Greatwall-Endos-PP2A/B55Twins network regulates translation and stability of maternal transcripts in the Drosophila oocyte-to-embryo transition

被引:0
作者
Rangone, Helene [1 ]
Bond, Laura [1 ]
Weil, Timothy T. [2 ]
Glover, David M. [1 ,3 ]
机构
[1] Univ Cambridge, Dept Genet, Downing St, Cambridge, England
[2] Univ Cambridge, Dept Zool, Downing St, Cambridge, England
[3] CALTECH, Div Biol & Biol Engn, 1200 E Calif Blvd, Pasadena, CA 91125 USA
关键词
Greatwall; Endosulfine; Pan Gu kinase; oocyte-to-embryo transition; maternal transcripts; Drosophila; MESSENGER-RNA; PAN-GU; ZYGOTIC TRANSITION; ALPHA-ENDOSULFINE; GREATWALL KINASE; BINDING-PROTEIN; GENETIC SCREEN; TRAILER HITCH; S-PHASE; COMPLEX;
D O I
10.1098/rsob.240065
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
The transition from oocyte to embryo requires translation of maternally provided transcripts that in Drosophila is activated by Pan Gu kinase to release a rapid succession of 13 mitotic cycles. Mitotic entry is promoted by several protein kinases that include Greatwall/Mastl, whose Endosulfine substrates antagonize Protein Phosphatase 2A (PP2A), facilitating mitotic Cyclin-dependent kinase 1/Cyclin B kinase activity. Here we show that hyperactive greatwall(Scant) can not only be suppressed by mutants in its Endos substrate but also by mutants in Pan Gu kinase subunits. Conversely, mutants in me31B or trailer hitch, which encode a complex that represses hundreds of maternal mRNAs, enhance greatwall(Scant). Me31B and Trailer Hitch proteins, known substrates of Pan Gu kinase, copurify with Endos. This echoes findings that budding yeast Dhh1, orthologue of Me31B, associates with Igo1/2, orthologues of Endos and substrates of the Rim15, orthologue of Greatwall. endos-derived mutant embryos show reduced Me31B and elevated transcripts for the mitotic activators Cyclin B, Polo and Twine/Cdc25. Together, our findings demonstrate a previously unappreciated conservation of the Greatwall-Endosulfine pathway in regulating translational repressors and its interactions with the Pan Gu kinase pathway to regulate translation and/or stability of maternal mRNAs upon egg activation.
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页数:15
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  • [1] Greatwall is essential to prevent mitotic collapse after nuclear envelope breakdown in mammals
    Alvarez-Fernandez, Monica
    Sanchez-Martinez, Ruth
    Sanz-Castillo, Belen
    Gan, Pei Pei
    Sanz-Flores, Maria
    Trakala, Marianna
    Ruiz-Torres, Miguel
    Lorca, Thierry
    Castro, Anna
    Malumbres, Marcos
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (43) : 17374 - 17379
  • [2] Mutations in drosophila Greatwall/Scant reveal its roles in mitosis and meiosis and interdependence with polo kinase
    Archambault, Vincent
    Zhao, Xinbei
    White-Cooper, Helen
    Carpenter, Adelaide T. C.
    Glover, David M.
    [J]. PLOS GENETICS, 2007, 3 (11): : 2163 - 2179
  • [3] The GNU subunit of PNG kinase, the developmental regulator of mRNA translation, binds BIC-C to localize to RNP granules
    Aviles-Pagan, Emir E.
    Hara, Masatoshi
    Orr-Weaver, Terry L.
    [J]. ELIFE, 2021, 10
  • [4] Drosophila Larp associates with poly(A)-binding protein and is required for male fertility and syncytial embryo development
    Blagden, Sarah P.
    Gatt, Melanie K.
    Archambault, Vincent
    Lada, Karolina
    Ichihara, Keiko
    Lilley, Kathryn S.
    Inoue, Yoshihiro H.
    Glover, David M.
    [J]. DEVELOPMENTAL BIOLOGY, 2009, 334 (01) : 186 - 197
  • [5] Loss of human Greatwall results in G2 arrest and multiple mitotic defects due to deregulation of the cyclin B-Cdc2/PP2A balance
    Burgess, Andrew
    Vigneron, Suzanne
    Brioudes, Estelle
    Labbe, Jean-Claude
    Lorca, Thierry
    Castro, Anna
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (28) : 12564 - 12569
  • [6] The M Phase Kinase Greatwall (Gwl) Promotes Inactivation of PP2A/B55δ, a Phosphatase Directed Against CDK Phosphosites
    Castilho, Priscila V.
    Williams, Byron C.
    Mochida, Satoru
    Zhao, Yong
    Goldberg, Michael L.
    [J]. MOLECULAR BIOLOGY OF THE CELL, 2009, 20 (22) : 4777 - 4789
  • [7] Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein
    Chen, Linan
    Dumelie, Jason G.
    Li, Xiao
    Cheng, Matthew H. K.
    Yang, Zhiyong
    Laver, John D.
    Siddiqui, Najeeb U.
    Westwood, J. Timothy
    Morris, Quaid
    Lipshitz, Howard D.
    Smibert, Craig A.
    [J]. GENOME BIOLOGY, 2014, 15 (01):
  • [8] The BEG (PP2A-B55/ENSA/Greatwall) Pathway Ensures Cytokinesis follows Chromosome Separation
    Cundell, Michael J.
    Bastos, Ricardo Nunes
    Zhang, Tongli
    Holder, James
    Gruneberg, Ulrike
    Novak, Bela
    Barr, Francis A.
    [J]. MOLECULAR CELL, 2013, 52 (03) : 393 - 405
  • [9] Localized Translation of gurken/TGF-α mRNA during Axis Specification Is Controlled by Access to Orb/CPEB on Processing Bodies
    Davidson, Alexander
    Parton, Richard M.
    Rabouille, Catherine
    Weil, Timothy T.
    Davis, Ilan
    [J]. CELL REPORTS, 2016, 14 (10): : 2451 - 2462
  • [10] RNA tales - how embryos read and discard messages from mom
    Despic, Vladimir
    Neugebauer, Karla M.
    [J]. JOURNAL OF CELL SCIENCE, 2018, 131 (05)