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Cbk1 Regulation of the RNA-Binding Protein Ssd1 Integrates Cell Fate with Translational Control

2009; Elsevier BV; Volume: 19; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2009.10.071

1879-0445

Jaclyn M. Jansen, Antony G. Wanless, Christopher Seidel, Eric L. Weiss,

Fungal and yeast genetics research

Spatial control of gene expression, at the level of both transcription and translation, is critical for cellular differentiation [1Paquin N. Ménade M. Poirier G. Donato D. Drouet E. Chartrand P. Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p.Mol. Cell. 2007; 26: 795-809Abstract Full Text Full Text PDF PubMed Scopus (91) Google Scholar, 2Ciosk R. DePalma M. Priess J.R. Translational regulators maintain totipotency in the Caenorhabditis elegans germline.Science. 2006; 311: 851-853Crossref PubMed Scopus (127) Google Scholar, 3Chia W. Somers W.G. Wang H. Drosophila neuroblast asymmetric divisions: Cell cycle regulators, asymmetric protein localization, and tumorigenesis.J. Cell Biol. 2008; 180: 267-272Crossref PubMed Scopus (104) Google Scholar, 4White R. Gonsior C. Krämer-Albers E.M. Stöhr N. Hüttelmaier S. Trotter J. Activation of oligodendroglial Fyn kinase enhances translation of mRNAs transported in hnRNP A2-dependent RNA granules.J. Cell Biol. 2008; 181: 579-586Crossref PubMed Scopus (130) Google Scholar]. 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 [5Colman-Lerner A. Chin T.E. Brent R. Yeast Cbk1 and Mob2 activate daughter-specific genetic programs to induce asymmetric cell fates.Cell. 2001; 107: 739-750Abstract Full Text Full Text PDF PubMed Scopus (258) Google Scholar, 6Weiss E.L. Kurischko C. Zhang C. Shokat K. Drubin D.G. Luca F.C. 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; 158: 885-900Crossref PubMed Scopus (158) Google Scholar, 7Bidlingmaier S. Weiss E.L. Seidel C. Drubin D.G. Snyder M. The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae.Mol. Cell. Biol. 2001; 21: 2449-2462Crossref PubMed Scopus (145) Google Scholar, 8Racki W.J. Bécam A.M. Nasr F. Herbert C.J. Cbk1p, a protein similar to the human myotonic dystrophy kinase, is essential for normal morphogenesis in Saccharomyces cerevisiae.EMBO J. 2000; 19: 4524-4532Crossref PubMed Scopus (114) Google Scholar]. Cbk1 is essential in cells expressing functional Ssd1, an RNA-binding protein of unknown function [9Jorgensen P. Nelson B. Robinson M.D. Chen Y. Andrews B. Tyers M. Boone C. High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants.Genetics. 2002; 162: 1091-1099Crossref PubMed Google Scholar, 10Hogan D.J. Riordan D.P. Gerber A.P. Herschlag D. Brown P.O. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system.PLoS Biol. 2008; 6: e255Crossref PubMed Scopus (423) Google Scholar, 11Uesono Y. Toh-e A. Kikuchi Y. Ssd1p of Saccharomyces cerevisiae associates with RNA.J. Biol. Chem. 1997; 272: 16103-16109Crossref PubMed Scopus (83) Google Scholar]. 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.