Skip to main content
SpringerLink
Log in

Spatiotemporal regulation of the Dma1-mediated mitotic checkpoint coordinates mitosis with cytokinesis

  • Mini-Review
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

During cell division, the timing of mitosis and cytokinesis must be ordered to ensure that each daughter cell receives a complete, undamaged copy of the genome. In fission yeast, the septation initiation network (SIN) is responsible for this coordination, and a mitotic checkpoint dependent on the E3 ubiquitin ligase Dma1 and the protein kinase CK1 controls SIN signaling to delay cytokinesis when there are errors in mitosis. The participation of kinases and ubiquitin ligases in cell cycle checkpoints that maintain genome integrity is conserved from yeast to human, making fission yeast an excellent model system in which to study checkpoint mechanisms. In this review, we highlight recent advances and remaining questions related to checkpoint regulation, which requires the synchronized modulation of protein ubiquitination, phosphorylation, and subcellular localization.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahel I, Ahel D, Matsusaka T, Clark AJ, Pines J, Boulton SJ, West SC (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451:81–85

    Article  CAS  PubMed  Google Scholar 

  • Bernatik O, Ganji RS, Dijksterhuis JP, Konik P, Cervenka I, Polonio T, Krejci P, Schulte G, Bryja V (2011) Sequential activation and inactivation of Dishevelled in the Wnt/β-catenin pathway by casein kinases. J Biol Chem 286:10396–10410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bieganowski P, Shilinski K, Tsichlis PN, Brenner C (2004) Cdc123 and checkpoint forkhead associated with RING proteins control the cell cycle by controlling eIF2γ abundance. J Biol Chem 279:44656–44666

    Article  CAS  PubMed  Google Scholar 

  • Botchkarev VV, Haber JE (2018) Functions and regulation of the Polo-like kinase Cdc5 in the absence and presence of DNA damage. Curr Genet 64:87–96

    Article  CAS  PubMed  Google Scholar 

  • Bothos J, Summers MK, Venere M, Scolnick DM, Halazonetis TD (2003) The Chfr mitotic checkpoint protein functions with Ubc13-Mms2 to form Lys63-linked polyubiquitin chains. Oncogene 22:7101–7107

    Article  CAS  PubMed  Google Scholar 

  • Brooks L, Heimsath EG, Loring GL, Brenner C (2008) FHA-RING ubiquitin ligases in cell division cycle control. Cell Mol Life Sci 65:3458–3466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryja V, Schulte G, Rawal N, Grahn A, Arenas E (2007) Wnt-5a induces Dishevelled phosphorylation and dopaminergic differentiation via a CK1-dependent mechanism. J Cell Sci 120:586–595

    Article  CAS  Google Scholar 

  • Burgess A, Labbé J-C, Vigneron S, Bonneaud N, Strub JM, Dorsselaer AV, Lorca T, Castro A (2008) Chfr interacts and colocalizes with TCTP to the mitotic spindle. Oncogene 27:5554–5566

    Article  CAS  PubMed  Google Scholar 

  • Carmel G, Leichus B, Cheng X, Patterson SD, Mirza U, Chait BT, Kuret J (1994) Expression, purification, crystallization, and preliminary X-ray analysis of casein kinase-1 from schizosaccharomyces pombe. J Biol Chem 269:7304–7309

    CAS  PubMed  Google Scholar 

  • Casagolda D, del Valle-Perez B, Valls G, Lugilde E, Vinyoles M, Casado-Vela J, Solanas G, Batlle E, Reynolds AB, Casal JI et al (2010) A p120-catenin-CK1 complex regulates Wnt signaling. J Cell Sci 123:2621–2631

    Article  CAS  Google Scholar 

  • Castiel A, Danieli MM, David A, Moshkovitz S, Aplan PD, Kirsch IR, Brandeis M, Krämer A, Izraeli S (2011) The Stil protein regulates centrosome integrity and mitosis through suppression of Chfr. J Cell Sci 124:532–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cegielska A, Gietzen KF, Rivers A, Virshup DM (1998) Autoinhibition of casein kinase I E (CKIe) is relieved by protein phosphatases and limited proteolysis. J Biol Chem 273:1357–1364

