Subunit organization in the Dam1 kinetochore complex and its ring around microtubules

Ramey, Vincent H.; Wong, Amanda; Fang, Jie; Howes, Stuart; Barnes, Georjana; Nogales, Eva

doi:10.1091/mbc.e11-07-0659

Subunit organization in the Dam1 kinetochore complex and its ring around microtubules

Journal Article · Fri Sep 30 00:00:00 EDT 2011 · Molecular Biology of the Cell

DOI:https://doi.org/10.1091/mbc.e11-07-0659· OSTI ID:1625227

Ramey, Vincent H. ^[1]; Wong, Amanda ^[2]; Fang, Jie ^[3]; Howes, Stuart ^[2]; Barnes, Georjana ^[4]; Nogales, Eva ^[5]

Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Science Division; DOE/OSTI
Univ. of California, Berkeley, CA (United States). Biophysics Graduate Group
Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.
Univ. of California, Berkeley, CA (United States). Molecular and Cell Biology Dept.
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Science Division; Univ. of California, Berkeley, CA (United States). Molecular and Cell Biology Dept.; Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.

All eukaryotic cells must segregate their chromosomes equally between two daughter cells at each division. This process needs to be robust, as errors in the form of loss or gain of genetic material have catastrophic effects on viability. Chromosomes are captured, aligned, and segregated to daughter cells via interaction with spindle microtubules mediated by the kinetochore. In Saccharomyces cerevisiae one microtubule attaches to each kinetochore, requiring extreme processivity from this single connection. The yeast Dam1 complex, an essential component of the outer kinetochore, forms rings around microtubules and in vitro recapitulates much of the functionality of a kinetochore–microtubule attachment. To understand the mechanism of the Dam1 complex at the kinetochore, we must know how it binds to microtubules, how it assembles into rings, and how assembly is regulated. We used electron microscopy to map several subunits within the structure of the Dam1 complex and identify the organization of Dam1 complexes within the ring. Of importance, new data strongly support a more passive role for the microtubule in Dam1 ring formation. Integrating this information with previously published data, we generated a structural model for the Dam1 complex assembly that advances our understanding of its function and will direct future experiments.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625227

Journal Information:: Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 22 Vol. 22; ISSN 1059-1524

Publisher:: American Society for Cell BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (37)

