39Mos-Xp42Mpk1 cascade proteins on Raf1 phosphorylation and spindle morphogenesis in Xenopus oocytes
    Bodart, JFL
    Baert, FY
    Sellier, C
    Duesbery, NS
    Flament, S
    Vilain, JP
    [J]. DEVELOPMENTAL BIOLOGY, 2005, 283 (02) : 373 - 383
  • [4] Characterization of MPF and MAPK activities during meiotic maturation of Xenopus tropicalis oocytes
    Bodart, JFL
    Gutierrez, DV
    Nebreda, AR
    Buckner, BD
    Resau, JR
    Duesbery, NS
    [J]. DEVELOPMENTAL BIOLOGY, 2002, 245 (02) : 348 - 361
  • [5] Reactive species-mediated regulation of cell signaling and the cell cycle: The role of MAPK
    Cakir, Y
    Ballinger, SW
    [J]. ANTIOXIDANTS & REDOX SIGNALING, 2005, 7 (5-6) : 726 - 740
  • [6] Glucosamine protects neonatal cardiomyocytes from ischemia-reperfusion injury via increased protein-associated O-GlcNAc
    Champattanachai, Voraratt
    Marchase, Richard B.
    Chatham, John C.
    [J]. AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, 2007, 292 (01): : C178 - C187
  • [7] Comparative effects of insulin on the activation of the Raf/Mos-dependent MAP kinase cascade in vitellogenic versus postvitellogenic Xenopus oocytes
    Chesnel, F
    Bonnec, G
    Tardivel, A
    Boujard, D
    [J]. DEVELOPMENTAL BIOLOGY, 1997, 188 (01) : 122 - 133
  • [8] Xenopus H-RasV12 promotes entry into meiotic M phase and cdc2 activation independently of Mos and p42MAPK
    Dupré, A
    Suziedelis, K
    Valuckaite, R
    de Gunzburg, J
    Ozon, R
    Jessus, C
    Haccard, O
    [J]. ONCOGENE, 2002, 21 (42) : 6425 - 6433
  • [9] GLYCOGEN BREAKDOWN IN CLEAVING XENOPUS EMBRYOS IS LIMITED BY ADP
    DWORKIN, MB
    DWORKINRASTL, E
    [J]. MOLECULAR REPRODUCTION AND DEVELOPMENT, 1992, 32 (04) : 354 - 362
  • [10] METABOLIC-REGULATION DURING EARLY FROG DEVELOPMENT - GLYCOGENIC FLUX IN XENOPUS OOCYTES, EGGS, AND EMBRYOS
    DWORKIN, MB
    DWORKINRASTL, E
    [J]. DEVELOPMENTAL BIOLOGY, 1989, 132 (02) : 512 - 523