    Article  CAS  PubMed  Google Scholar 

  • Chahwan R, Gravel S, Matsusaka T, Jackson SP (2013) Dma/RNF8 proteins are evolutionarily conserved E3 ubiquitin ligases that target septins. Cell Cycle 12:1000–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaturvedi P, Sudakin V, Bobiak ML, Fisher PW, Mattern MR, Jablonski SA, Hurle MR, Zhu Y, Yen TJ, Zhou B-BS (2002) Chfr regulates a mitotic stress pathway through its RING-finger domain with ubiquitin ligase activity. Cancer Res 62:1797–1801

    CAS  PubMed  Google Scholar 

  • Chin CF, Yeong FM (2010) Safeguarding entry into mitosis: the antephase checkpoint. Mol Cell Biol 30:22–32

    Article  CAS  PubMed  Google Scholar 

  • Cruciat C-M, Dolde C, de Groot REA, Ohkawara B, Reinhard C, Korswagen HC, Niehrs C (2013) RNA helicase DDX3 is a regulatory subunit of casein kinase 1 in Wnt–b-catenin signaling. Science 339:1436–1441

    Article  CAS  PubMed  Google Scholar 

  • Daniels MJ, Marson A, Venkitaraman AR (2004) PML bodies control the nuclear dynamics and function of the CHFR mitotic checkpoint protein. Nat Struct Mol Biol 11:1114–1121

    Article  CAS  PubMed  Google Scholar 

  • del Valle-Perez B, Arques O, Vinyoles M, de Herreros AG, Dunach M (2011) Coordinated action of CK1 isoforms in canonical Wnt signaling. Mol Cell Biol 31:2877–2888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dhillon N, Hoekstra MF (1994) Characterization of two protein kinases from Schizosaccharomyces pombe involved in the regulation of DNA repair. EMBO J 13:2777–2788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elmore ZC, Guillen RX, Gould KL (2018) The kinase domain of CK1 enzymes contains the localization cue essential for compartmentalized signaling at the spindle pole. Mol Biol Cell 29:1664–1674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eng GWL, Edison, Virshup DM (2017) Site-specific phosphorylation of casein kinase 1 δ (CK1δ) regulates its activity towards the circadian regulator PER2. PLoS One 12:e0177834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fan J-Y, Preuss F, Muskus MJ, Bjes ES, Price JL (2008) Drosophila and vertebrate casein kinase I exhibits evolutionary conservation of circadian function. Genetics 181:139–152

    Article  CAS  PubMed  Google Scholar 

  • Fraschini R, Bilotta D, Lucchini G, Piatti S (2004) Functional characterization of Dma1 and Dma2, the budding yeast homologues of Schizosaccharomyces Pombe Dma1 and Human Chfr. Mol Biol Cell 15:3796–3810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gietzen KF, Virshup DM (1999) Identification of inhibitory autophosphorylation sites in casein kinase I E. J Biol Chem 274:32063–32070

    Article  CAS  PubMed  Google Scholar 

  • Graves PR, Roach PJ (1995) Role of COOH-terminal phosphorylation in the regulation of casein kinase Id. J Biol Chem 270:21689–21694

    Article  CAS  PubMed  Google Scholar 

  • Greer YE, Rubin JS (2011) Casein kinase 1 delta functions at the centrosome to mediate Wnt-3a–dependent neurite outgrowth. J Cell Biol 192:993–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guertin DA, Venkatram S, Gould KL, McCollum D (2002) Dma1 prevents mitotic exit and cytokinesis by inhibiting the septation initiation network (SIN). Dev Cell 3:779–790

    Article  CAS  PubMed  Google Scholar 

  • Halaby M-J, Hakem A, Li L, Ghamrasni SE, Venkatesan S, Hande PM, Sanchez O, Hakem R (2013) Synergistic interaction of Rnf8 and p53 in the protection against genomic instability and tumorigenesis. PLOS Genet 9:e1003259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoekstra MF, Dhillon N, Carmel G, DeMaggio AJ, Lindberg RA, Hunter T, Kuret J (1994) Budding and fission yeast casein kinase I isoforms have dual-specificity protein kinase activity. Mol Biol Cell 5:877–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huen MSY, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131:901–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson AE, Gould KL (2011) Dma1 ubiquitinates the SIN scaffold, Sid4, to impede the mitotic localization of Plo1 kinase. EMBO J 30:341–354