A method for reverse interactome analysis: High-resolution mapping of interdomain interaction network in Dam1 complex and its specific disorganization based on the interaction domain expression Ikeuchi, Akinori; Nakano, Hideo; Kamiya, Takuma Biotechnology Progress https://doi.org/10.1002/btpr.403	journal	January 2010
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
A New Generation of the IMAGIC Image Processing System van Heel, Marin; Harauz, George; Orlova, Elena V. Journal of Structural Biology, Vol. 116, Issue 1 https://doi.org/10.1006/jsbi.1996.0004	journal	January 1996
When 2+2=5: The origins and fates of aneuploid and tetraploid cells King, Randall W. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, Vol. 1786, Issue 1 https://doi.org/10.1016/j.bbcan.2008.07.007	journal	September 2008
Kinetochore–microtubule interactions: the means to the end Tanaka, Tomoyuki U.; Desai, Arshad Current Opinion in Cell Biology, Vol. 20, Issue 1 https://doi.org/10.1016/j.ceb.2007.11.005	journal	February 2008
The Set1 Methyltransferase Opposes Ipl1 Aurora Kinase Functions in Chromosome Segregation Zhang, Ke; Lin, Wenchu; Latham, John A. Cell, Vol. 122, Issue 5 https://doi.org/10.1016/j.cell.2005.06.021	journal	September 2005
Topology representing network enables highly accurate classification of protein images taken by cryo electron-microscope without masking Ogura, Toshihiko; Iwasaki, Kenji; Sato, Chikara Journal of Structural Biology, Vol. 143, Issue 3 https://doi.org/10.1016/j.jsb.2003.08.005	journal	September 2003
Ab initio reconstruction of helical samples with heterogeneity, disorder and coexisting symmetries Ramey, Vincent H.; Wang, Hong-Wei; Nogales, Eva Journal of Structural Biology, Vol. 167, Issue 2 https://doi.org/10.1016/j.jsb.2009.05.002	journal	August 2009
Phospho-Regulation of Kinetochore-Microtubule Attachments by the Aurora Kinase Ipl1p Cheeseman, Iain M.; Anderson, Scott; Jwa, Miri Cell, Vol. 111, Issue 2 https://doi.org/10.1016/s0092-8674(02)00973-x	journal	October 2002
Polewards chromosome movement driven by microtubule depolymerization in vitro Koshland, Douglas E.; Mitchison, T. J.; Kirschner, Marc W. Nature, Vol. 331, Issue 6156 https://doi.org/10.1038/331499a0	journal	February 1988
Molecular architecture of the kinetochore–microtubule interface Cheeseman, Iain M.; Desai, Arshad Nature Reviews Molecular Cell Biology, Vol. 9, Issue 1 https://doi.org/10.1038/nrm2310	journal	January 2008
Architecture of the Dam1 kinetochore ring complex and implications for microtubule-driven assembly and force-coupling mechanisms Wang, Hong-Wei; Ramey, Vincent H.; Westermann, Stefan Nature Structural & Molecular Biology, Vol. 14, Issue 8 https://doi.org/10.1038/nsmb1274	journal	July 2007
The yeast DASH complex forms closed rings on microtubules Miranda, Jj L.; Wulf, Peter De; Sorger, Peter K. Nature Structural & Molecular Biology, Vol. 12, Issue 2 https://doi.org/10.1038/nsmb896	journal	January 2005
The Dam1 kinetochore complex harnesses microtubule dynamics to produce force and movement Asbury, C. L.; Gestaut, D. R.; Powers, A. F. Proceedings of the National Academy of Sciences, Vol. 103, Issue 26 https://doi.org/10.1073/pnas.0602249103	journal	June 2006
Different assemblies of the DAM1 complex follow shortening microtubules by distinct mechanisms Grishchuk, E. L.; Spiridonov, I. S.; Volkov, V. A. Proceedings of the National Academy of Sciences, Vol. 105, Issue 19 https://doi.org/10.1073/pnas.0801811105	journal	May 2008
The architecture of the DNA replication origin recognition complex in Saccharomyces cerevisiae Chen, Z.; Speck, C.; Wendel, P. Proceedings of the National Academy of Sciences, Vol. 105, Issue 30 https://doi.org/10.1073/pnas.0803829105	journal	July 2008
Theoretical problems related to the attachment of microtubules to kinetochores. Hill, T. L. Proceedings of the National Academy of Sciences, Vol. 82, Issue 13 https://doi.org/10.1073/pnas.82.13.4404	journal	July 1985
Implication of a novel multiprotein Dam1p complex in outer kinetochore function Cheeseman, Iain M.; Brew, Christine; Wolyniak, Michael Journal of Cell Biology, Vol. 155, Issue 7 https://doi.org/10.1083/jcb.200109063	journal	December 2001
Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity Maresca, Thomas J.; Salmon, Edward D. Journal of Cell Biology, Vol. 184, Issue 3 https://doi.org/10.1083/jcb.200808130	journal	February 2009
