HDAC6 and Ovarian Cancer

International Journal of Molecular Sciences

Volumn 14, Issue 5, 2013, Pages 9514-9535

  Haakenson, Joshua ^a   Zhang, Xiaohong ^a,b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Cancer related signaling pathways; Cell stress response; HDAC6; HDAC6 inhibitors; Histone deacetylase; Motility; Oncogenesis; Ovarian cancer

Indexed keywords

3,4 DIHYDROQUINAXALIN 2(1H) ONE; ANTINEOPLASTIC AGENT; BORTEZOMIB; DYSFERLIN; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; NK 84; PIPERAZINE 2,5 DIONE ARYL HYDROXAMATE DERIVATIVE; SMALL INTERFERING RNA; SURVIVIN; TRANSCRIPTION FACTOR RUNX2; TRICHOSTATIN A; TUBACIN; UNCLASSIFIED DRUG; VORINOSTAT; HISTONE DEACETYLASE;

AGGRESOME; ANTINEOPLASTIC ACTIVITY; AUTOPHAGY; CANCER CELL CULTURE; CARCINOGENESIS; CELL MOTILITY; CELLULAR STRESS RESPONSE; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; ENZYME INHIBITION; GENE EXPRESSION; GENE LOCATION; HISTONE ACETYLRTANSFERASE AND DEACETYLASE GENE; HUMAN; INTRACELLULAR SIGNALING; NONHUMAN; OVARY CANCER; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; UNSPECIFIED SIDE EFFECT; ANIMAL; CELL MOTION; DRUG EFFECTS; ENZYMOLOGY; FEMALE; METABOLISM; OVARY TUMOR; PATHOLOGY; PHYSIOLOGICAL STRESS;

ANIMALS; CARCINOGENESIS; CELL MOVEMENT; FEMALE; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; OVARIAN NEOPLASMS; STRESS, PHYSIOLOGICAL;

EID: 84877330665     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14059514     Document Type: Review

References (152)

1. Wang, Z.; Zang, C.; Cui, K.; Schones, D.E.; Barski, A.; Peng, W.; Zhao, K. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009, 138, 1019-1031.
2. Marks, P.A.; Miller, T.; Richon, V.M. Histone deacetylases. Curr. Opin. Pharmacol. 2003, 3, 344-351.
3. Yang, X.J.; Seto, E. The Rpd3/Hda1 family of lysine deacetylases: From bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 2009, 9, 206-218.
4. Khochbin, S.; Verdel, A.; Lemercier, C.; Seigneurin-Berny, D. Functional significance of histone deacetylase diversity. Curr. Opin. Genet. Dev. 2001, 11, 162-166.
5. Fischle, W.; Kiermer, V.; Dequiedt, F.; Verdin, E. The emerging role of class II histone deacetylases. Biochem. Cell Biol. 2001, 79, 337-348.
6. Verdin, E.; Dequiedt, F.; Kasler, H.G. Class II histone deacetylases: Versatile regulators. Trends Genet. 2003, 19, 286-293.
7. Marks, P.; Rifkind, R.A.; Richon, V.M.; Breslow, R.; Miller, T.; Kelly, W.K. Histone deacetylases and cancer: Causes and therapies. Nat. Rev. Cancer 2001, 1, 194-202.
8. Zhang, J.; Sprung, R.; Pei, J.; Tan, X.; Kim, S.; Zhu, H.; Liu, C.F.; Grishin, N.V.; Zhao, Y. Lysine acetylation is a highly abundant and evolutionarily conserved modification in Escherichia coli. Mol. Cell. Proteomics 2009, 8, 215-225.
9. Choudhary, C.; Kumar, C.; Gnad, F.; Nielsen, M.L.; Rehman, M.; Walther, T.C.; Olsen, J.V.; Mann, M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325, 834-840.
10. Zhang, Y.; Gilquin, B.; Khochbin, S.; Matthias, P. Two catalytic domains are required for protein deacetylation. J. Biol. Chem. 2006, 281, 2401-2404.
11. Zou, H.; Wu, Y.; Navre, M.; Sang, B.C. Characterization of the two catalytic domains in histone deacetylase 6. Biochem. Biophys. Res. Commun. 2006, 341, 45-50.
12. Hershko, A.; Ciechanover, A. The ubiquitin system. Annu. Rev. Biochem. 1998, 67, 425-479.
13. Boyault, C.; Sadoul, K.; Pabion, M.; Khochbin, S. HDAC6, at the crossroads between cytoskeleton and cell signaling by acetylation and ubiquitination. Oncogene 2007, 26, 5468-5476.
14. Bertos, N.R.; Gilquin, B.; Chan, G.K.; Yen, T.J.; Khochbin, S.; Yang, X.J. Role of the tetradecapeptide repeat domain of human histone deacetylase 6 in cytoplasmic retention. J. Biol. Chem. 2004, 279, 48246-48254.
15. Kawaguchi, Y.; Kovacs, J.J.; McLaurin, A.; Vance, J.M.; Ito, A.; Yao, T.P. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 2003, 115, 727-738.
16. Boyault, C.; Gilquin, B.; Zhang, Y.; Rybin, V.; Garman, E.; Meyer-Klaucke, W.; Matthias, P.; Muller, C.W.; Khochbin, S. HDAC6-p97/VCP controlled polyubiquitin chain turnover. EMBO J. 2006, 25, 3357-3366.