    Article  CAS  PubMed  Google Scholar 

  • Johnson AE, Chen J-S, Gould KL (2013) CK1 Is required for a mitotic checkpoint that delays cytokinesis. Curr Biol 23:1920–1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones CM, Chen J-S, Johnson AE, Elmore ZC, Cullati SN, Beckley JR, Gould KL (2018) Relief of the Dma1-mediated checkpoint requires Dma1 autoubiquitination and dynamic localization. Mol Biol Cell 29:2176–2189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang D, Chen J, Wong J, Fang G (2002) The checkpoint protein Chfr is a ligase that ubiquitinates Plk1 and inhibits Cdc2 at the G2 to M transition. J Cell Biol 156:249–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashima L, Idogawa M, Mita H, Shitashige M, Yamada T, Ogi K, Suzuki H, Toyota M, Ariga H, Sasaki Y et al (2012) CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J Biol Chem 287:12975–12984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA (2011) Quantitative phosphoproteomics identifies substrates and functional modules of aurora and polo-like kinase activities in mitotic cells. Sci Signal 4:rs5–rs5

    Article  CAS  PubMed  Google Scholar 

  • Kim J-S, Park Y-Y, Park S-Y, Cho H, Kang D, Cho H (2011) The auto-ubiquitylation of E3 ubiquitin-protein ligase Chfr at G2 phase is required for accumulation of polo-like kinase 1 and mitotic entry in mammalian cells. J Biol Chem 286:30615–30623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knippschild U, Kruger M, Richter J, Xu P, García-Reyes B, Peifer C, Halekotte J, Bakulev V, Bischof J (2014) The CK1 family: contribution to cellular stress response and its role in carcinogenesis. Front Oncol 4:1–32

    Article  Google Scholar 

  • Koch A, Krug K, Pengelley S, Macek B, Hauf S (2011) Mitotic substrates of the kinase aurora with roles in chromatin regulation identified through quantitative phosphoproteomics of fission yeast. Sci Signal 4:rs6–rs6

    Article  CAS  PubMed  Google Scholar 

  • Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM et al (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318:1637–1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuret J, Johnson GS, Cha D, Christenson ER, DeMaggio AJ, Hoekstra MF (2002) Casein kinase 1 Is tightly associated with paired-helical filaments isolated from Alzheimer’s disease brain. J Neurochem 69:2506–2515

    Article  Google Scholar 

  • Kwon YE, Kim YS, Oh YM, Seol JH (2009) Nuclear localization of Chfr is crucial for its checkpoint function. Mol Cells 27:359–363

    Article  CAS  PubMed  Google Scholar 

  • Lera RF, Burkard ME (2012) High Mitotic activity of polo-like kinase 1 Is required for chromosome segregation and genomic integrity in human epithelial cells. J Biol Chem 287:42812–42825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li G, Yin H, Kuret J (2004) Casein kinase 1 delta phosphorylates Tau and disrupts its binding to microtubules. J Biol Chem 279:15938–15945

    Article  CAS  PubMed  Google Scholar 

  • Li L, Halaby M-J, Hakem A, Cardoso R, Ghamrasni SE, Harding S, Chan N, Bristow R, Sanchez O, Durocher D et al (2010) Rnf8 deficiency impairs class switch recombination, spermatogenesis, and genomic integrity and predisposes for cancer. J Exp Med 207:983–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Longenecker KL, Roach PJ, Hurley TD (1996) Three-dimensional structure of mammalian casein kinase I: molecular basis for phosphate recognition. J Mol Biol 257:618–631

    Article  CAS  PubMed  Google Scholar 

  • Longenecker KL, Roach PJ, Hurley TD (1998) Crystallographic studies of casein kinase I δ: toward a structural understanding of auto-inhibition. Acta Crystallogr D Biol Crystallogr 54:473–475

    Article  CAS  PubMed  Google Scholar 

  • Loring GL, Christensen KC, Gerber SA, Brenner C (2008) Yeast Chfr homologs retard cell cycle at G1 and G2/M via Ubc4 and Ubc13/Mms2-dependent ubiquitination. Cell Cycle 7:96–105

