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Research Article

The reciprocal coordination and mechanics of molecular motors in living cells

Jeneva A. Laib, John A. Marin, Robert A. Bloodgood, and William H. Guilford
  1. Departments of aBiomedical Engineering and
  2. bCell Biology, University of Virginia, Charlottesville, VA 22908

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PNAS first published February 12, 2009; https://doi.org/10.1073/pnas.0809849106
Jeneva A. Laib
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John A. Marin
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Robert A. Bloodgood
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William H. Guilford
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  • For correspondence: guilford@virginia.edu
  1. Edited by J. Richard McIntosh, University of Colorado, Boulder, CO, and approved January 7, 2009 (received for review October 1, 2008)

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Abstract

Molecular motors in living cells are involved in whole-cell locomotion, contractility, developmental shape changes, and organelle movement and positioning. Whether motors of different directionality are functionally coordinated in cells or operate in a semirandom “tug of war” is unclear. We show here that anterograde and retrograde microtubule-based motors in the flagella of Chlamydomonas are regulated such that only motors of a common directionality are engaged at any single time. A laser trap was used to position microspheres on the plasma membrane of immobilized paralyzed Chlamydomonas flagella. The anterograde and retrograde movements of the microsphere were measured with nanometer resolution as microtubule-based motors engaged the transmembrane protein FMG-1. An average of 10 motors acted to move the microsphere in either direction. Reversal of direction during a transport event was uncommon, and quiescent periods separated every transport event, suggesting the coordinated and exclusive action of only a single motor type. After a jump to 32 °C, temperature-sensitive mutants of kinesin-2 (fla10) showed exclusively retrograde transport events, driven by 7 motors on average. These data suggest that molecular motors in living cells can be reciprocally coordinated to engage simultaneously in large numbers and for exclusive transport in a single direction, even when a mixed population of motors is present. This offers a unique model for studying the mechanics, regulation, and directional coordination of molecular motors in a living intracellular environment.

Keywords:
  • Chlamydomonas
  • dynein
  • flagella
  • kinesin-2
  • laser trap

Footnotes

  • 1To whom correspondence should be addressed. E-mail: guilford{at}virginia.edu
  • Author contributions: R.A.B. and W.H.G. designed research; J.A.L. and J.A.M. performed research; R.A.B. contributed new reagents/analytical tools; J.A.L. and W.H.G. analyzed data; and R.A.B. and W.H.G. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

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The reciprocal coordination and mechanics of molecular motors in living cells
Jeneva A. Laib, John A. Marin, Robert A. Bloodgood, William H. Guilford
Proceedings of the National Academy of Sciences Feb 2009, pnas.0809849106; DOI: 10.1073/pnas.0809849106

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The reciprocal coordination and mechanics of molecular motors in living cells
Jeneva A. Laib, John A. Marin, Robert A. Bloodgood, William H. Guilford
Proceedings of the National Academy of Sciences Feb 2009, pnas.0809849106; DOI: 10.1073/pnas.0809849106
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