17. Aldana-Masangkay, G.I.; Sakamoto, K.M. The role of HDAC6 in cancer. J. Biomed. Biotechnol. 2011, 2011, 875824:1-875824:10.
18. Zhang, X.; Yuan, Z.; Zhang, Y.; Yong, S.; Salas-Burgos, A.; Koomen, J.; Olashaw, N.; Parsons, J.T.; Yang, X.J.; Dent, S.R.; et al. HDAC6 modulates cell motility by altering the acetylation level of cortactin. Mol. Cell 2007, 27, 197-213.
19. Siegel, R.; DeSantis, C.; Virgo, K.; Stein, K.; Mariotto, A.; Smith, T.; Cooper, D.; Gansler, T.; Lerro, C.; Fedewa, S.; et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J. Clin. 2012, 62, 220-241.
20. National Cancer Institute. Drugs Approved for Ovarian Cancer. Available online: http://www.cancer.gov/cancertopics/druginfo/ovariancancer (accessed on 20 March 2013).
21. American Cancer Society. Cancer: Facts & Figures 2013. Available online: http://www.cancer.org/acs/groups/content/@epidemiologysurveilance/documents/document/acsp accessed on 20 March 2013.
22. Kuhn, E.; Kurman, R.J.; Shih, L.M. Ovarian cancer is an imported disease: Fact of fiction? Curr. Obstet. Gynecol. Rep. 2012, 1, 1-9.
23. Dinulescu, D.M.; Ince, T.A.; Quade, B.J.; Shafer, S.A.; Crowley, D.; Jacks, T. Role of K-ras and Pten in the development of mouse models of endometriosis and endometrioid ovarian cancer. Nat. Med. 2005, 11, 63-70.
24. Weinberg, R.A. The Biology of Cancer, 1st ed.; Garland Science: New York, NY, USA, 2007.
25. Schuler, S.; Ponnath, M.; Engel, J.; Ortmann, O. Ovarian epithelial tumors and reproductive factors: A systematic review. Arch. Gynecol. Obstet. 2013, doi:10.1007/s00404-013-2784-1
26. Verdel, A.; Curtet, S.; Brocard, M.P.; Rousseaux, S.; Lemercier, C.; Yoshida, M.; Khochbin, S. Active maintenance of mHDA2/mHDAC6 histone-deacetylase in the cytoplasm. Curr. Biol. 2000, 10, 747-749.
27. Inoue, A.; Yoshida, N.; Omoto, Y.; Oguchi, S.; Yamori, T.; Kiyama, R.; Hayashi, S. Development of cDNA microarray for expression profiling of estrogen-responsive genes. J. Mol. Endocrinol. 2002, 29, 175-192.
28. De Ruijter, A.J.; van Gennip, A.H.; Caron, H.N.; Kemp, S.; van Kuilenburg, A.B. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem. J. 2003, 370, 737-749.
29. Zhang, Z.; Yamashita, H.; Toyama, T.; Sugiura, H.; Omoto, Y.; Ando, Y.; Mita, K.; Hamaguchi, M.; Hayashi, S.; Iwase, H. HDAC6 expression is correlated with better survival in breast cancer. Clin. Cancer Res. 2004, 10, 6962-6968.
30. Sakuma, T.; Uzawa, K.; Onda, T.; Shiiba, M.; Yokoe, H.; Shibahara, T.; Tanzawa, H. Aberrant expression of histone deacetylase 6 in oral squamous cell carcinoma. Int. J. Oncol. 2006, 29, 117-124.
31. Bradbury, C.A.; Khanim, F.L.; Hayden, R.; Bunce, C.M.; White, D.A.; Drayson, M.T.; Craddock, C.; Turner, B.M. Histone deacetylases in acute myeloid leukaemia show a distinctive pattern of expression that changes selectively in response to deacetylase inhibitors. Leukemia 2005, 19, 1751-1759.
32. Lee, Y.S.; Lim, K.H.; Guo, X.; Kawaguchi, Y.; Gao, Y.; Barrientos, T.; Ordentlich, P.; Wang, X.F.; Counter, C.M.; Yao, T.P. The cytoplasmic deacetylase HDAC6 is required for efficient oncogenic tumorigenesis. Cancer Res. 2008, 68, 7561-7569.
33. Wang, H.; Holloway, M.P.; Ma, L.; Cooper, Z.A.; Riolo, M.; Samkari, A.; Elenitoba-Johnson, K.S.; Chin, Y.E.; Altura, R.A. Acetylation directs survivin nuclear localization to repress STAT3 oncogenic activity. J. Biol. Chem. 2010, 285, 36129-36137.
34. Riolo, M.T.; Cooper, Z.A.; Holloway, M.P.; Cheng, Y.; Bianchi, C.; Yakirevich, E.; Ma, L.; Chin, Y.E.; Altura, R.A. Histone deacetylase 6 (HDAC6) deacetylates survivin for its nuclear export in breast cancer. J. Biol. Chem. 2012, 287, 10885-10893.
35. Marcus, A.I.; Zhou, J.; O'Brate, A.; Hamel, E.; Wong, J.; Nivens, M.; El-Naggar, A.; Yao, T.P.; Khuri, F.R.; Giannakakou, P. The synergistic combination of the farnesyl transferase inhibitor lonafarnib and paclitaxel enhances tubulin acetylation and requires a functional tubulin deacetylase. Cancer Res. 2005, 65, 3883-3893.