    Article  CAS  PubMed  Google Scholar 

  • Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131:887–900

    Article  CAS  PubMed  Google Scholar 

  • Matsusaka T, Pines J (2004) Chfr acts with the p38 stress kinases to block entry to mitosis in mammalian cells. J Cell Biol 166:507–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng Q-J, Logunova L, Maywood ES, Gallego M, Lebiecki J, Brown TM, Sládek M, Semikhodskii AS, Glossop NRJ, Piggins HD et al (2008) Setting clock speed in mammals: The CK1ɛ tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 58:78–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merlini L, Fraschini R, Boettcher B, Barral Y, Lucchini G, Piatti S (2012) Budding yeast Dma proteins control septin dynamics and the spindle position checkpoint by promoting the recruitment of the Elm1 kinase to the bud neck. PLOS Genet 8:e1002670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milne DM, Looby P, Meek DW (2001) Catalytic activity of protein kinase CK1δ (Casein Kinase 1δ) is essential for its normal subcellular localization. Exp Cell Res 263:43–54

    Article  CAS  PubMed  Google Scholar 

  • Morgenstern Y, Das Adhikari U, Ayyash M, Elyada E, Tóth B, Moor A, Itzkovitz S, Ben-Neriah Y (2017) Casein kinase 1-epsilon or 1-delta required for Wnt-mediated intestinal stem cell maintenance. EMBO J 36:3046–3061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murone M, Simanis V (1996) The fission yeast dma1 gene is a component of the spindle assembly checkpoint, required to prevent septum formation and premature exit from mitosis if spindle function is compromised. EMBO J 15:6605–6616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Musacchio A (2015) The molecular biology of spindle assembly checkpoint signaling dynamics. Curr Biol 25:R1002–R1018

    Article  CAS  Google Scholar 

  • Narasimamurthy R, Hunt SR, Lu Y, Fustin J-M, Okamura H, Partch CL, Forger DB, Kim JK, Virshup DM (2018) CK1δ/ε protein kinase primes the PER2 circadian phosphoswitch. Proc Natl Acad Sci 115:5986–5991

    Article  CAS  PubMed  Google Scholar 

  • Palou R, Palou G, Quintana DG (2017) A role for the spindle assembly checkpoint in the DNA damage response. Curr Genet 63:275–280

    Article  CAS  PubMed  Google Scholar 

  • Peng Y, Grassart A, Lu R, Wong CCL, Yates J, Barnes G, Drubin DG (2015) Casein kinase 1 promotes initiation of Clathrin-mediated endocytosis. Dev Cell 32:231–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peters JM, McKay RM, McKay JP, Graff JM (1999) Casein kinase I transduces Wnt signals. Nature 401:345–350

    Article  CAS  PubMed  Google Scholar 

  • Petronczki M, Matos J, Mori S, Gregan J, Bogdanova A, Schwickart M, Mechtler K, Shirahige K, Zachariae W, Nasmyth K (2006) Monopolar attachment of sister kinetochores at meiosis I requires casein kinase 1. Cell 126:1049–1064

    Article  CAS  PubMed  Google Scholar 

  • Plans V, Guerra-Rebollo M, Thomson TM (2008) Regulation of mitotic exit by the RNF8 ubiquitin ligase. Oncogene 27:1355–1365

    Article  CAS  PubMed  Google Scholar 

  • Rivers A, Gietzen KF, Vielhaber E, Virshup DM (1998) Regulation of casein kinase I E and casein kinase I D by an in vivo futile phosphorylation cycle. J Biol Chem 273:15980–15984

    Article  CAS  PubMed  Google Scholar 

  • Sanbhnani S, Yeong FM (2012) CHFR: a key checkpoint component implicated in a wide range of cancers. Cell Mol Life Sci 69:1669–1687

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Mir L, Salat-Canela C, Paulo E, Carmona M, Ayté J, Oliva B, Hidalgo E (2018) Phospho-mimicking Atf1 mutants bypass the transcription activating function of the MAP kinase Sty1 of fission yeast. Curr Genet 64:97–102

    Article  CAS  PubMed  Google Scholar 

  • Scolnick DM, Halazonetis TD (2000) Chfr defines a mitotic stress checkpoint that delays entry into metaphase. Nature 406:430–435

    Article  CAS  PubMed  Google Scholar 

  • Shtivelman E (2003) Promotion of mitosis by activated protein kinase B after DNA damage involves polo-like kinase 1 and checkpoint protein CHFR. Mol Cancer Res 1:959–969

