Minireview - Microtubules and Tubulin Oligomers: Shape Transitions and Assembly by Intrinsically Disordered Protein Tau and Cationic Biomolecules
Abstract
In this minireview, which is part of a special issue in honor of Jacob N. Israelachvili’s remarkable research career on intermolecular forces and interfacial science, we present studies of structures, phase behavior, and forces in reaction mixtures of microtubules (MTs) and tubulin oligomers with either intrinsically disordered protein (IDP) Tau, cationic vesicles, or the polyamine spermine (4+). Bare MTs consist of 13 protofilaments (PFs), on average, where each PF is made of a linear stack of αβ-tubulin dimers (i.e., tubulin oligomers). We begin with a series of experiments which demonstrate the flexibility of PFs toward shape changes in response to local environmental cues. First, studies show that MT-associated protein (MAP) Tau controls the diameter of microtubules upon binding to the outer surface, implying a shape change in the cross-sectional area of PFs forming the MT perimeter. The diameter of a MT may also be controlled by the charge density of a lipid bilayer membrane that coats the outer surface. We further describe an experimental study where it is unexpectedly found that the biologically relevant polyamine spermine (+4e) is able to depolymerize taxol-stabilized microtubules with efficiency that increases with decreasing temperature. This MT destabilization drives a dynamical structural transition where inside-outmore »
- Authors:
-
- Univ. of California, Santa Barbara, CA (United States)
- Univ. of Chicago, IL (United States)
- Amorepacific Corporation R&D Center, Yongin (Korea)
- Korea Advanced Inst. of Science and Technology (KAIST), Daejeon (Korea)
- The Hebrew Univ. of Jerusalem (Israel)
- Publication Date:
- Research Org.:
- Univ. of California, Santa Barbara, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1763429
- Grant/Contract Number:
- FG02-06ER46314
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Langmuir
- Additional Journal Information:
- Journal Volume: 35; Journal Issue: 48; Journal ID: ISSN 0743-7463
- Publisher:
- American Chemical Society
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Vesicles; Lipids; Oligomers; X-ray scattering; Mixtures
Citation Formats
Safinya, Cyrus R., Chung, Peter J., Song, Chaeyeon, Li, Youli, Miller, Herbert P., Choi, Myung Chul, Raviv, Uri, Ewert, Kai K., Wilson, Leslie, and Feinstein, Stuart C. Minireview - Microtubules and Tubulin Oligomers: Shape Transitions and Assembly by Intrinsically Disordered Protein Tau and Cationic Biomolecules. United States: N. p., 2019.
Web. doi:10.1021/acs.langmuir.9b02208.
Safinya, Cyrus R., Chung, Peter J., Song, Chaeyeon, Li, Youli, Miller, Herbert P., Choi, Myung Chul, Raviv, Uri, Ewert, Kai K., Wilson, Leslie, & Feinstein, Stuart C. Minireview - Microtubules and Tubulin Oligomers: Shape Transitions and Assembly by Intrinsically Disordered Protein Tau and Cationic Biomolecules. United States. https://doi.org/10.1021/acs.langmuir.9b02208
Safinya, Cyrus R., Chung, Peter J., Song, Chaeyeon, Li, Youli, Miller, Herbert P., Choi, Myung Chul, Raviv, Uri, Ewert, Kai K., Wilson, Leslie, and Feinstein, Stuart C. Fri .
"Minireview - Microtubules and Tubulin Oligomers: Shape Transitions and Assembly by Intrinsically Disordered Protein Tau and Cationic Biomolecules". United States. https://doi.org/10.1021/acs.langmuir.9b02208. https://www.osti.gov/servlets/purl/1763429.
@article{osti_1763429,
title = {Minireview - Microtubules and Tubulin Oligomers: Shape Transitions and Assembly by Intrinsically Disordered Protein Tau and Cationic Biomolecules},
author = {Safinya, Cyrus R. and Chung, Peter J. and Song, Chaeyeon and Li, Youli and Miller, Herbert P. and Choi, Myung Chul and Raviv, Uri and Ewert, Kai K. and Wilson, Leslie and Feinstein, Stuart C.},
abstractNote = {In this minireview, which is part of a special issue in honor of Jacob N. Israelachvili’s remarkable research career on intermolecular forces and interfacial science, we present studies of structures, phase behavior, and forces in reaction mixtures of microtubules (MTs) and tubulin oligomers with either intrinsically disordered protein (IDP) Tau, cationic vesicles, or the polyamine spermine (4+). Bare MTs consist of 13 protofilaments (PFs), on average, where each PF is made of a linear stack of αβ-tubulin dimers (i.e., tubulin oligomers). We begin with a series of experiments which demonstrate the flexibility of PFs toward shape changes in response to local environmental cues. First, studies show that MT-associated protein (MAP) Tau controls the diameter of microtubules upon binding to the outer surface, implying a shape change in the cross-sectional area of PFs forming the MT perimeter. The diameter of a MT may also be controlled by the charge density of a lipid bilayer membrane that coats the outer surface. We further describe an experimental study where it is unexpectedly found that the biologically relevant polyamine spermine (+4e) is able to depolymerize taxol-stabilized microtubules with efficiency that increases with decreasing temperature. This MT destabilization drives a dynamical structural transition where inside-out curving of PFs, during the depolymerization peeling process, is followed by reassembly of ring-like curved PF building blocks into an array of helical inverted tubulin tubules. We finally turn to a very recent study on pressure–distance measurements in bundles of MTs employing the small-angle X-ray scattering (SAXS)-osmotic pressure technique, which complements the surface-forces-apparatus technique developed by Jacob N. Israelachvili. Furthermore, these latter studies are among the very few which are beginning to shed light on the precise nature of the interactions between MTs mediated by MAP Tau in 37 °C reaction mixtures containing GTP and lacking taxol.},
doi = {10.1021/acs.langmuir.9b02208},
journal = {Langmuir},
number = 48,
volume = 35,
place = {United States},
year = {Fri Sep 20 00:00:00 EDT 2019},
month = {Fri Sep 20 00:00:00 EDT 2019}
}
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