Published 5 June 2006. doi:10.1083/jcb.200601060
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 173, Number 5, 733-741
Microtubules can bear enhanced compressive loads in living cells because of lateral reinforcement
Clifford P. Brangwynne2,
Frederick C. MacKintosh3,
Sanjay Kumar4,6,
Nicholas A. Geisse2,
Jennifer Talbot2,
L. Mahadevan2,
Kevin K. Parker2,
Donald E. Ingber4,5,6, and
David A. Weitz1,2
1 Department of Physics and 2 Division of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138
3 Department of Physics and Astronomy, Vrije Universiteit, 1081 HV Amsterdam, Netherlands
4 Vascular Biology Program, 5 Department of Pathology, and 6 Department of Surgery, Children's Hospital, Harvard Medical School, Boston, MA 02115
Correspondence to David A. Weitz: weitz{at}deas.harvard.edu
Cytoskeletal microtubules have been proposed to influence cell shape and mechanics based on their ability to resist large-scale compressive forces exerted by the surrounding contractile cytoskeleton. Consistent with this, cytoplasmic microtubules are often highly curved and appear buckled because of compressive loads. However, the results of in vitro studies suggest that microtubules should buckle at much larger length scales, withstanding only exceedingly small compressive forces. This discrepancy calls into question the structural role of microtubules, and highlights our lack of quantitative knowledge of the magnitude of the forces they experience and can withstand in living cells. We show that intracellular microtubules do bear large-scale compressive loads from a variety of physiological forces, but their buckling wavelength is reduced significantly because of mechanical coupling to the surrounding elastic cytoskeleton. We quantitatively explain this behavior, and show that this coupling dramatically increases the compressive forces that microtubules can sustain, suggesting they can make a more significant structural contribution to the mechanical behavior of the cell than previously thought possible.
S. Kumar's present address is Dept. of Bioengineering, University of California, Berkeley, Berkeley, CA 94720.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
Related Article
-
Reinforced microtubules
- Rabiya S. Tuma
J. Cell Biol. 2006 173: 640.
[Full Text]
[PDF]
This article has been cited by other articles:
-
Lautenschlager, F., Paschke, S., Schinkinger, S., Bruel, A., Beil, M., Guck, J.
(2009). The regulatory role of cell mechanics for migration of differentiating myeloid cells. Proc. Natl. Acad. Sci. USA
106: 15696-15701
[Abstract]
[Full Text]
-
Fassett, J. T., Xu, X., Hu, X., Zhu, G., French, J., Chen, Y., Bache, R. J.
(2009). Adenosine regulation of microtubule dynamics in cardiac hypertrophy. Am. J. Physiol. Heart Circ. Physiol.
297: H523-H532
[Abstract]
[Full Text]
-
Matos, I., Pereira, A. J., Lince-Faria, M., Cameron, L. A., Salmon, E. D., Maiato, H.
(2009). Synchronizing chromosome segregation by flux-dependent force equalization at kinetochores. JCB
186: 11-26
[Abstract]
[Full Text]
-
Bicek, A. D., Tuzel, E., Demtchouk, A., Uppalapati, M., Hancock, W. O., Kroll, D. M., Odde, D. J.
(2009). Anterograde Microtubule Transport Drives Microtubule Bending in LLC-PK1 Epithelial Cells. Mol. Biol. Cell
20: 2943-2953
[Abstract]
[Full Text]
-
Iribe, G., Ward, C. W., Camelliti, P., Bollensdorff, C., Mason, F., Burton, R. A.B., Garny, A., Morphew, M. K., Hoenger, A., Lederer, W. J., Kohl, P.
(2009). Axial Stretch of Rat Single Ventricular Cardiomyocytes Causes an Acute and Transient Increase in Ca2+ Spark Rate. Circ. Res.
104: 787-795
[Abstract]
[Full Text]
-
Geiger, R. C., Kaufman, C. D., Lam, A. P., Budinger, G. R. S., Dean, D. A.
(2009). Tubulin Acetylation and Histone Deacetylase 6 Activity in the Lung under Cyclic Load. Am. J. Respir. Cell Mol. Bio.
40: 76-82
[Abstract]
[Full Text]
-
Nagayama, K., Matsumoto, T.
(2008). Contribution of actin filaments and microtubules to quasi-in situ tensile properties and internal force balance of cultured smooth muscle cells on a substrate. Am. J. Physiol. Cell Physiol.
295: C1569-C1578
[Abstract]
[Full Text]
-
Brangwynne, C. P., Koenderink, G. H., MacKintosh, F. C., Weitz, D. A.
(2008). Cytoplasmic diffusion: molecular motors mix it up. JCB
183: 583-587
[Abstract]
[Full Text]
-
Brangwynne, C. P., MacKintosh, F. C., Weitz, D. A.
(2007). Force fluctuations and polymerization dynamics of intracellular microtubules. Proc. Natl. Acad. Sci. USA
104: 16128-16133
[Abstract]
[Full Text]
-
Malek, A. M., Xu, C., Kim, E. S., Alper, S. L.
(2007). Hypertonicity triggers RhoA-dependent assembly of myosin-containing striated polygonal actin networks in endothelial cells. Am. J. Physiol. Cell Physiol.
292: C1645-C1659
[Abstract]
[Full Text]