    CAS  PubMed  Google Scholar 

  • Sillibourne JE, Milne DM, Takahashi M, Ono Y, Meek DW (2002) Centrosomal anchoring of the protein kinase CK1δ mediated by attachment to the large, coiled-coil Scaffolding protein CG-NAP/AKAP450. J Mol Biol 322:785–797

    Article  CAS  PubMed  Google Scholar 

  • Simanis V (2015) Pombe’s thirteen - control of fission yeast cell division by the septation initiation network. J Cell Sci 128:1465–1474

    Article  CAS  PubMed  Google Scholar 

  • Sveiczer Á, Horváth A (2017) How do fission yeast cells grow and connect growth to the mitotic cycle? Curr Genet 63:165–173

    Article  CAS  PubMed  Google Scholar 

  • Sy SM-H, Jiang J, Dong S, Lok GTM, Wu J, Cai H, Yeung ESL, Huang J, Chen J, Deng Y et al (2011) Critical roles of ring finger protein RNF8 in replication stress responses. J Biol Chem 286:22355–22361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takaki T, Trenz K, Costanzo V, Petronczki M (2008) Polo-like kinase 1 reaches beyond mitosis—cytokinesis, DNA damage response, and development. Curr Opin Cell Biol 20:650–660

    Article  CAS  PubMed  Google Scholar 

  • Tuttle RL, Bothos J, Summers MK, Luca FC, Halazonetis TD (2007) Defective in mitotic arrest 1/ring finger 8 is a checkpoint protein that antagonizes the human mitotic exit network. Mol Cancer Res 5:1304–1311

    Article  CAS  PubMed  Google Scholar 

  • Venerando A, Ruzzene M, Pinna LA (2014) Casein kinase: the triple meaning of a misnomer. Biochem J 460:141–156

    Article  CAS  PubMed  Google Scholar 

  • Vinyoles M, Del Valle-Pérez B, Curto J, Padilla M, Villarroel A, Yang J, de Herreros AG, Duñach M (2017) Activation of CK1ɛ by PP2A/PR61ɛ is required for the initiation of Wnt signaling. Oncogene 36:429–438

    Article  CAS  Google Scholar 

  • Wang B, Elledge SJ (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci 104:20759–20763

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Davis S, Menon S, Zhang J, Ding J, Cervantes S, Miller E, Jiang Y, Ferro-Novick S (2015) Ypt1/Rab1 regulates Hrr25/CK1δ kinase activity in ER–Golgi traffic and macroautophagy. J Cell Biol 210:273–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R-M, Carmel G, Sweet RM, Kuret J, Cheng X (1995) Crystal structure of casein kinase-1, a phosphate-directed protein kinase. EMBO J 14:1015–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Xu T, Zhang Y, Qin X (2017) Molecular basis for the regulation of the circadian clock kinases CK1δ and CK1ε. Cell Signal 31:58–65

    Article  CAS  PubMed  Google Scholar 

  • Ye Q, Ur SN, Su TY, Corbett KD (2016) Structure of the Saccharomyces cerevisiae Hrr25:Mam1 monopolin subcomplex reveals a novel kinase regulator. EMBO J 35:2139–2151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu X, Minter-Dykhouse K, Malureanu L, Zhao W-M, Zhang D, Merkle CJ, Ward IM, Saya H, Fang G, Deursen J van et al (2005) Chfr is required for tumor suppression and Aurora A regulation. Nat Genet 37:401–406

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Alaina Willet, MariaSanta Mangione, and other members of the Gould lab for critical comments on the manuscript. This work is supported by NIH R01-GM112989 (to KLG) and T32-CA119925 (to SNC).

Author information

Authors and Affiliations

  1. Vanderbilt University School of Medicine, Nashville, USA

    Sierra N. Cullati & Kathleen L. Gould

Authors
  1. Sierra N. Cullati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kathleen L. Gould
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathleen L. Gould.

Additional information

Communicated by M. Kupiec.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cullati, S.N., Gould, K.L. Spatiotemporal regulation of the Dma1-mediated mitotic checkpoint coordinates mitosis with cytokinesis. Curr Genet 65, 663–668 (2019). https://doi.org/10.1007/s00294-018-0921-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-018-0921-x

Keywords

Search

Navigation