Microtubule protofilament number is modulated in a stepwise fashion by the charge density of an enveloping layer

Uri Raviv; Toan Nguyen; Rouzbeh Ghafouri; Daniel J. Needleman; Youli Li; Herbert P. Miller; Leslie Wilson; Robijn F. Bruinsma; Cyrus R. Safinya

doi:10.1529/biophysj.106.087478

Microtubule protofilament number is modulated in a stepwise fashion by the charge density of an enveloping layer

Uri Raviv^*
, Toan Nguyen
, Rouzbeh Ghafouri
, Daniel J. Needleman
, Youli Li
, Herbert P. Miller
, Leslie Wilson
, Robijn F. Bruinsma
, Cyrus R. Safinya

^*Corresponding author for this work

Institute of Chemistry

Research output: Contribution to journal › Article › peer-review

30 Scopus citations

Abstract

Microtubules are able to adjust their protofilament (PF) number and, as a consequence, their dynamics and function, to the assembly conditions and presence of cofactors. However, the principle behind such variations is poorly understood. Using synchrotron x-ray scattering and transmission electron microscopy, we studied how charged membranes, which under certain conditions can envelop preassembled MTs, regulate the PF number of those MTs. We show that the mean PF number, 〈N〉, is modulated primarily by the charge density of the membranes. 〈N〉 decreases in a stepwise fashion with increasing membrane charge density. 〈N〉 does not depend on the membrane-protein stoichiometry or the solution ionic strength. We studied the effect of taxol and found that 〈N〉 increases logarithmically with taxol/tubulin stoichiometry. We present a theoretical model, which by balancing the electrostatic and elastic interactions in the system accounts for the trends in our findings and reveals an effective MT bending stiffness of order 10-100 k_BT/nm, associated with the observed changes in PF number.

Original language	English
Pages (from-to)	278-287
Number of pages	10
Journal	Biophysical Journal
Volume	92
Issue number	1
DOIs	https://doi.org/10.1529/biophysj.106.087478
State	Published - Jan 2007

Bibliographical note

Funding Information:
This work was supported by National Institutes of Health grant GM-59288 (to U.R., D.J.N., Y.L., and C.R.S.), National Science Foundation grants DMR-0503347 and CTS-0404444, Dept. of Energy grant DE-FG02-06ER46314 (to U.R., D.J.N., Y.L., and C.R.S.), and National Institutes of Health grant NS13560 (to H.P.M. and L.W.). The University of California, Santa Barbara, Material Research Laboratory received support from National Science Foundation grant DMR-0080034. The Stanford Synchrotron Radiation Laboratory, where some of this work was done, is supported by the U.S. Dept. of Energy. U.R. received fellowship support from the International Human Frontier Science Program Organization and the European Molecular Biology Organization.

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title = "Microtubule protofilament number is modulated in a stepwise fashion by the charge density of an enveloping layer",

abstract = "Microtubules are able to adjust their protofilament (PF) number and, as a consequence, their dynamics and function, to the assembly conditions and presence of cofactors. However, the principle behind such variations is poorly understood. Using synchrotron x-ray scattering and transmission electron microscopy, we studied how charged membranes, which under certain conditions can envelop preassembled MTs, regulate the PF number of those MTs. We show that the mean PF number, 〈N〉, is modulated primarily by the charge density of the membranes. 〈N〉 decreases in a stepwise fashion with increasing membrane charge density. 〈N〉 does not depend on the membrane-protein stoichiometry or the solution ionic strength. We studied the effect of taxol and found that 〈N〉 increases logarithmically with taxol/tubulin stoichiometry. We present a theoretical model, which by balancing the electrostatic and elastic interactions in the system accounts for the trends in our findings and reveals an effective MT bending stiffness of order 10-100 kBT/nm, associated with the observed changes in PF number.",