36. Seigneurin-Berny, D.; Verdel, A.; Curtet, S.; Lemercier, C.; Garin, J.; Rousseaux, S.; Khochbin, S. Identification of components of the murine histone deacetylase 6 complex: Link between acetylation and ubiquitination signaling pathways. Mol. Cell. Biol. 2001, 21, 8035-8044.
37. Hook, S.S.; Orian, A.; Cowley, S.M.; Eisenman, R.N. Histone deacetylase 6 binds polyubiquitin through its zinc finger (PAZ domain) and copurifies with deubiquitinating enzymes. Proc. Natl. Acad. Sci. USA 2002, 99, 13425-13430.
38. Wojcik, C.; Yano, M.; DeMartino, G.N. RNA interference of valosin-containing protein (VCP/p97) reveals multiple cellular roles linked to ubiquitin/proteasome-dependent proteolysis. J. Cell Sci. 2004, 117, 281-292.
39. Kwon, S.; Zhang, Y.; Matthias, P. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 2007, 21, 3381-3394.
40. Mazroui, R.; di Marco, S.; Kaufman, R.J.; Gallouzi, I.E. Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell. 2007, 18, 2603-2618.
41. Legros, S.; Boxus, M.; Gatot, J.S.; Van Lint, C.; Kruys, V.; Kettmann, R.; Twizere, J.C.; Dequiedt, F. The HTLV-1 Tax protein inhibits formation of stress granules by interacting with histone deacetylase 6. Oncogene 2011, 30, 4050-4062.
42. Fusco, C.; Micale, L.; Egorov, M.; Monti, M.; D'Addetta, E.V.; Augello, B.; Cozzolino, F.; Calcagni, A.; Fontana, A.; Polishchuk, R.S.; et al. The E3-ubiquitin ligase TRIM50 interacts with HDAC6 and p62, and promotes the sequestration and clearance of ubiquitinated proteins into the aggresome. PLoS One 2012, 7, e40440.
43. Kopito, R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000, 10, 524-530.
44. Rodriguez-Gonzalez, A.; Lin, T.; Ikeda, A.K.; Simms-Waldrip, T.; Fu, C.; Sakamoto, K.M. Role of the aggresome pathway in cancer: Targeting histone deacetylase 6-dependent protein degradation. Cancer Res. 2008, 68, 2557-2560.
45. Garcia-Mata, R.; Gao, Y.S.; Sztul, E. Hassles with taking out the garbage: Aggravating aggresomes. Traffic 2002, 3, 388-396.
46. Wang, Y.; Meriin, A.B.; Zaarur, N.; Romanova, N.V.; Chernoff, Y.O.; Costello, C.E.; Sherman, M.Y. Abnormal proteins can form aggresome in yeast: Aggresome-targeting signals and components of the machinery. FASEB J. 2009, 23, 451-463.
47. Watabe, M.; Nakaki, T. Protein kinase CK2 regulates the formation and clearance of aggresomes in response to stress. J. Cell Sci. 2011, 124, 1519-1532.
48. Boyault, C.; Zhang, Y.; Fritah, S.; Caron, C.; Gilquin, B.; Kwon, S.H.; Garrido, C.; Yao, T.P.; Vourc'h, C.; Matthias, P.; et al. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes Dev. 2007, 21, 2172-2181.
49. +-induced stress. J. Neurochem. 2011, 117, 112-120.
50. Seibenhener, M.L.; Babu, J.R.; Geetha, T.; Wong, H.C.; Krishna, N.R.; Wooten, M.W. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 2004, 24, 8055-8068.
51. Bjorkoy, G.; Lamark, T.; Brech, A.; Outzen, H.; Perander, M.; Overvatn, A.; Stenmark, H.; Johansen, T. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 2005, 171, 603-614.
52. Klionsky, D.J. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8, 931-937.
53. Levine, B.; Klionsky, D.J. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev. Cell 2004, 6, 463-477.
54. Pandey, U.B.; Nie, Z.; Batlevi, Y.; McCray, B.A.; Ritson, G.P.; Nedelsky, N.B.; Schwartz, S.L.; DiProspero, N.A.; Knight, M.A.; Schuldiner, O.; et al. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 2007, 447, 859-863.
55. Lee, J.Y.; Yao, T.P. Quality control autophagy: A joint effort of ubiquitin, protein deacetylase and actin cytoskeleton. Autophagy 2010, 6, 555-557.
56. Lee, J.Y.; Koga, H.; Kawaguchi, Y.; Tang, W.; Wong, E.; Gao, Y.S.; Pandey, U.B.; Kaushik, S.; Tresse, E.; Lu, J.; et al. HDAC6 controls autophagosome maturation essential for ubiquitin-selective quality-control autophagy. EMBO J. 2010, 29, 969-980.
57. Iwata, A.; Riley, B.E.; Johnston, J.A.; Kopito, R.R. HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem. 2005, 280, 40282-40292.
58. Milani, M.; Rzymski, T.; Mellor, H.R.; Pike, L.; Bottini, A.; Generali, D.; Harris, A.L. The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res. 2009, 69, 4415-4423.
