Myosin I Can Act As a Molecular Force Sensor
Abstract
The ability to sense molecular tension is crucial for a wide array of cellular processes, including the detection of auditory stimuli, control of cell shape, and internalization and transport of membranes. We show that myosin I, a motor protein that has been implicated in powering key steps in these processes, dramatically alters its motile properties in response to tension. We measured the displacement generated by single myosin I molecules, and we determined the actin-attachment kinetics with varying tensions using an optical trap. The rate of myosin I detachment from actin decreases >75-fold under tension of 2 piconewtons or less, resulting in myosin I transitioning from a low (<0.2) to a high (>0.9) duty-ratio motor. This impressive tension sensitivity supports a role for myosin I as a molecular force sensor.
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References and Notes
1
J. S. Berg, B. C. Powell, R. E. Cheney, Mol. Biol. Cell12, 780 (2001).
2
J. R. Holtet al., Cell108, 371 (2002).
3
C. Batters, M. I. Wallace, L. M. Coluccio, J. E. Molloy, Philos. Trans. R. Soc. London Ser. B359, 1895 (2004).
4
P. G. Gillespie, J. L. Cyr, Annu. Rev. Physiol.66, 521 (2004).
5
A. Boseet al., Nature420, 821 (2002).
6
R. E. McConnell, M. J. Tyska, J. Cell Biol.177, 671 (2007).
7
D. E. Hokanson, J. M. Laakso, T. Lin, D. Sept, E. M. Ostap, Mol. Biol. Cell17, 4856 (2006).
8
L. Salas-Corteset al., J. Cell Sci.118, 4823 (2005).
9
M. A. Geeves, C. Perreault-Micale, L. M. Coluccio, J. Biol. Chem.275, 21624 (2000).
10
C. Veigelet al., Nature398, 530 (1999).
11
J. D. Jontes, E. M. Wilson-Kubalek, R. A. Milligan, Nature378, 751 (1995).
12
R. F. Siemankowski, M. O. Wiseman, H. D. White, Proc. Natl. Acad. Sci. U.S.A.82, 658 (1985).
13
J. H. Lewis, T. Lin, D. E. Hokanson, E. M. Ostap, Biochemistry45, 11589 (2006).
14
C. Veigel, S. Schmitz, F. Wang, J. R. Sellers, Nat. Cell Biol.7, 861 (2005).
15
J. T. Finer, R. M. Simmons, J. A. Spudich, Nature368, 113 (1994).
16
T. Lin, N. Tang, E. M. Ostap, J. Biol. Chem.280, 41562 (2005).
17
See methods in supporting information on Science Online.
18
C. Veigel, J. E. Molloy, S. Schmitz, J. Kendrick-Jones, Nat. Cell Biol.5, 980 (2003).
19
D. M. Warshawet al., J. Biol. Chem.275, 37167 (2000).
20
C. Ruppert, R. Kroschewski, M. Bahler, J. Cell Biol.120, 1393 (1993).
21
Y. Takagi, E. E. Homsher, Y. E. Goldman, H. Shuman, Biophys. J.90, 1295 (2006).
22
G. I. Bell, Science200, 618 (1978).
23
D. Altman, H. L. Sweeney, J. A. Spudich, Cell116, 737 (2004).
24
D. Tsygankov, M. E. Fisher, Proc. Natl. Acad. Sci. U.S.A.104, 19321 (2007).
25
We thank T. Lin for technical assistance and Y. E. Goldman for helpful discussions. Supported by NIH grants AR051174 (H.S. and E.M.O.) and GM057247 (E.M.O.).
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Published In
Science
Volume 321 | Issue 5885
4 July 2008
4 July 2008
Copyright
American Association for the Advancement of Science.
Submission history
Received: 21 April 2008
Accepted: 9 June 2008
Published in print: 4 July 2008
Notes
Supporting Online Material
www.sciencemag.org/cgi/content/full/321/5885/133/DC1
Materials and Methods
Figs. S1 to S5
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- Joseph M. Laakso et al.
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