Ensemble-Level Organization of Human Kinetochores and Evidence for Distinct Tension and Attachment Sensors

Cell Reports - Tập 31 Số 4 - Trang 107535 - 2020
Emanuele Roscioli1,2, Tsvetelina E. Germanova1,2, Christopher A. Smith1,2, Peter Embacher1,3, Muriel Erent1,2, Amelia I. Thompson1,2, Nigel J. Burroughs1,3, Andrew D. McAinsh1,2
1Centre for Mechanochemical Cell Biology, University of Warwick, Coventry, UK
2Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, UK
3Mathematics Institute, University of Warwick, Coventry, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Allan, 2020, Cyclin B1 scaffolds MAD1 at the kinetochore corona to activate the mitotic checkpoint, EMBO J., e103180, 10.15252/embj.2019103180

Alushin, 2010, The Ndc80 kinetochore complex forms oligomeric arrays along microtubules, Nature, 467, 805, 10.1038/nature09423

Amaro, 2010, Molecular control of kinetochore-microtubule dynamics and chromosome oscillations, Nat. Cell Biol., 12, 319, 10.1038/ncb2033

Aravamudhan, 2015, The kinetochore encodes a mechanical switch to disrupt spindle assembly checkpoint signalling, Nat. Cell Biol., 17, 868, 10.1038/ncb3179

Auckland, 2015, Building an integrated model of chromosome congression, J. Cell Sci., 128, 3363

Bajaj, 2018, KNL1 Binding to PP1 and Microtubules Is Mutually Exclusive, Structure, 26, 1327, 10.1016/j.str.2018.06.013

Booth, 2011, A TACC3/ch-TOG/clathrin complex stabilises kinetochore fibres by inter-microtubule bridging, EMBO J., 30, 906, 10.1038/emboj.2011.15

Brinkley, 1992, Structure and molecular organization of the centromere-kinetochore complex, Trends Cell Biol., 2, 15, 10.1016/0962-8924(92)90139-E

Burroughs, 2015, Super-resolution kinetochore tracking reveals the mechanisms of human sister kinetochore directional switching, eLife, 4, e09500, 10.7554/eLife.09500

Cheeseman, 2006, The conserved KMN network constitutes the core microtubule-binding site of the kinetochore, Cell, 127, 983, 10.1016/j.cell.2006.09.039

Churchman, 2005, Single molecule high-resolution colocalization of Cy3 and Cy5 attached to macromolecules measures intramolecular distances through time, Proc. Natl. Acad. Sci. USA, 102, 1419, 10.1073/pnas.0409487102

Churchman, 2006, A non-Gaussian distribution quantifies distances measured with fluorescence localization techniques, Biophys. J., 90, 668, 10.1529/biophysj.105.065599

Ciferri, 2005, Architecture of the human ndc80-hec1 complex, a critical constituent of the outer kinetochore, J. Biol. Chem., 280, 29088, 10.1074/jbc.M504070200

Ciferri, 2008, Implications for kinetochore-microtubule attachment from the structure of an engineered Ndc80 complex, Cell, 133, 427, 10.1016/j.cell.2008.03.020

Collin, 2013, The spindle assembly checkpoint works like a rheostat rather than a toggle switch, Nat. Cell Biol., 15, 1378, 10.1038/ncb2855

Craiu, 2014, Bayesian Computation via Markov Chain Monte Carlo, Annual Review of Statistics and Its Application, 1, 179, 10.1146/annurev-statistics-022513-115540

Currie, 2018, Bub1 is not essential for the checkpoint response to unattached kinetochores in diploid human cells, Curr. Biol., 28, R929, 10.1016/j.cub.2018.07.040

de Gennes, 1993

DeLuca, 2006, Kinetochore microtubule dynamics and attachment stability are regulated by Hec1, Cell, 127, 969, 10.1016/j.cell.2006.09.047

Doostmohammadi, 2018, Active nematics, Nat. Commun., 9, 3246, 10.1038/s41467-018-05666-8

Dudka, 2018, Complete microtubule-kinetochore occupancy favours the segregation of merotelic attachments, Nat. Commun., 9, 2042, 10.1038/s41467-018-04427-x

Etemad, 2015, Kinetochore-microtubule attachment is sufficient to satisfy the human spindle assembly checkpoint, Nat. Commun., 6, 8987, 10.1038/ncomms9987

Etemad, 2019, Spindle checkpoint silencing at kinetochores with submaximal microtubule occupancy, J. Cell Sci., 132, jcs231589, 10.1242/jcs.231589

Famulski, 2007, Aurora B kinase-dependent recruitment of hZW10 and hROD to tensionless kinetochores, Curr. Biol., 17, 2143, 10.1016/j.cub.2007.11.037

Gascoigne, 2011, Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes, Cell, 145, 410, 10.1016/j.cell.2011.03.031

Hamilton, 2019, Seeing is believing: our evolving view of kinetochore structure, composition, and assembly, Curr. Opin. Cell Biol., 60, 44, 10.1016/j.ceb.2019.03.016