59. True, O.; Matthias, P. Interplay between histone deacetylases and autophagy-From cancer therapy to neurodegeneration. Immunol. Cell Biol. 2011, 90, 78-84.
60. Hohfeld, J.; Cyr, D.M.; Patterson, C. From the cradle to the grave: Molecular chaperones that may choose between folding and degradation. EMBO Rep. 2001, 2, 885-890.
61. Kovacs, J.J.; Murphy, P.J.; Gaillard, S.; Zhao, X.; Wu, J.T.; Nicchitta, C.V.; Yoshida, M.; Toft, D.O.; Pratt, W.B.; Yao, T.P. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell. 2005, 18, 601-607.
62. Murphy, P.J.; Morishima, Y.; Kovacs, J.J.; Yao, T.P.; Pratt, W.B. Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J. Biol. Chem. 2005, 280, 33792-33799.
63. Espallergues, J.; Teegarden, S.L.; Veerakumar, A.; Boulden, J.; Challis, C.; Jochems, J.; Chan, M.; Petersen, T.; Deneris, E.; Matthias, P.; et al. HDAC6 regulates glucocorticoid receptor signaling in serotonin pathways with critical impact on stress resilience. J. Neurosci. 2012, 32, 4400-4416.
64. Ai, J.; Wang, Y.; Dar, J.A.; Liu, J.; Liu, L.; Nelson, J.B.; Wang, Z. HDAC6 regulates androgen receptor hypersensitivity and nuclear localization via modulating Hsp90 acetylation in castration-resistant prostate cancer. Mol. Endocrinol. 2009, 23, 1963-1972.
65. Bali, P.; Pranpat, M.; Bradner, J.; Balasis, M.; Fiskus, W.; Guo, F.; Rocha, K.; Kumaraswamy, S.; Boyapalle, S.; Atadja, P.; et al. 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. J. Biol. Chem. 2005, 280, 26729-26734.
66. Evgrafov, O.V.; Mersiyanova, I.; Irobi, J.; Van Den Bosch, L.; Dierick, I.; Leung, C.L.; Schagina, O.; Verpoorten, N.; van Impe, K.; Fedotov, V.; et al. Mutant small heat-shock protein 27 causes axonal Charcot-Marie-Tooth disease and distal hereditary motor neuropathy. Nat. Genet. 2004, 36, 602-606.
67. Dai, C.; Whitesell, L.; Rogers, A.B.; Lindquist, S. Heat shock factor 1 is a powerful multifaceted modifier of carcinogenesis. Cell 2007, 130, 1005-1018.
68. Valenzuela-Fernandez, A.; Cabrero, J.R.; Serrador, J.M.; Sanchez-Madrid, F. HDAC6: A key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol. 2008, 18, 291-297.
69. Gundersen, G.G.; Bulinski, J.C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc. Natl. Acad. Sci. USA 1988, 85, 5946-5950.
70. Glasgow, J.E.; Daniele, R.P. Role of microtubules in random cell migration: Stabilization of cell polarity. Cell Motil. Cytoskeleton 1994, 27, 88-96.
71. Nogales, E. Structural insights into microtubule function. Annu. Rev. Biochem. 2000, 69, 277-302.
72. Piperno, G.; LeDizet, M.; Chang, X.J. Microtubules containing acetylated alpha-tubulin in mammalian cells in culture. J. Cell Biol. 1987, 104, 289-302.
73. Hubbert, C.; Guardiola, A.; Shao, R.; Kawaguchi, Y.; Ito, A.; Nixon, A.; Yoshida, M.; Wang, X.F.; Yao, T.P. HDAC6 is a microtubule-associated deacetylase. Nature 2002, 417, 455-458.
74. +-dependent tubulin deacetylase. Mol. Cell. 2003, 11, 437-444.
75. Matsuyama, A.; Shimazu, T.; Sumida, Y.; Saito, A.; Yoshimatsu, Y.; Seigneurin-Berny, D.; Osada, H.; Komatsu, Y.; Nishino, N.; Khochbin, S.; et al. In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 2002, 21, 6820-6831.
76. Zhang, Y.; Li, N.; Caron, C.; Matthias, G.; Hess, D.; Khochbin, S.; Matthias, P. HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J. 2003, 22, 1168-1179.
77. Zilberman, Y.; Ballestrem, C.; Carramusa, L.; Mazitschek, R.; Khochbin, S.; Bershadsky, A. Regulation of microtubule dynamics by inhibition of the tubulin deacetylase HDAC6. J. Cell Sci. 2009, 122, 3531-3541.
78. Tran, A.D.; Marmo, T.P.; Salam, A.A.; Che, S.; Finkelstein, E.; Kabarriti, R.; Xenias, H.S.; Mazitschek, R.; Hubbert, C.; Kawaguchi, Y.; et al. HDAC6 deacetylation of tubulin modulates dynamics of cellular adhesions. J. Cell Sci. 2007, 120, 1469-1479.
79. Zhang, Y.; Kwon, S.; Yamaguchi, T.; Cubizolles, F.; Rousseaux, S.; Kneissel, M.; Cao, C.; Li, N.; Cheng, H.L.; Chua, K.; et al. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol. Cell. Biol. 2008, 28, 1688-1701.
80. Destaing, O.; Saltel, F.; Gilquin, B.; Chabadel, A.; Khochbin, S.; Ory, S.; Jurdic, P. A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J. Cell Sci. 2005, 118, 2901-2911.
