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SIN-Dependent Dissociation of the SAD Kinase Cdr2 from the Cell Cortex Resets the Division Plane

2017; Elsevier BV; Volume: 27; Issue: 4 Linguagem: Inglês

10.1016/j.cub.2016.12.050

1879-0445

Sergio A. Rincón, Miguel Estravís, Florent Dingli, Damarys Loew, Phong T. Tran, Anne Paoletti,

Microtubule and mitosis dynamics

Proper division plane positioning is crucial for faithful chromosome segregation but also influences cell size, position, or fate [1Green R.A. Paluch E. Oegema K. Cytokinesis in animal cells.Annu. Rev. Cell Dev. Biol. 2012; 28: 29-58Crossref PubMed Scopus (383) Google Scholar]. In fission yeast, medial division is controlled through negative signaling by the cell tips during interphase and positive signaling by the centrally placed nucleus at mitotic entry [2Rincon S.A. Paoletti A. Molecular control of fission yeast cytokinesis.Semin. Cell Dev. Biol. 2016; 53: 28-38Crossref PubMed Scopus (28) Google Scholar, 3Gu Y. Oliferenko S. Comparative biology of cell division in the fission yeast clade.Curr. Opin. Microbiol. 2015; 28: 18-25Crossref PubMed Scopus (18) Google Scholar, 4Willet A.H. McDonald N.A. Gould K.L. Regulation of contractile ring formation and septation in Schizosaccharomyces pombe.Curr. Opin. Microbiol. 2015; 28: 46-52Crossref PubMed Scopus (35) Google Scholar]: the cell geometry network (CGN), controlled by the inhibitory cortical gradient of the DYRK kinase Pom1 emanating from the cell tips, first promotes the medial localization of cytokinetic ring precursors organized by the SAD kinase Cdr2 to pre-define the division plane [5Almonacid M. Moseley J.B. Janvore J. Mayeux A. Fraisier V. Nurse P. Paoletti A. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export.Curr. Biol. 2009; 19: 961-966Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar, 6Hachet O. Berthelot-Grosjean M. Kokkoris K. Vincenzetti V. Moosbrugger J. Martin S.G. A phosphorylation cycle shapes gradients of the DYRK family kinase Pom1 at the plasma membrane.Cell. 2011; 145: 1116-1128Abstract Full Text Full Text PDF PubMed Scopus (91) Google Scholar, 7Martin S.G. Berthelot-Grosjean M. Polar gradients of the DYRK-family kinase Pom1 couple cell length with the cell cycle.Nature. 2009; 459: 852-856Crossref PubMed Scopus (233) Google Scholar, 8Moseley J.B. Mayeux A. Paoletti A. Nurse P. A spatial gradient coordinates cell size and mitotic entry in fission yeast.Nature. 2009; 459: 857-860Crossref PubMed Scopus (284) Google Scholar]; then, massive nuclear export of the anillin-like protein Mid1 at mitosis entry confirms or readjusts the division plane according to nuclear position and triggers the assembly of a medial contractile ring [5Almonacid M. Moseley J.B. Janvore J. Mayeux A. Fraisier V. Nurse P. Paoletti A. Spatial control of cytokinesis by Cdr2 kinase and Mid1/anillin nuclear export.Curr. Biol. 2009; 19: 961-966Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar, 9Almonacid M. Celton-Morizur S. Jakubowski J.L. Dingli F. Loew D. Mayeux A. Chen J.S. Gould K.L. Clifford D.M. Paoletti A. Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin.Curr. Biol. 2011; 21: 473-479Abstract Full Text Full Text PDF PubMed Scopus (52) Google Scholar, 10Bähler J. Steever A.B. Wheatley S. Wang Yl. Pringle J.R. Gould K.L. McCollum D. Role of polo kinase and Mid1p in determining the site of cell division in fission yeast.J. Cell Biol. 1998; 143: 1603-1616Crossref PubMed Scopus (271) Google Scholar, 11Sohrmann M. Fankhauser C. Brodbeck C. Simanis V. The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast.Genes Dev. 1996; 10: 2707-2719Crossref PubMed Scopus (215) Google Scholar]. Strikingly, the Hippo-like septation initiation network (SIN) induces Cdr2 dissociation from cytokinetic precursors at this stage [12Goyal A. Takaine M. Simanis V. Nakano K. Dividing the spoils of growth and the cell cycle: The fission yeast as a model for the study of cytokinesis.Cytoskeleton. 2011; 68: 69-88Crossref Scopus (54) Google Scholar, 13Akamatsu M. Berro J. Pu K.M. Tebbs I.R. Pollard T.D. Cytokinetic nodes in fission yeast arise from two distinct types of nodes that merge during interphase.J. Cell Biol. 2014; 204: 977-988Crossref PubMed Scopus (46) Google Scholar, 14Pu K.M. Akamatsu M. Pollard T.D. The septation initiation network controls the assembly of nodes containing Cdr2p for cytokinesis in fission yeast.J. Cell Sci. 2015; 128: 441-446Crossref PubMed Scopus (12) Google Scholar]. We show here that SIN-dependent phosphorylation of Cdr2 promotes its interaction with the 14-3-3 protein Rad24 that sequesters it in the cytoplasm during cell division. If this interaction is compromised, cytokinetic precursors are asymmetrically distributed in the cortex of newborn cells, leading to asymmetrical division if nuclear signaling is abolished. We conclude that, through this new function, the SIN resets the division plane in newborn cells to ensure medial division.