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PMID: 19962308 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Cbk1 regulation of the RNA-binding protein Ssd1 integrates cell fate with translational control.

Current biology : CB ·Vol. 19 ·No. 24 ·2009-12-29 ·Pages 2114-20

Jansen JM, Wanless AG, Seidel CW, Weiss EL

Abstract

Spatial control of gene expression, at the level of both transcription and translation, is critical for cellular differentiation [1-4]. In budding yeast, the conserved Ndr/warts kinase Cbk1 localizes to the new daughter cell, where it acts as a cell fate determinant. Cbk1 both induces a daughter-specific transcriptional program and promotes morphogenesis in a less well-defined role [5-8]. Cbk1 is essential in cells expressing functional Ssd1, an RNA-binding protein of unknown function [9-11]. We show here that Cbk1 inhibits Ssd1 in vivo. Loss of this regulation dramatically slows bud expansion, leading to highly aberrant cell wall organization at the site of cell growth. Ssd1 associates with specific mRNAs, a significant number of which encode cell wall remodeling proteins. Translation of these messages is rapidly and specifically suppressed when Cbk1 is inhibited; this suppression requires Ssd1. Transcription of several of these Ssd1-associated mRNAs is also regulated by Cbk1, indicating that the kinase controls both the transcription and translation of daughter-specific mRNAs. This work suggests a novel system by which cells coordinate localized expression of genes involved in processes critical for cell growth and division.