Cooperation of the Dam1 and Ndc80 kinetochore complexes enhances microtubule coupling and is regulated by aurora B Tien, Jerry F.; Umbreit, Neil T.; Gestaut, Daniel R. The Journal of Cell Biology, Vol. 189, Issue 4 https://doi.org/10.1083/jcb.200910142	journal	May 2010
The Dam1 complex confers microtubule plus end–tracking activity to the Ndc80 kinetochore complex Lampert, Fabienne; Hornung, Peter; Westermann, Stefan The Journal of Cell Biology, Vol. 189, Issue 4 https://doi.org/10.1083/jcb.200912021	journal	May 2010
Kinetochore Protein Interactions and their Regulation by the Aurora Kinase Ipl1p Shang, Ching; Hazbun, Tony R.; Cheeseman, Iain M. Molecular Biology of the Cell, Vol. 14, Issue 8 https://doi.org/10.1091/mbc.e02-11-0765	journal	August 2003
Protein Arms in the Kinetochore-Microtubule Interface of the Yeast DASH Complex Miranda, Jj L.; King, David S.; Harrison, Stephen C. Molecular Biology of the Cell, Vol. 18, Issue 7 https://doi.org/10.1091/mbc.e07-02-0135	journal	July 2007
Structures and Functions of Yeast Kinetochore Complexes Westermann, Stefan; Drubin, David G.; Barnes, Georjana Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.76.052705.160607	journal	June 2007
Structure-function insights into the yeast Dam1 kinetochore complex Nogales, Eva; Ramey, Vincent H. Journal of Cell Science, Vol. 122, Issue 21 https://doi.org/10.1242/jcs.004689	journal	November 2009
Mps1 Phosphorylation of Dam1 Couples Kinetochores to Microtubule Plus Ends at Metaphase R., Yates, John; Kerry, Bloom,; M., Shimogawa, Michelle The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/fnev-4658	text	January 2006
Phospho-Regulation of Kinetochore-Microtubule Attachments by the Aurora Kinase Ipl1p Cheeseman, Iain M.; Anderson, Scott; Jwa, Miri Cell, Vol. 111, Issue 2 https://doi.org/10.1016/S0092-8674(02)00973-X	journal	October 2002
Mps1 Phosphorylation of Dam1 Couples Kinetochores to Microtubule Plus Ends at Metaphase Shimogawa, Michelle M.; Graczyk, Beth; Gardner, Melissa K. Current Biology, Vol. 16, Issue 15 https://doi.org/10.1016/j.cub.2006.06.063	journal	August 2006
Formation of a Dynamic Kinetochore- Microtubule Interface through Assembly of the Dam1 Ring Complex Westermann, Stefan; Avila-Sakar, Agustin; Wang, Hong-Wei Molecular Cell, Vol. 17, Issue 2 https://doi.org/10.1016/j.molcel.2004.12.019	journal	January 2005
Mitotic forces control a cell-cycle checkpoint Li, Xiaotong; Nicklas, R. Bruce Nature, Vol. 373, Issue 6515 https://doi.org/10.1038/373630a0	journal	February 1995
The Dam1 kinetochore ring complex moves processively on depolymerizing microtubule ends Westermann, Stefan; Wang, Hong-Wei; Avila-Sakar, Agustin Nature, Vol. 440, Issue 7083 https://doi.org/10.1038/nature04409	journal	January 2006
Chromosomal passengers: conducting cell division Ruchaud, Sandrine; Carmena, Mar; Earnshaw, William C. Nature Reviews Molecular Cell Biology, Vol. 8, Issue 10 https://doi.org/10.1038/nrm2257	journal	October 2007
Saccharomyces cerevisiae septins: Supramolecular organization of heterooligomers and the mechanism of filament assembly Bertin, A.; McMurray, M. A.; Grob, P. Proceedings of the National Academy of Sciences, Vol. 105, Issue 24 https://doi.org/10.1073/pnas.0803330105	journal	June 2008
Saccharomyces cerevisiae Duo1p and Dam1p, Novel Proteins Involved in Mitotic Spindle Function Hofmann, Christian; Cheeseman, Iain M.; Goode, Bruce L. Journal of Cell Biology, Vol. 143, Issue 4 https://doi.org/10.1083/jcb.143.4.1029	journal	November 1998
Kinetochore stretching inactivates the spindle assembly checkpoint Uchida, Kazuhiko S. K.; Takagaki, Kentaro; Kumada, Kazuki Journal of Cell Biology, Vol. 184, Issue 3 https://doi.org/10.1083/jcb.200811028	journal	February 2009
The Dam1 ring binds to the E-hook of tubulin and diffuses along the microtubule Ramey, Vincent H.; Wang, Hong-Wei; Nakajima, Yuko Molecular Biology of the Cell, Vol. 22, Issue 4 https://doi.org/10.1091/mbc.e10-10-0841	journal	February 2011
Intrakinetochore stretch is associated with changes in kinetochore phosphorylation and spindle assembly checkpoint activity J., Maresca, Thomas; D., Salmon, Edward The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/vbse-3s42	text	January 2009

