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Eribulin Binds at Microtubule Ends to a Single Site on Tubulin To Suppress Dynamic Instability

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Department of Molecular, Cellular, and Developmental Biology and Neuroscience Research Institute, University of California, Santa Barbara, California 93106
§ Process Development
Scientific Administration
Eisai Research Institute, Andover, Massachusetts 01810.
*To whom correspondence should be addressed: Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93106. Phone: (805) 893-5317. Fax: (805) 893-5081. E-mail: [email protected]
⊥Current address: Harvard Medical School, Landmark 22A-West, 401 Park Dr., Boston, MA 01810.
Cite this: Biochemistry 2010, 49, 6, 1331–1337
Publication Date (Web):December 23, 2009
https://doi.org/10.1021/bi901810u
Copyright © 2009 American Chemical Society

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    Abstract

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    Eribulin mesylate (E7389), a synthetic analogue of the marine natural product halichondrin B, is in phase III clinical trials for the treatment of cancer. Eribulin targets microtubules, suppressing dynamic instability at microtubule plus ends through an inhibition of microtubule growth with little or no effect on shortening [Jordan, M. A., et al. (2005) Mol. Cancer Ther. 4, 1086−1095]. Using [3H]eribulin, we found that eribulin binds soluble tubulin at a single site; however, this binding is complex with an overall Kd of 46 μM, but also showing a real or apparent very high affinity (Kd = 0.4 μM) for a subset of 25% of the tubulin. Eribulin also binds microtubules with a maximum stoichiometry of 14.7 ± 1.3 molecules per microtubule (Kd = 3.5 μM), strongly suggesting the presence of a relatively high-affinity binding site at microtubule ends. At 100 nM, the concentration that inhibits microtubule plus end growth by 50%, we found that one molecule of eribulin is bound per two microtubules, indicating that the binding of a single eribulin molecule at a microtubule end can potently inhibit its growth. Eribulin does not suppress dynamic instability at microtubule minus ends. Preincubation of microtubules with 2 or 4 μM vinblastine induced additional lower-affinity eribulin binding sites, most likely at splayed microtubule ends. Overall, our results indicate that eribulin binds with high affinity to microtubule plus ends and thereby suppresses dynamic instability.

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