MeSH Terms
Blotting, Northern Cell Differentiation/genetics,physiology Cell Wall/genetics,physiology DNA Primers/genetics Fluorescence Recovery After Photobleaching Gene Components Gene Expression Regulation, Fungal/genetics,physiology Intracellular Signaling Peptides and Proteins/metabolism Microscopy, Electron, Transmission Microscopy, Fluorescence Phosphorylation Protein Serine-Threonine Kinases/metabolism RNA, Messenger/metabolism RNA-Binding Proteins/metabolism Reverse Transcriptase Polymerase Chain Reaction Saccharomyces cerevisiae Proteins/metabolism
Chemicals
DNA Primers Intracellular Signaling Peptides and Proteins RNA, Messenger RNA-Binding Proteins Saccharomyces cerevisiae Proteins Ssd1 protein, S cerevisiae CBK1 protein, S cerevisiae Protein Serine-Threonine Kinases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jansen Jaclyn M
Department of Biochemistry, Molecular Biology, and Cell Biology, Northwestern University, Evanston, IL 60208, USA.
Wanless Antony G
Seidel Christopher W
Weiss Eric L
References (38)
38 references, click to expand
  1. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1.
    Nature. 2005 Nov 24;438(7067):512-5 PMID: 16306994
  2. The yeast LATS/Ndr kinase Cbk1 regulates growth via Golgi-dependent glycosylation and secretion.
    Mol Biol Cell. 2008 Dec;19(12):5559-78 PMID: 18843045
  3. The product of the UTH1 gene, required for Bax-induced cell death in yeast, is involved in the response to rapamycin.
    Mol Microbiol. 2003 Jan;47(2):495-506 PMID: 12519199
  4. Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules.
    J Cell Biol. 2008 May 19;181(4):579-86 PMID: 18490510
  5. The furry gene of Drosophila is important for maintaining the integrity of cellular extensions during morphogenesis.
    Development. 2001 Jul;128(14):2793-802 PMID: 11526084
  6. Ssd1 is required for thermotolerance and Hsp104-mediated protein disaggregation in Saccharomyces cerevisiae.
    Mol Cell Biol. 2009 Jan;29(1):187-200 PMID: 18936161
  7. The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Apr;21(7):2449-62 PMID: 11259593
  8. A role for the Saccharomyces cerevisiae regulation of Ace2 and polarized morphogenesis signaling network in cell integrity.
    Genetics. 2005 Oct;171(2):443-55 PMID: 15972461
  9. Resistance to the plant PR-5 protein osmotin in the model fungus Saccharomyces cerevisiae is mediated by the regulatory effects of SSD1 on cell wall composition.
    Plant J. 2001 Feb;25(3):271-80 PMID: 11208019
  10. A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation.
    Lett Appl Microbiol. 2003;37(3):268-74 PMID: 12904232
  11. The tricornered Ser/Thr protein kinase is regulated by phosphorylation and interacts with furry during Drosophila wing hair development.
    Mol Biol Cell. 2005 Feb;16(2):689-700 PMID: 15591127
  12. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system.
    PLoS Biol. 2008 Oct 28;6(10):e255 PMID: 18959479
  13. Genetic interactions with CLF1 identify additional pre-mRNA splicing factors and a link between activators of yeast vesicular transport and splicing.
    Genetics. 2003 Jul;164(3):895-907 PMID: 12871902
  14. Phosphoregulation of Cbk1 is critical for RAM network control of transcription and morphogenesis.
    J Cell Biol. 2006 Dec 4;175(5):755-66 PMID: 17145962
  15. PhosphoPep--a phosphoproteome resource for systems biology research in Drosophila Kc167 cells.
    Mol Syst Biol. 2007;3:139 PMID: 17940529
  16. The 'SUN' family: yeast SUN4/SCW3 is involved in cell septation.
    Yeast. 2000 Jul;16(10):905-19 PMID: 10870102
  17. The NDR/LATS family kinase Cbk1 directly controls transcriptional asymmetry.
    PLoS Biol. 2008 Aug 19;6(8):e203 PMID: 18715118
  18. Phenotypic activation to discover biological pathways and kinase substrates.
    Cell Cycle. 2006 Jul;5(13):1397-402 PMID: 16855397
  19. Pag1p, a novel protein associated with protein kinase Cbk1p, is required for cell morphogenesis and proliferation in Saccharomyces cerevisiae.
    Mol Biol Cell. 2002 Feb;13(2):503-14 PMID: 11854408
  20. P bodies and the control of mRNA translation and degradation.
    Mol Cell. 2007 Mar 9;25(5):635-46 PMID: 17349952
  21. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling.
    Science. 2009 Apr 10;324(5924):218-23 PMID: 19213877
  22. Daughter-specific transcription factors regulate cell size control in budding yeast.
    PLoS Biol. 2009 Oct;7(10):e1000221 PMID: 19841732
  23. Translational regulators maintain totipotency in the Caenorhabditis elegans germline.
    Science. 2006 Feb 10;311(5762):851-3 PMID: 16469927
  24. Saccharomyces cerevisiae SSD1-V confers longevity by a Sir2p-independent mechanism.
    Genetics. 2004 Apr;166(4):1661-72 PMID: 15126388
  25. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry.
    Nature. 2002 Jan 10;415(6868):180-3 PMID: 11805837
  26. Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates.
    Cell. 2001 Dec 14;107(6):739-50 PMID: 11747810
  27. Comprehensive proteomic analysis of Saccharomyces cerevisiae cell walls: identification of proteins covalently attached via glycosylphosphatidylinositol remnants or mild alkali-sensitive linkages.
    J Biol Chem. 2005 May 27;280(21):20894-901 PMID: 15781460
  28. Analysis of genetic interactions between DHH1, SSD1 and ELM1 indicates their involvement in cellular morphology determination in Saccharomyces cerevisiae.
    Yeast. 1999 Apr;15(6):481-96 PMID: 10234786
  29. Cbk1p, a protein similar to the human myotonic dystrophy kinase, is essential for normal morphogenesis in Saccharomyces cerevisiae.
    EMBO J. 2000 Sep 1;19(17):4524-32 PMID: 10970846
  30. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  31. Control of dendritic branching and tiling by the Tricornered-kinase/Furry signaling pathway in Drosophila sensory neurons.
    Cell. 2004 Oct 15;119(2):245-56 PMID: 15479641
  32. High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants.
    Genetics. 2002 Nov;162(3):1091-9 PMID: 12454058
  33. Mutations in the Saccharomyces cerevisiae type 2A protein phosphatase catalytic subunit reveal roles in cell wall integrity, actin cytoskeleton organization and mitosis.
    Genetics. 1997 Feb;145(2):227-41 PMID: 9071579
  34. The Saccharomyces cerevisiae Mob2p-Cbk1p kinase complex promotes polarized growth and acts with the mitotic exit network to facilitate daughter cell-specific localization of Ace2p transcription factor.
    J Cell Biol. 2002 Sep 2;158(5):885-900 PMID: 12196508
  35. Ssd1p of Saccharomyces cerevisiae associates with RNA.
    J Biol Chem. 1997 Jun 27;272(26):16103-9 PMID: 9195905
  36. Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p.
    Mol Cell. 2007 Jun 22;26(6):795-809 PMID: 17588515
  37. Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis.
    J Cell Biol. 2008 Jan 28;180(2):267-72 PMID: 18209103
  38. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis.
    Mol Biol Cell. 2003 Sep;14(9):3782-803 PMID: 12972564
Article Info
Journal
Current biology : CB
Abbr.
Curr Biol
ISSN
1879-0445
Published
2009-12-29
Epub
2009-00-03
Pages
2114-20
Language
English
Region
England
NLM ID
9107782
PMCID
PMC2805764
Subset
IM
Grants
NIGMS NIH HHS · GM084223 · United States
NIGMS NIH HHS · 5T32GM008061-24 · United States
NIGMS NIH HHS · T32 GM008061 · United States
NIGMS NIH HHS · R01 GM084223-02 · United States
NIGMS NIH HHS · T32 GM008449 · United States
NIGMS NIH HHS · 5T32GM8449-14 · United States
NIGMS NIH HHS · R01 GM084223 · United States
NIGMS NIH HHS · R01 GM084223-01 · United States
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