The Dam1 ring binds to the E-hook of tubulin and diffuses along the microtubule

Ramey, Vincent H.; Wang, Hong-Wei; Nakajima, Yuko; Wong, Amanda; Liu, Jian; Drubin, David; Barnes, Georjana; Nogales, Eva

doi:10.1091/mbc.e10-10-0841

The Dam1 ring binds to the E-hook of tubulin and diffuses along the microtubule

Journal Article · Fri Dec 17 00:00:00 EST 2010 · Molecular Biology of the Cell

DOI:https://doi.org/10.1091/mbc.e10-10-0841· OSTI ID:1625224

Ramey, Vincent H. ^[1]; Wang, Hong-Wei ^[2]; Nakajima, Yuko ^[3]; Wong, Amanda ^[4]; Liu, Jian ^[5]; Drubin, David ^[3]; Barnes, Georjana ^[3]; Nogales, Eva ^[6]

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

There has been much effort in recent years aimed at understanding the molecular mechanism by which the Dam1 kinetochore complex is able to couple microtubule depolymerization to poleward movement. Both a biased diffusion and a forced walk model have been proposed, and several key functional aspects of Dam1-microtubule binding are disputed. Here, we investigate the elements involved in tubulin-Dam1 complex interactions and directly visualize Dam1 rings on microtubules in order to infer their dynamic behavior on the microtubule lattice and its likely relevance at the kinetochore. We find that the Dam1 complex has a preference for native tubulin over tubulin that is lacking its acidic C-terminal tail. Statistical mechanical analysis of images of Dam1 rings on microtubules, applied to both the distance between rings and the tilt angle of the rings with respect to the microtubule axis, supports a diffusive ring model. We also present a cryo-EM reconstruction of the Dam1 ring, likely the relevant assembly form of the complex for energy coupling during microtubule depolymerization in budding yeast. The present studies constitute a significant step forward by linking structural and biochemical observations toward a comprehensive understanding of the Dam1 complex.

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:: 1625224

Journal Information:: Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 4 Vol. 22; ISSN 1059-1524

Publisher:: American Society for Cell BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Processivity vs. Beating: Comparing Cytoplasmic and Axonemal Dynein Microtubule Binding Domain Association with Microtubule Tajielyato, Nayere; Alexov, Emil International Journal of Molecular Sciences, Vol. 20, Issue 5 https://doi.org/10.3390/ijms20051090	journal	March 2019
E-hooks provide guidance and a soft landing for the microtubule binding domain of dynein Tajielyato, Nayere; Li, Lin; Peng, Yunhui Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-31480-9	journal	September 2018
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An array of nuclear microtubules reorganizes the budding yeast nucleus during quiescence Laporte, Damien; Courtout, Fabien; Salin, Bénédicte Journal of Cell Biology, Vol. 203, Issue 4 https://doi.org/10.1083/jcb.201306075	journal	November 2013
Subunit organization in the Dam1 kinetochore complex and its ring around microtubules Ramey, Vincent H.; Wong, Amanda; Fang, Jie Molecular Biology of the Cell, Vol. 22, Issue 22 https://doi.org/10.1091/mbc.e11-07-0659	journal	November 2011
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