81. Gao, Y.S.; Hubbert, C.C.; Yao, T.P. The microtubule-associated histone deacetylase 6 (HDAC6) regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation. J. Biol. Chem. 2010, 285, 11219-11226.
82. Reed, N.A.; Cai, D.; Blasius, T.L.; Jih, G.T.; Meyhofer, E.; Gaertig, J.; Verhey, K.J. Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 2006, 16, 2166-2172.
83. Dompierre, J.P.; Godin, J.D.; Charrin, B.C.; Cordelieres, F.P.; King, S.J.; Humbert, S.; Saudou, F. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 2007, 27, 3571-3583.
84. Patel-Hett, S.; Richardson, J.L.; Schulze, H.; Drabek, K.; Isaac, N.A.; Hoffmeister, K.; Shivdasani, R.A.; Bulinski, J.C.; Galjart, N.; Hartwig, J.H.; et al. Visualization of microtubule growth in living platelets reveals a dynamic marginal band with multiple microtubules. Blood 2008, 111, 4605-4616.
85. Luxton, G.W.; Gundersen, G.G. HDAC6-pack: Cortactin acetylation joins the brew. Dev. Cell 2007, 13, 161-162.
86. Wu, H.; Parsons, J.T. Cortactin, an 80/85-kilodalton pp60src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell Biol. 1993, 120, 1417-1426.
87. Bryce, N.S.; Clark, E.S.; Leysath, J.L.; Currie, J.D.; Webb, D.J.; Weaver, A.M. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr. Biol. 2005, 15, 1276-1285.
88. Kaluza, D.; Kroll, J.; Gesierich, S.; Yao, T.P.; Boon, R.A.; Hergenreider, E.; Tjwa, M.; Rossig, L.; Seto, E.; Augustin, H.G.; et al. Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin. EMBO J. 2011, 30, 4142-4156.
89. Zuo, Q.; Wu, W.; Li, X.; Zhao, L.; Chen, W. HDAC6 and SIRT2 promote bladder cancer cell migration and invasion by targeting cortactin. Oncol. Rep. 2012, 27, 819-824.
90. Di Fulvio, S.; Azakir, B.A.; Therrien, C.; Sinnreich, M. Dysferlin interacts with histone deacetylase 6 and increases alpha-tubulin acetylation. PLoS One 2011, 6, e28563.
91. Therrien, C.; di Fulvio, S.; Pickles, S.; Sinnreich, M. Characterization of lipid binding specificities of dysferlin C2 domains reveals novel interactions with phosphoinositides. Biochemistry 2009, 48, 2377-2384.
92. Penela, P.; Lafarga, V.; Tapia, O.; Rivas, V.; Nogues, L.; Lucas, E.; Vila-Bedmar, R.; Murga, C.; Mayor, F., Jr. Roles of GRK2 in cell signaling beyond GPCR desensitization: GRK2-HDAC6 interaction modulates cell spreading and motility. Sci. Signal. 2012, 5, pt3.
93. Lafarga, V.; Aymerich, I.; Tapia, O.; Mayor, F., Jr.; Penela, P. A novel GRK2/HDAC6 interaction modulates cell spreading and motility. EMBO J. 2011, 31, 856-869.
94. Huttenlocher, A.; Palecek, S.P.; Lu, Q.; Zhang, W.; Mellgren, R.L.; Lauffenburger, D.A.; Ginsberg, M.H.; Horwitz, A.F. Regulation of cell migration by the calcium-dependent protease calpain. J. Biol. Chem. 1997, 272, 32719-32722.
95. Gupta, G.P.; Massague, J. Cancer metastasis: Building a framework. Cell 2006, 127, 679-695.
96. Kaverina, I.; Krylyshkina, O.; Small, J.V. Regulation of substrate adhesion dynamics during cell motility. Int. J. Biochem. Cell Biol. 2002, 34, 746-761.
97. Saji, S.; Kawakami, M.; Hayashi, S.; Yoshida, N.; Hirose, M.; Horiguchi, S.; Itoh, A.; Funata, N.; Schreiber, S.L.; Yoshida, M.; et al. Significance of HDAC6 regulation via estrogen signaling for cell motility and prognosis in estrogen receptor-positive breast cancer. Oncogene 2005, 24, 4531-4539.
98. Hurst, D.R.; Mehta, A.; Moore, B.P.; Phadke, P.A.; Meehan, W.J.; Accavitti, M.A.; Shevde, L.A.; Hopper, J.E.; Xie, Y.; Welch, D.R.; et al. Breast cancer metastasis suppressor 1 (BRMS1) is stabilized by the Hsp90 chaperone. Biochem. Biophys. Res. Commun. 2006, 348, 1429-1435.
99. Rey, M.; Irondelle, M.; Waharte, F.; Lizarraga, F.; Chavrier, P. HDAC6 is required for invadopodia activity and invasion by breast tumor cells. Eur. J. Cell Biol. 2011, 90, 128-135.
100. Kanno, K.; Kanno, S.; Nitta, H.; Uesugi, N.; Sugai, T.; Masuda, T.; Wakabayashi, G.; Maesawa, C. Overexpression of histone deacetylase 6 contributes to accelerated migration and invasion activity of hepatocellular carcinoma cells. Oncol. Rep. 2012, 20, 867-873.
