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Originally published In Press as doi:10.1074/jbc.C500186200 on June 2, 2005

J. Biol. Chem., Vol. 280, Issue 29, 26729-26734, July 22, 2005
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Inhibition of Histone Deacetylase 6 Acetylates and Disrupts the Chaperone Function of Heat Shock Protein 90

A NOVEL BASIS FOR ANTILEUKEMIA ACTIVITY OF HISTONE DEACETYLASE INHIBITORS*

Purva Bali{ddagger}, Michael Pranpat{ddagger}, James Bradner§, Maria Balasis{ddagger}, Warren Fiskus{ddagger}, Fei Guo{ddagger}, Kathy Rocha{ddagger}, Sandhya Kumaraswamy{ddagger}, Sandhya Boyapalle{ddagger}, Peter Atadja¶, Edward Seto{ddagger}, and Kapil Bhalla{ddagger}||

From the {ddagger}Department of Interdisciplinary Oncology, H. Lee Moffitt Cancer Center, Tampa, Florida 33612, §Dana-Farber Cancer Institute, Boston, Massachusetts 02115, and Novartis Pharmaceuticals Inc., Cambridge, Massachusetts 02139

The hydroxamic acid (HAA) analogue pan-histone deacetylase (HDAC) inhibitors (HDIs) LAQ824 and LBH589 have been shown to induce acetylation and inhibit the ATP binding and chaperone function of heat shock protein (HSP) 90. This promotes the polyubiquitylation and degradation of the pro-growth and pro-survival client proteins Bcr-Abl, mutant FLT-3, c-Raf, and AKT in human leukemia cells. HDAC6 is a member of the class IIB HDACs. It is predominantly cytosolic, microtubule-associated {alpha}-tubulin deacetylase that is also known to promote aggresome inclusion of the misfolded polyubiquitylated proteins. Here we demonstrate that in the Bcr-abl oncogene expressing human leukemia K562 cells, HDAC6 can be co-immunoprecipitated with HSP90, and the knock-down of HDAC6 by its siRNA induced the acetylation of HSP90 and {alpha}-tubulin. Depletion of HDAC6 levels also inhibited the binding of HSP90 to ATP, reduced the chaperone association of HSP90 with its client proteins, e.g. Bcr-Abl, and induced polyubiquitylation and partial depletion of Bcr-Abl. Conversely, the ectopic overexpression of HDAC6 inhibited LAQ824-induced acetylation of HSP90 and {alpha}-tubulin and reduced LAQ824-mediated depletion of Bcr-Abl, AKT, and c-Raf. Collectively, these findings indicate that HDAC6 is also an HSP90 deacetylase. Targeted inhibition of HDAC6 leads to acetylation of HSP90 and disruption of its chaperone function, resulting in polyubiquitylation and depletion of pro-growth and pro-survival HSP90 client proteins including Bcr-Abl. Depletion of HDAC6 sensitized human leukemia cells to HAA-HDIs and proteasome inhibitors.

Received for publication, May 5, 2005 , and in revised form, May 27, 2005.

* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

|| To whom correspondence should be addressed: Interdisciplinary Oncology Program, Moffitt Cancer Center and Research Inst., University of South Florida, 12902 Magnolia Dr., MRC 3 East, Rm. 3056, Tampa, FL 33612. Tel.: 813-903-6861; Fax: 813-903-6817; E-mail: bhallakn{at}moffitt.usf.edu.


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