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Mutations in Drosophila Greatwall/Scant Reveal Its Roles in Mitosis and Meiosis and Interdependence with Polo Kinase

Archambault, Vincent and Zhao, Xinbei and White-Cooper, Helen and Carpenter, Adelaide T. C. and Glover, David M. (2007) Mutations in Drosophila Greatwall/Scant Reveal Its Roles in Mitosis and Meiosis and Interdependence with Polo Kinase. PLOS Genetics, 3 (11). Art. No. e200. ISSN 1553-7404. PMCID PMC2065886. https://resolver.caltech.edu/CaltechAUTHORS:20200807-170351991

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[img] MS PowerPoint (Figure S1. Second Round Generation of Scant Revertant Alleles) - Supplemental Material
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[img] MS PowerPoint (Figure S2. Centrosome Disassociation Is Occasionally Observed in Embryos Derived from Females Heterozygous for polo or Scant Singly) - Supplemental Material
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[img] MS PowerPoint (Figure S3. The Centrosome Disassociation of polo-Scant-Derived Embryos Is Still Observed in the Absence of Mnk/Chk2) - Supplemental Material
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[img] MS PowerPoint (Figure S4. Gwl Depletion by RNAi in S2 Cells and Associated Phenotypes) - Supplemental Material
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[img] MS PowerPoint (Figure S5. Examples of Somatic Defects Observed in gwl Mutant Flies) - Supplemental Material
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[img] PDF (Figure S6. Quantitation of Defects Observed in gwl Mutant Neuroblasts of Additional Genotypes (to Be Compared with the Data in Figure 6)) - Supplemental Material
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[img] MS PowerPoint (Figure S7. The Localization of Gwl Is Cell Cycle-Regulated in Embryos) - Supplemental Material
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[img] MS Word (Table S1. Progeny from Females with Normal X Chromosomes and the Indicated Third-Chromosome Genotype Crossed to Y^SX.Y^L, v f B/0; C(4)RM, ci ey^R/0 Males) - Supplemental Material
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[img] MS Word (Table S2. Progeny from FM7/+ Females with the Indicated Third-Chromosome Genotype Crossed to Y^SX.Y^L, v f B/0; C(4)RM, ci ey^R/0 Males. Females tested are sibs of those in Table S1. FM7/0 males are nearly always lethal) - Supplemental Material
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[img] MS Word (Table S3. Progeny from Females with Normal X Chromosomes and the Indicated Third-Chromosome Genotype Crossed to Y^SX.Y^L, v f B/0; C(4)RM, ci ey^R/0 Males.Parental crosses were FM7/+; sr Scant females x + Scantf / TM6Bf, mtrm13 Scant/TM6B13, or mtrm126...) - Supplemental Material
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[img] MS Word (Table S4. Progeny from FM7/+ Females with the Indicated Third-Chromosome Genotype Crossed to Y^SX.Y^L, v f B/0; C(4)RM, ci ey^R/0 Males.Females tested are sibs of those in Table S3.) - Supplemental Material
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[img] MS Word (Text S2. Supporting Results) - Supplemental Material
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[img] Video (AVI) (Video S1. Wild-Type (Oregon R) Syncytial Embryos (GFP-β-Tubulin): Control for Video S2) - Supplemental Material
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[img] Video (AVI) (Video S2. polo¹¹ Scant/+ + -Derived Syncytial Embryos (GFP-β-Tubulin)) - Supplemental Material
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Abstract

Polo is a conserved kinase that coordinates many events of mitosis and meiosis, but how it is regulated remains unclear. Drosophila females having only one wild-type allele of the polo kinase gene and the dominant Scant mutation produce embryos in which one of the centrosomes detaches from the nuclear envelope in late prophase. We show that Scant creates a hyperactive form of Greatwall (Gwl) with altered specificity in vitro, another protein kinase recently implicated in mitotic entry in Drosophila and Xenopus. Excess Gwl activity in embryos causes developmental failure that can be rescued by increasing maternal Polo dosage, indicating that coordination between the two mitotic kinases is crucial for mitotic progression. Revertant alleles of Scant that restore fertility to polo–Scant heterozygous females are recessive alleles or deficiencies of gwl; they show chromatin condensation defects and anaphase bridges in larval neuroblasts. One recessive mutant allele specifically disrupts a Gwl isoform strongly expressed during vitellogenesis. Females hemizygous for this allele are sterile, and their oocytes fail to arrest in metaphase I of meiosis; both homologues and sister chromatids separate on elongated meiotic spindles with little or no segregation. This allelic series of gwl mutants highlights the multiple roles of Gwl in both mitotic and meiotic progression. Our results indicate that Gwl activity antagonizes Polo and thus identify an important regulatory interaction of the cell cycle.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pgen.0030200DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2065886/PubMed CentralArticle
ORCID:
AuthorORCID
Archambault, Vincent0000-0002-2857-7667
White-Cooper, Helen0000-0002-3373-8023
Glover, David M.0000-0003-0956-0103
Additional Information:© 2007 Archambault et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: June 27, 2007; Accepted: September 28, 2007; Published: November 9, 2007. A was supported by Long-Term Fellowships from the European Molecular Biology Organization and from the International Human Frontier Science Program Organization. XZ was supported by a Raymond and Helen Kwok Research Scholarship. ATCC and DMG are grateful to the MRC for supporting this work. We are thankful to Margit Pal for performing the injections to generate the transgenic flies and to W.E. Theurkauf for providing the chk2 mutant flies. We also thank Youbin Xiang and Scott Hawley for the oocyte immunostaining protocol, for communicating results on mtrm and stocks prior to publication, and for stimulating discussions. We are very grateful to Yutaka Yamamoto for his early time-lapse imaging studies. We thank members of the Glover lab for helpful interactions. Author Contributions. VA, XZ, and ATCC conceived and designed the experiments, performed the experiments, and analyzed the data. VA, XZ, HWC, and ATCC contributed reagents/materials/analysis tools. VA, XZ, ATCC, and DMG wrote the paper. HWC made key preliminary observations. DMG and ATCC supervised the work. The authors have declared that no competing interests exist.
Funders:
Funding AgencyGrant Number
European Molecular Biology Organization (EMBO)UNSPECIFIED
Human Frontier Science ProgramUNSPECIFIED
Raymond and Helen Kwok Research ScholarshipUNSPECIFIED
Medical Research Council (UK)UNSPECIFIED
Issue or Number:11
PubMed Central ID:PMC2065886
Record Number:CaltechAUTHORS:20200807-170351991
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200807-170351991
Official Citation:Archambault V, Zhao X, White-Cooper H, Carpenter ATC, Glover DM (2007) Mutations in Drosophila Greatwall/Scant Reveal Its Roles in Mitosis and Meiosis and Interdependence with Polo Kinase. PLoS Genet 3(11): e200. https://doi.org/10.1371/journal.pgen.0030200
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:104852
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:12 Aug 2020 22:01
Last Modified:12 Aug 2020 22:01

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