101. Sadoul, K.; Wang, J.; Diagouraga, B.; Vitte, A.L.; Buchou, T.; Rossini, T.; Polack, B.; Xi, X.; Matthias, P.; Khochbin, S. HDAC6 controls the kinetics of platelet activation. Blood 2012, 120, 4215-4218.
102. Featherstone, C.; Jackson, S.P. Ku, a DNA repair protein with multiple cellular functions? Mutat. Res. 1999, 434, 3-15.
103. Cohen, H.Y.; Lavu, S.; Bitterman, K.J.; Hekking, B.; Imahiyerobo, T.A.; Miller, C.; Frye, R.; Ploegh, H.; Kessler, B.M.; Sinclair, D.A. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell 2004, 13, 627-638.
104. Subramanian, C.; Jarzembowski, J.A.; Opipari, A.W., Jr.; Castle, V.P.; Kwok, R.P. HDAC6 deacetylates Ku70 and regulates Ku70-Bax binding in neuroblastoma. Neoplasia 2011, 13, 726-734.
105. Kiernan, R.E.; Vanhulle, C.; Schiltz, L.; Adam, E.; Xiao, H.; Maudoux, F.; Calomme, C.; Burny, A.; Nakatani, Y.; Jeang, K.T.; et al. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J. 1999, 18, 6106-6118.
106. Huo, L.; Li, D.; Sun, X.; Shi, X.; Karna, P.; Yang, W.; Liu, M.; Qiao, W.; Aneja, R.; Zhou, J. Regulation of Tat acetylation and transactivation activity by the microtubule-associated deacetylase HDAC6. J. Biol. Chem. 2011, 286, 9280-9286.
107. Poblete Gutierrez, P.; Eggermann, T.; Holler, D.; Jugert, F.K.; Beermann, T.; Grussendorf-Conen, E.I.; Zerres, K.; Merk, H.F.; Frank, J. Phenotype diversity in familial cylindromatosis: A frameshift mutation in the tumor suppressor gene CYLD underlies different tumors of skin appendages. J. Invest. Dermatol. 2002, 119, 527-531.
108. Massoumi, R.; Kuphal, S.; Hellerbrand, C.; Haas, B.; Wild, P.; Spruss, T.; Pfeifer, A.; Fassler, R.; Bosserhoff, A.K. Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J. Exp. Med. 2009, 206, 221-232.
109. Wickstrom, S.A.; Masoumi, K.C.; Khochbin, S.; Fassler, R.; Massoumi, R. CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J. 2009, 29, 131-144.
110. Zhang, W.; Kone, B.C. NF-kappaB inhibits transcription of the H(+)-K(+)-ATPase alpha(2)-subunit gene: Role of histone deacetylases. Am. J. Physiol. Renal. Physiol. 2002, 283, F904-F911.
111. Westendorf, J.J.; Zaidi, S.K.; Cascino, J.E.; Kahler, R.; van Wijnen, A.J.; Lian, J.B.; Yoshida, M.; Stein, G.S.; Li, X. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol. Cell. Biol. 2002, 22, 7982-7992.
112. Wood, Z.A.; Poole, L.B.; Karplus, P.A. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 2003, 300, 650-653.
113. Parmigiani, R.B.; Xu, W.S.; Venta-Perez, G.; Erdjument-Bromage, H.; Yaneva, M.; Tempst, P.; Marks, P.A. HDAC6 is a specific deacetylase of peroxiredoxins and is involved in redox regulation. Proc. Natl. Acad. Sci. USA 2008, 105, 9633-9638.
114. Fernandes, I.; Bastien, Y.; Wai, T.; Nygard, K.; Lin, R.; Cormier, O.; Lee, H.S.; Eng, F.; Bertos, N.R.; Pelletier, N.; et al. Ligand-dependent nuclear receptor corepressor LCoR functions by histone deacetylase-dependent and -independent mechanisms. Mol. Cell 2003, 11, 139-150.
115. Palijan, A.; Fernandes, I.; Bastien, Y.; Tang, L.; Verway, M.; Kourelis, M.; Tavera-Mendoza, L.E.; Li, Z.; Bourdeau, V.; Mader, S.; et al. Function of histone deacetylase 6 as a cofactor of nuclear receptor coregulator LCoR. J. Biol. Chem. 2009, 284, 30264-30274.
116. Pugacheva, E.N.; Jablonski, S.A.; Hartman, T.R.; Henske, E.P.; Golemis, E.A. HEF1-dependent Aurora A activation induces disassembly of the primary cilium. Cell 2007, 129, 1351-1363.
117. Li, Y.; Zhang, X.; Polakiewicz, R.D.; Yao, T.P.; Comb, M.J. HDAC6 is required for epidermal growth factor-induced beta-catenin nuclear localization. J. Biol. Chem. 2008, 283, 12686-12690.
118. Zhu, J.; Coyne, C.B.; Sarkar, S.N. PKC alpha regulates Sendai virus-mediated interferon induction through HDAC6 and beta-catenin. EMBO J. 2011, 30, 4838-4849.
119. Han, Y.; Jeong, H.M.; Jin, Y.H.; Kim, Y.J.; Jeong, H.G.; Yeo, C.Y.; Lee, K.Y. Acetylation of histone deacetylase 6 by p300 attenuates its deacetylase activity. Biochem. Biophys. Res. Commun. 2009, 383, 88-92.