Cited By (12)

The kinetochore encodes a mechanical switch to disrupt spindle assembly checkpoint signalling Aravamudhan, Pavithra; Goldfarb, Alan A.; Joglekar, Ajit P. Nature Cell Biology, Vol. 17, Issue 7 https://doi.org/10.1038/ncb3179	journal	June 2015
The molecular architecture of the Dam1 kinetochore complex is defined by cross-linking based structural modelling Zelter, Alex; Bonomi, Massimiliano; Kim, Jae ook Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9673	journal	November 2015
Phosphoregulation promotes release of kinetochores from dynamic microtubules via multiple mechanisms Sarangapani, K. K.; Akiyoshi, B.; Duggan, N. M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 18 https://doi.org/10.1073/pnas.1220700110	journal	April 2013
Structural insights into WHAMM-mediated cytoskeletal coordination during membrane remodeling Shen, Qing-Tao; Hsiue, Peter P.; Sindelar, Charles V. Journal of Cell Biology, Vol. 199, Issue 1 https://doi.org/10.1083/jcb.201204010	journal	October 2012
Molecular requirements for the formation of a kinetochore–microtubule interface by Dam1 and Ndc80 complexes Lampert, Fabienne; Mieck, Christine; Alushin, Gregory M. The Journal of Cell Biology, Vol. 200, Issue 1 https://doi.org/10.1083/jcb.201210091	journal	December 2012
Structural plasticity of the living kinetochore Dhatchinamoorthy, Karthik; Shivaraju, Manjunatha; Lange, Jeffrey J. Journal of Cell Biology, Vol. 216, Issue 11 https://doi.org/10.1083/jcb.201703152	journal	September 2017
A Molecular View of Kinetochore Assembly and Function Musacchio, Andrea; Desai, Arshad Biology, Vol. 6, Issue 4 https://doi.org/10.3390/biology6010005	journal	January 2017
Synthetic protein interactions reveal a functional map of the cell Berry, Lisa K.; Ólafsson, Guðjón; Ledesma-Fernández, Elena eLife, Vol. 5 https://doi.org/10.7554/elife.13053	journal	April 2016
Kinetochore–microtubule error correction is driven by differentially regulated interaction modes Kalantzaki, Maria; Kitamura, Etsushi; Zhang, Tongli Nature Cell Biology, Vol. 17, Issue 4 https://doi.org/10.1038/ncb3128	journal	March 2015
A multi-scale model of the yeast chromosome-segregation system Ng, Cai Tong; Deng, Li; Chen, Chen Journal of Cell Biology https://doi.org/10.1101/299487	posted_content	April 2018
Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface Jenni, Simon; Harrison, Stephen C. Science, Vol. 360, Issue 6388 https://doi.org/10.1126/science.aar6436	journal	May 2018
The Ndc80 complex bridges two Dam1 complex rings Kim, Jae ook; Zelter, Alex; Umbreit, Neil T. eLife, Vol. 6 https://doi.org/10.7554/elife.21069	journal	February 2017

Similar Records

Molecular requirements for the formation of a kinetochore–microtubule interface by Dam1 and Ndc80 complexes

Journal Article · Sun Dec 30 19:00:00 EST 2012 · Journal of Cell Biology · OSTI ID:1625166

Structure of the DASH/Dam1 complex shows its role at the yeast kinetochore-microtubule interface

Journal Article · Thu May 03 20:00:00 EDT 2018 · Science · OSTI ID:1438840

Fission yeast dam1-A8 mutant is resistant to and rescued by an anti-microtubule agent

Journal Article · Fri Apr 11 00:00:00 EDT 2008 · Biochemical and Biophysical Research Communications · OSTI ID:21043703

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Cell Biology

Subunit organization in the Dam1 kinetochore complex and its ring around microtubules

Citation Formats

References (37)

Cited By (12)

Similar Records

Related Subjects