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Molecular Cancer Therapeutics
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Cancer Therapeutics Insights

Microtubule Dynamics Control Tail Retraction in Migrating Vascular Endothelial Cells

Anutosh Ganguly, Hailing Yang, Hong Zhang, Fernando Cabral and Kamala D. Patel
Anutosh Ganguly
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
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Hailing Yang
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
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Hong Zhang
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
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Fernando Cabral
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
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Kamala D. Patel
1Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, University of Calgary, Calgary, Alberta, Canada; 2Department of Integrative Biology and Pharmacology, University of Texas Medical School; and 3University of Texas, MD Anderson Cancer Center, Houston, Texas
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DOI: 10.1158/1535-7163.MCT-13-0401 Published December 2013
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Abstract

Drugs that target microtubules are potent inhibitors of angiogenesis, but their mechanism of action is not well understood. To explore this, we treated human umbilical vein endothelial cells with paclitaxel, vinblastine, and colchicine and measured the effects on microtubule dynamics and cell motility. In general, lower drug concentrations suppressed microtubule dynamics and inhibited cell migration whereas higher concentrations were needed to inhibit cell division; however, surprisingly, large drug-dependent differences were seen in the relative concentrations needed to inhibit these two processes. Suppression of microtubule dynamics did not significantly affect excursions of lamellipodia away from the nucleus or prevent cells from elongating; but, it did inhibit retraction of the trailing edges that are normally enriched in dynamic microtubules, thereby limiting cell locomotion. Complete removal of microtubules with a high vinblastine concentration caused a loss of polarity that resulted in roundish, rather than elongated, cells, rapid but nondirectional membrane activity, and little cell movement. The results are consistent with a model in which more static microtubules stabilize the leading edge of migrating cells, whereas more dynamic microtubules locate to the rear where they can remodel and allow tail retraction. Suppressing microtubule dynamics interferes with tail retraction, but removal of microtubules destroys the asymmetry needed for cell elongation and directional motility. The prediction that suppressing microtubule dynamics might be sufficient to prevent angiogenesis was supported by showing that low concentrations of paclitaxel could prevent the formation of capillary-like structures in an in vitro tube formation assay. Mol Cancer Ther; 12(12); 2837–46. ©2013 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Molecular Cancer Therapeutics Online (http://mct.aacrjournals.org/).

  • Received May 17, 2013.
  • Revision received September 25, 2013.
  • Accepted September 27, 2013.
  • ©2013 American Association for Cancer Research.
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Molecular Cancer Therapeutics: 12 (12)
December 2013
Volume 12, Issue 12
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Microtubule Dynamics Control Tail Retraction in Migrating Vascular Endothelial Cells
Anutosh Ganguly, Hailing Yang, Hong Zhang, Fernando Cabral and Kamala D. Patel
Mol Cancer Ther December 1 2013 (12) (12) 2837-2846; DOI: 10.1158/1535-7163.MCT-13-0401

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Microtubule Dynamics Control Tail Retraction in Migrating Vascular Endothelial Cells
Anutosh Ganguly, Hailing Yang, Hong Zhang, Fernando Cabral and Kamala D. Patel
Mol Cancer Ther December 1 2013 (12) (12) 2837-2846; DOI: 10.1158/1535-7163.MCT-13-0401
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Molecular Cancer Therapeutics
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