120. Liu, Y.; Peng, L.; Seto, E.; Huang, S.; Qiu, Y. Modulation of histone deacetylase 6 (HDAC6) nuclear import and tubulin deacetylase activity through acetylation. J. Biol. Chem. 2012, 287, 29168-29174.
121. Chen, S.; Owens, G.C.; Makarenkova, H.; Edelman, D.B. HDAC6 regulates mitochondrial transport in hippocampal neurons. PLoS One 2010, 5, e10848.
122. d'Ydewalle, C.; Krishnan, J.; Chiheb, D.M.; van Damme, P.; Irobi, J.; Kozikowski, A.P.; Berghe, P.V.; Timmerman, V.; Robberecht, W.; van den Bosch, L. HDAC6 inhibitors reverse axonal loss in a mouse model of mutant HSPB1-induced Charcot-Marie-Tooth disease. Nat. Med. 2011, 17, 968-974.
123. Finnin, M.S.; Donigian, J.R.; Cohen, A.; Richon, V.M.; Rifkind, R.A.; Marks, P.A.; Breslow, R.; Pavletich, N.P. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 1999, 401, 188-193.
124. Haggarty, S.J.; Koeller, K.M.; Wong, J.C.; Grozinger, C.M.; Schreiber, S.L. Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. USA 2003, 100, 4389-4394.
125. Haggarty, S.J.; Koeller, K.M.; Wong, J.C.; Butcher, R.A.; Schreiber, S.L. Multidimensional chemical genetic analysis of diversity-oriented synthesis-derived deacetylase inhibitors using cell-based assays. Chem. Biol. 2003, 10, 383-396.
126. Somoza, J.R.; Skene, R.J.; Katz, B.A.; Mol, C.; Ho, J.D.; Jennings, A.J.; Luong, C.; Arvai, A.; Buggy, J.J.; Chi, E.; et al. Structural snapshots of human HDAC8 provide insights into the class I histone deacetylases. Structure 2004, 12, 1325-1334.
127. Hideshima, T.; Bradner, J.E.; Wong, J.; Chauhan, D.; Richardson, P.; Schreiber, S.L.; Anderson, K.C. Small-molecule inhibition of proteasome and aggresome function induces synergistic antitumor activity in multiple myeloma. Proc. Natl. Acad. Sci. USA 2005, 102, 8567-8572.
128. Nawrocki, S.T.; Carew, J.S.; Pino, M.S.; Highshaw, R.A.; Andtbacka, R.H.; Dunner, K., Jr.; Pal, A.; Bornmann, W.G.; Chiao, P.J.; Huang, P.; et al. Aggresome disruption: A novel strategy to enhance bortezomib-induced apoptosis in pancreatic cancer cells. Cancer Res. 2006, 66, 3773-3781.
129. Nahhas, F.; Dryden, S.C.; Abrams, J.; Tainsky, M.A. Mutations in SIRT2 deacetylase which regulate enzymatic activity but not its interaction with HDAC6 and tubulin. Mol. Cell Biochem. 2007, 303, 221-230.
130. Butler, K.V.; Kozikowski, A.P. Chemical origins of isoform selectivity in histone deacetylase inhibitors. Curr. Pharm. Des. 2008, 14, 505-528.
131. Itoh, Y.; Suzuki, T.; Kouketsu, A.; Suzuki, N.; Maeda, S.; Yoshida, M.; Nakagawa, H.; Miyata, N. Design, synthesis, structure-Selectivity relationship, and effect on human cancer cells of a novel series of histone deacetylase 6-selective inhibitors. J. Med. Chem. 2007, 50, 5425-5438.
132. Kozikowski, A.P.; Chen, Y.; Gaysin, A.M.; Savoy, D.N.; Billadeau, D.D.; Kim, K.H. Chemistry, biology, and QSAR studies of substituted biaryl hydroxamates and mercaptoacetamides as HDAC inhibitors-nanomolar-potency inhibitors of pancreatic cancer cell growth. ChemMedChem 2008, 3, 487-501.
133. Chen, Y.; Lopez-Sanchez, M.; Savoy, D.N.; Billadeau, D.D.; Dow, G.S.; Kozikowski, A.P. A series of potent and selective, triazolylphenyl-based histone deacetylases inhibitors with activity against pancreatic cancer cells and Plasmodium falciparum. J. Med. Chem. 2008, 51, 3437-3448.
134. Kozikowski, A.P.; Tapadar, S.; Luchini, D.N.; Kim, K.H.; Billadeau, D.D. Use of the nitrile oxide cycloaddition (NOC) reaction for molecular probe generation: A new class of enzyme selective histone deacetylase inhibitors (HDACIs) showing picomolar activity at HDAC6. J. Med. Chem. 2008, 51, 4370-4373.
135. Nawrocki, S.T.; Carew, J.S.; Maclean, K.H.; Courage, J.F.; Huang, P.; Houghton, J.A.; Cleveland, J.L.; Giles, F.J.; McConkey, D.J. Myc regulates aggresome formation, the induction of Noxa, and apoptosis in response to the combination of bortezomib and SAHA. Blood 2008, 112, 2917-2926.