Helgeson, 2018, Human Ska complex and Ndc80 complex interact to form a load-bearing assembly that strengthens kinetochore-microtubule attachments, Proc. Natl. Acad. Sci. USA, 115, 2740, 10.1073/pnas.1718553115

Hiruma, 2015, Competition between MPS1 and microtubules at kinetochores regulates spindle checkpoint signaling, Science, 348, 1264, 10.1126/science.aaa4055

Huis In ’t Veld, 2016, Molecular basis of outer kinetochore assembly on CENP-T, eLife, 5, e21007, 10.7554/eLife.21007

Huis In ’t Veld, 2019, Molecular determinants of the Ska-Ndc80 interaction and their influence on microtubule tracking and force-coupling, eLife, 8, e49539, 10.7554/eLife.49539

Ji, 2015, CELL DIVISION CYCLE. Kinetochore attachment sensed by competitive Mps1 and microtubule binding to Ndc80C, Science, 348, 1260, 10.1126/science.aaa4029

Joglekar, 2006, Molecular architecture of a kinetochore-microtubule attachment site, Nat. Cell Biol., 8, 581, 10.1038/ncb1414

Johnston, 2010, Vertebrate kinetochore protein architecture: protein copy number, J. Cell Biol., 189, 937, 10.1083/jcb.200912022

Kim, 2012, Structure of human Mad1 C-terminal domain reveals its involvement in kinetochore targeting, Proc. Natl. Acad. Sci. USA, 109, 6549, 10.1073/pnas.1118210109

Klare, 2015, CENP-C is a blueprint for constitutive centromere-associated network assembly within human kinetochores, J. Cell Biol., 210, 11, 10.1083/jcb.201412028

Kops, 2005, ZW10 links mitotic checkpoint signaling to the structural kinetochore, J. Cell Biol., 169, 49, 10.1083/jcb.200411118

Kuhn, 2017, Spindle assembly checkpoint satisfaction occurs via end-on but not lateral attachments under tension, J. Cell Biol., 216, 1533, 10.1083/jcb.201611104

Lampson, 2011, Sensing centromere tension: Aurora B and the regulation of kinetochore function, Trends Cell Biol., 21, 133, 10.1016/j.tcb.2010.10.007

Ledbetter, 1963, A “Microtubule” in Plant Cell Fine Structure, J. Cell Biol., 19, 239, 10.1083/jcb.19.1.239

London, 2012, Phosphoregulation of Spc105 by Mps1 and PP1 regulates Bub1 localization to kinetochores, Curr. Biol., 22, 900, 10.1016/j.cub.2012.03.052

Long, 2019, The mammalian kinetochore-microtubule interface: robust mechanics and computation with many microtubules, Curr. Opin. Cell Biol., 60, 60, 10.1016/j.ceb.2019.04.004

Magidson, 2016, Unattached kinetochores rather than intrakinetochore tension arrest mitosis in taxol-treated cells, J. Cell Biol., 212, 307, 10.1083/jcb.201412139

Maiolica, 2007, Structural analysis of multiprotein complexes by cross-linking, mass spectrometry, and database searching, Mol. Cell. Proteomics, 6, 2200, 10.1074/mcp.M700274-MCP200

Maresca, 2009, Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity, J. Cell Biol., 184, 373, 10.1083/jcb.200808130

Maresca, 2010, Welcome to a new kind of tension: translating kinetochore mechanics into a wait-anaphase signal, J. Cell Sci., 123, 825, 10.1242/jcs.064790

McAinsh, 2006, The human kinetochore proteins Nnf1R and Mcm21R are required for accurate chromosome segregation, EMBO J., 25, 4033, 10.1038/sj.emboj.7601293

Mosalaganti, 2017, Structure of the RZZ complex and molecular basis of its interaction with Spindly, J. Cell Biol., 216, 961, 10.1083/jcb.201611060

Musacchio, 2017, A Molecular View of Kinetochore Assembly and Function, Biology (Basel), 6, E5

Nicklas, 1969, Chromosome micromanipulation. 3. Spindle fiber tension and the reorientation of mal-oriented chromosomes, J. Cell Biol., 43, 40, 10.1083/jcb.43.1.40

Nicklas, 1995, Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint, J. Cell Biol., 130, 929, 10.1083/jcb.130.4.929

Nixon, 2015, The mesh is a network of microtubule connectors that stabilizes individual kinetochore fibers of the mitotic spindle, eLife, 4, e07635, 10.7554/eLife.07635

Olziersky, 2018, Mitotic live-cell imaging at different timescales, Methods Cell Biol., 145, 1, 10.1016/bs.mcb.2018.03.009

Pesenti, 2016, Progress in the structural and functional characterization of kinetochores, Curr. Opin. Struct. Biol., 37, 152, 10.1016/j.sbi.2016.03.003

Petrovic, 2010, The MIS12 complex is a protein interaction hub for outer kinetochore assembly, J. Cell Biol., 190, 835, 10.1083/jcb.201002070