author = "Uri Raviv and Toan Nguyen and Rouzbeh Ghafouri and Needleman, \{Daniel J.\} and Youli Li and Miller, \{Herbert P.\} and Leslie Wilson and Bruinsma, \{Robijn F.\} and Safinya, \{Cyrus R.\}",

note = "Funding Information: This work was supported by National Institutes of Health grant GM-59288 (to U.R., D.J.N., Y.L., and C.R.S.), National Science Foundation grants DMR-0503347 and CTS-0404444, Dept. of Energy grant DE-FG02-06ER46314 (to U.R., D.J.N., Y.L., and C.R.S.), and National Institutes of Health grant NS13560 (to H.P.M. and L.W.). The University of California, Santa Barbara, Material Research Laboratory received support from National Science Foundation grant DMR-0080034. The Stanford Synchrotron Radiation Laboratory, where some of this work was done, is supported by the U.S. Dept. of Energy. U.R. received fellowship support from the International Human Frontier Science Program Organization and the European Molecular Biology Organization. ",

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AU - Raviv, Uri

AU - Nguyen, Toan

AU - Ghafouri, Rouzbeh

AU - Needleman, Daniel J.

AU - Li, Youli

AU - Miller, Herbert P.

AU - Wilson, Leslie

AU - Bruinsma, Robijn F.

AU - Safinya, Cyrus R.

N1 - Funding Information: This work was supported by National Institutes of Health grant GM-59288 (to U.R., D.J.N., Y.L., and C.R.S.), National Science Foundation grants DMR-0503347 and CTS-0404444, Dept. of Energy grant DE-FG02-06ER46314 (to U.R., D.J.N., Y.L., and C.R.S.), and National Institutes of Health grant NS13560 (to H.P.M. and L.W.). The University of California, Santa Barbara, Material Research Laboratory received support from National Science Foundation grant DMR-0080034. The Stanford Synchrotron Radiation Laboratory, where some of this work was done, is supported by the U.S. Dept. of Energy. U.R. received fellowship support from the International Human Frontier Science Program Organization and the European Molecular Biology Organization.

PY - 2007/1

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N2 - Microtubules are able to adjust their protofilament (PF) number and, as a consequence, their dynamics and function, to the assembly conditions and presence of cofactors. However, the principle behind such variations is poorly understood. Using synchrotron x-ray scattering and transmission electron microscopy, we studied how charged membranes, which under certain conditions can envelop preassembled MTs, regulate the PF number of those MTs. We show that the mean PF number, 〈N〉, is modulated primarily by the charge density of the membranes. 〈N〉 decreases in a stepwise fashion with increasing membrane charge density. 〈N〉 does not depend on the membrane-protein stoichiometry or the solution ionic strength. We studied the effect of taxol and found that 〈N〉 increases logarithmically with taxol/tubulin stoichiometry. We present a theoretical model, which by balancing the electrostatic and elastic interactions in the system accounts for the trends in our findings and reveals an effective MT bending stiffness of order 10-100 kBT/nm, associated with the observed changes in PF number.

AB - Microtubules are able to adjust their protofilament (PF) number and, as a consequence, their dynamics and function, to the assembly conditions and presence of cofactors. However, the principle behind such variations is poorly understood. Using synchrotron x-ray scattering and transmission electron microscopy, we studied how charged membranes, which under certain conditions can envelop preassembled MTs, regulate the PF number of those MTs. We show that the mean PF number, 〈N〉, is modulated primarily by the charge density of the membranes. 〈N〉 decreases in a stepwise fashion with increasing membrane charge density. 〈N〉 does not depend on the membrane-protein stoichiometry or the solution ionic strength. We studied the effect of taxol and found that 〈N〉 increases logarithmically with taxol/tubulin stoichiometry. We present a theoretical model, which by balancing the electrostatic and elastic interactions in the system accounts for the trends in our findings and reveals an effective MT bending stiffness of order 10-100 kBT/nm, associated with the observed changes in PF number.

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Microtubule protofilament number is modulated in a stepwise fashion by the charge density of an enveloping layer

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