136. Bazzaro, M.; Lin, Z.; Santillan, A.; Lee, M.K.; Wang, M.C.; Chan, K.C.; Bristow, R.E.; Mazitschek, R.; Bradner, J.; Roden, R.B. Ubiquitin proteasome system stress underlies synergistic killing of ovarian cancer cells by bortezomib and a novel HDAC6 inhibitor. Clin. Cancer Res. 2008, 14, 7340-7347.
137. Schafer, S.; Saunders, L.; Schlimme, S.; Valkov, V.; Wagner, J.M.; Kratz, F.; Sippl, W.; Verdin, E.; Jung, M. Pyridylalanine-containing hydroxamic acids as selective HDAC6 inhibitors. ChemMedChem 2009, 4, 283-290.
138. Smil, D.V.; Manku, S.; Chantigny, Y.A.; Leit, S.; Wahhab, A.; Yan, T.P.; Fournel, M.; Maroun, C.; Li, Z.; Lemieux, A.M.; et al. Novel HDAC6 isoform selective chiral small molecule histone deacetylase inhibitors. Bioorg. Med. Chem. Lett. 2009, 19, 688-692.
139. Witt, O.; Deubzer, H.E.; Milde, T.; Oehme, I. HDAC family: What are the cancer relevant targets? Cancer Lett. 2009, 277, 8-21.
140. Dallavalle, S.; Cincinelli, R.; Nannei, R.; Merlini, L.; Morini, G.; Penco, S.; Pisano, C.; Vesci, L.; Barbarino, M.; Zuco, V.; et al. Design, synthesis, and evaluation of biphenyl-4-yl-acrylohydroxamic acid derivatives as histone deacetylase (HDAC) inhibitors. Eur. J. Med. Chem. 2009, 44, 1900-1912.
141. Olsen, C.A.; Ghadiri, M.R. Discovery of potent and selective histone deacetylase inhibitors via focused combinatorial libraries of cyclic alpha3beta-tetrapeptides. J. Med. Chem. 2009, 52, 7836-7846.
142. Auzzas, L.; Larsson, A.; Matera, R.; Baraldi, A.; Deschenes-Simard, B.; Giannini, G.; Cabri, W.; Battistuzzi, G.; Gallo, G.; Ciacci, A.; et al. Non-natural macrocyclic inhibitors of histone deacetylases: Design, synthesis, and activity. J. Med. Chem. 2010, 53, 8387-8399.
143. Inks, E.S.; Josey, B.J.; Jesinkey, S.R.; Chou, C.J. A novel class of small molecule inhibitors of HDAC6. ACS Chem. Biol. 2011, 7, 331-339.
144. Dallavalle, S.; Pisano, C.; Zunino, F. Development and therapeutic impact of HDAC6-selective inhibitors. Biochem. Pharmacol. 2012, 84, 756-765.
145. Carew, J.S.; Giles, F.J.; Nawrocki, S.T. Histone deacetylase inhibitors: Mechanisms of cell death and promise in combination cancer therapy. Cancer Lett. 2008, 269, 7-17.
146. Arts, J.; Angibaud, P.; Marien, A.; Floren, W.; Janssens, B.; King, P.; van Dun, J.; Janssen, L.; Geerts, T.; Tuman, R.W.; et al. R306465 is a novel potent inhibitor of class I histone deacetylases with broad-spectrum antitumoral activity against solid and haematological malignancies. Br. J. Cancer 2007, 97, 1344-1353.
147. Angelucci, A.; Mari, M.; Millimaggi, D.; Giusti, I.; Carta, G.; Bologna, M.; Dolo, V. Suberoylanilide hydroxamic acid partly reverses resistance to paclitaxel in human ovarian cancer cell lines. Gynecol. Oncol. 2010, 119, 557-563.
148. Zhu, Q.Y.; Wang, Z.; Ji, C.; Cheng, L.; Yang, Y.L.; Ren, J.; Jin, Y.H.; Wang, Q.J.; Gu, X.J.; Bi, Z.G.; et al. C6-ceramide synergistically potentiates the anti-tumor effects of histone deacetylase inhibitors via AKT dephosphorylation and alpha-tubulin hyperacetylation both in vitro and in vivo. Cell Death Dis. 2011, 2, 10.1038/cddis.2010.96.
149. Wang, C.; Henkes, L.M.; Doughty, L.B.; He, M.; Wang, D.; Meyer-Almes, F.J.; Cheng, Y.Q. Thailandepsins: Bacterial products with potent histone deacetylase inhibitory activities and broad-spectrum antiproliferative activities. J. Nat. Prod. 2011, 74, 2031-2038.
150. Ketene, A.N.; Roberts, P.C.; Shea, A.A.; Schmelz, E.M.; Agah, M. Actin filaments play a primary role for structural integrity and viscoelastic response in cells. Integr. Biol. (Camb.) 2012, 4, 540-549.
151. Wilson, A.J.; Cheng, Y.Q.; Khabele, D. Thailandepsins are new small molecule class I HDAC inhibitors with potent cytotoxic activity in ovarian cancer cells: A preclinical study of epigenetic ovarian cancer therapy. J. Ovarian Res. 2012, 5, 1-7.
152. Li, Y.; Shin, D.; Kwon, S.H. Histone deacetylase 6 plays a role as a distinct regulator of diverse cellular processes. FEBS J. 2013, 280, 775-793.