Petrovic, 2014, Modular assembly of RWD domains on the Mis12 complex underlies outer kinetochore organization, Mol. Cell, 53, 591, 10.1016/j.molcel.2014.01.019

Rago, 2013, Review series: the functions and consequences of force at kinetochores, J. Cell Biol., 200, 557, 10.1083/jcb.201211113

Ran, 2013, Genome engineering using the CRISPR-Cas9 system, Nat. Protoc., 8, 2281, 10.1038/nprot.2013.143

Scarborough, 2019, Tight bending of the Ndc80 complex provides intrinsic regulation of its binding to microtubules, eLife, 8, e44489, 10.7554/eLife.44489

Screpanti, 2011, Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore, Curr. Biol., 21, 391, 10.1016/j.cub.2010.12.039

Shepperd, 2012, Phosphodependent recruitment of Bub1 and Bub3 to Spc7/KNL1 by Mph1 kinase maintains the spindle checkpoint, Curr. Biol., 22, 891, 10.1016/j.cub.2012.03.051

Silió, 2015, KNL1-Bubs and RZZ Provide Two Separable Pathways for Checkpoint Activation at Human Kinetochores, Dev. Cell, 35, 600, 10.1016/j.devcel.2015.11.012

Sironi, 2002, Crystal structure of the tetrameric Mad1-Mad2 core complex: implications of a ‘safety belt’ binding mechanism for the spindle checkpoint, EMBO J., 21, 2496, 10.1093/emboj/21.10.2496

Smith, 2016, Human kinetochores are swivel joints that mediate microtubule attachments, eLife, 5, e16159, 10.7554/eLife.16159

Suzuki, 2011, Spindle microtubules generate tension-dependent changes in the distribution of inner kinetochore proteins, J. Cell Biol., 193, 125, 10.1083/jcb.201012050

Suzuki, 2014, The architecture of CCAN proteins creates a structural integrity to resist spindle forces and achieve proper Intrakinetochore stretch, Dev. Cell, 30, 717, 10.1016/j.devcel.2014.08.003

Suzuki, 2018, An optimized method for 3D fluorescence co-localization applied to human kinetochore protein architecture, eLife, 7, e32418, 10.7554/eLife.32418

Tanaka, 2005, Kinetochore capture and bi-orientation on the mitotic spindle, Nat. Rev. Mol. Cell Biol., 6, 929, 10.1038/nrm1764

Tauchman, 2015, Stable kinetochore-microtubule attachment is sufficient to silence the spindle assembly checkpoint in human cells, Nat. Commun., 6, 10036, 10.1038/ncomms10036

Toso, 2009, Kinetochore-generated pushing forces separate centrosomes during bipolar spindle assembly, J. Cell Biol., 184, 365, 10.1083/jcb.200809055

Uchida, 2009, Kinetochore stretching inactivates the spindle assembly checkpoint, J. Cell Biol., 184, 383, 10.1083/jcb.200811028

Wan, 2009, Protein architecture of the human kinetochore microtubule attachment site, Cell, 137, 672, 10.1016/j.cell.2009.03.035

Wan, 2012, The coupling between sister kinetochore directional instability and oscillations in centromere stretch in metaphase PtK1 cells, Mol. Biol. Cell, 23, 1035, 10.1091/mbc.e11-09-0767

Wang, 2008, Architecture and flexibility of the yeast Ndc80 kinetochore complex, J. Mol. Biol., 383, 894, 10.1016/j.jmb.2008.08.077

Wei, 2005, Molecular organization of the Ndc80 complex, an essential kinetochore component, Proc. Natl. Acad. Sci. USA, 102, 5363, 10.1073/pnas.0501168102

Welburn, 2008, Toward a molecular structure of the eukaryotic kinetochore, Dev. Cell, 15, 645, 10.1016/j.devcel.2008.10.011

Welburn, 2010, Aurora B phosphorylates spatially distinct targets to differentially regulate the kinetochore-microtubule interface, Mol. Cell, 38, 383, 10.1016/j.molcel.2010.02.034

Wilson-Kubalek, 2008, Orientation and structure of the Ndc80 complex on the microtubule lattice, J. Cell Biol., 182, 1055, 10.1083/jcb.200804170

Yamagishi, 2012, MPS1/Mph1 phosphorylates the kinetochore protein KNL1/Spc7 to recruit SAC components, Nat. Cell Biol., 14, 746, 10.1038/ncb2515

Yoo, 2018, Measuring NDC80 binding reveals the molecular basis of tension-dependent kinetochore-microtubule attachments, eLife, 7, e36392, 10.7554/eLife.36392

Zhang, 2012, The Ndc80 internal loop is required for recruitment of the Ska complex to establish end-on microtubule attachment to kinetochores, J. Cell Sci., 125, 3243

Zhang, 2017, Bub1 positions Mad1 close to KNL1 MELT repeats to promote checkpoint signalling, Nat. Commun., 8, 15822, 10.1038/ncomms15822

Zhang, 2019, Efficient mitotic checkpoint signaling depends on integrated activities of Bub1 and the RZZ complex, EMBO J., 38, e100977, 10.15252/embj.2018100977