HDAC6: A Novel Histone Deacetylase Implicated in Pulmonary Arterial Hypertension

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Boucherat, Olivier ^a   Chabot, Sophie ^a   Paulin, Roxane ^a   Trinh, Isabelle ^a   Bourgeois, Alice ^a   Potus, François ^a   Lampron, Marie Claude ^a   Lambert, Caroline ^a   Breuils Bonnet, Sandra ^a   Nadeau, Valérie ^a   Paradis, Renée ^a   Goncharova, Elena A ^b   Provencher, Steeve ^a   Bonnet, Sébastien ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HDAC6 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 90; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; KU ANTIGEN; PROTEIN BAX;

ACETYLATION; ANIMAL; APOPTOSIS; BIOLOGICAL MODEL; CELL LINE; CELL MOTION; CELL PROLIFERATION; DISEASE MODEL; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PULMONARY HYPERTENSION; RAT; SMOOTH MUSCLE CELL;

ACETYLATION; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITORS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYPERTENSION, PULMONARY; IMMUNOHISTOCHEMISTRY; KU AUTOANTIGEN; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MYOCYTES, SMOOTH MUSCLE; RATS;

EID: 85021749244     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-04874-4     Document Type: Article

References (57)

1. Leopold, J. A. & Maron, B. A. Molecular Mechanisms of Pulmonary Vascular Remodeling in Pulmonary Arterial Hypertension. Int J Mol Sci 17, doi: 10.3390/ijms17050761 (2016).
2. Lajoie, A. C. et al. Combination therapy versus monotherapy for pulmonary arterial hypertension: a meta-analysis. The Lancet. Respiratory medicine 4, 291-305, doi: 10.1016/s2213-2600(16)00027-8 (2016).
3. Bonnet, S. et al. Translating Research into Improved Patient Care in Pulmonary Arterial Hypertension. Am J Respir Crit Care Med, doi: 10.1164/rccm.201607-1515PP (2016).
4. Pullamsetti, S. S., Savai, R., Seeger, W. & Goncharova, E. A. From Cancer Biology to New PAH Therapeutics: Targeting Cell Growth and Proliferation Signaling Hubs. American Journal of Respiratory and Critical Care Medicine, doi: 10.1164/rccm.201606-1226PP (2016).
5. Meloche, J. et al. Bromodomain-Containing Protein 4: The Epigenetic Origin of Pulmonary Arterial Hypertension. Circ Res 117, 525-535, doi: 10.1161/CIRCRESAHA.115.307004 (2015).
6. Paulin, R. et al. Signal transducers and activators of transcription-3/pim1 axis plays a critical role in the pathogenesis of human pulmonary arterial hypertension. Circulation 123, 1205-1215, doi: 10.1161/CIRCULATIONAHA.110.963314 (2011).
7. McMurtry, M. S. et al. Gene therapy targeting survivin selectively induces pulmonary vascular apoptosis and reverses pulmonary arterial hypertension. J Clin Invest 115, 1479-1491, doi: 10.1172/JCI23203 (2005).
8. Meloche, J. et al. Role for DNA damage signaling in pulmonary arterial hypertension. Circulation 129, 786-797, doi: 10.1161/CIRCULATIONAHA.113.006167 (2014).
9. Ranchoux, B. et al. DNA Damage and Pulmonary Hypertension. International Journal of Molecular Sciences 17, 990, doi: 10.3390/ijms17060990 (2016).
10. Meloche, J. et al. miR-223 reverses experimental pulmonary arterial hypertension. American journal of physiology. Cell physiology 309, C363-372, doi: 10.1152/ajpcell.00149.2015 (2015).
11. Bonnet, S. et al. An abnormal mitochondrial-hypoxia inducible factor-1alpha-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: similarities to human pulmonary arterial hypertension. Circulation 113, 2630-2641, doi: 10.1161/CIRCULATIONAHA.105.609008 (2006).
12. Dromparis, P. et al. Uncoupling protein 2 deficiency mimics the effects of hypoxia and endoplasmic reticulum stress on mitochondria and triggers pseudohypoxic pulmonary vascular remodeling and pulmonary hypertension. Circ Res 113, 126-136, doi: 10.1161/circresaha.112.300699 (2013).
13. Wang, G. K. et al. Inhibition of heat shock protein 90 improves pulmonary arteriole remodeling in pulmonary arterial hypertension. Oncotarget, doi: 10.18632/oncotarget.10855 (2016).
14. Long, L. et al. Chloroquine prevents progression of experimental pulmonary hypertension via inhibition of autophagy and lysosomal bone morphogenetic protein type II receptor degradation. Circ Res 112, 1159-1170, doi: 10.1161/circresaha.111.300483 (2013).
15. Matthias, P., Yoshida, M. & Khochbin, S. HDAC6 a new cellular stress surveillance factor. Cell Cycle 7, 7-10, doi: 10.4161/cc.7.1.5186 (2008).
16. 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 13, 726-734 (2011).
17. Boyault, C. et al. HDAC6 controls major cell response pathways to cytotoxic accumulation of protein aggregates. Genes & development 21, 2172-2181, doi: 10.1101/gad.436407 (2007).
18. Hubbert, C. et al. HDAC6 is a microtubule-associated deacetylase. Nature 417, 455-458, doi: 10.1038/417455a (2002).
19. Ding, G. et al. HDAC6 promotes hepatocellular carcinoma progression by inhibiting P53 transcriptional activity. FEBS letters 587, 880-886, doi: 10.1016/j.febslet.2013.02.001 (2013).
20. Wang, Z. et al. HDAC6 promotes cell proliferation and confers resistance to temozolomide in glioblastoma. Cancer letters 379, 134-142, doi: 10.1016/j.canlet.2016.06.001 (2016).
21. 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 100, 4389-4394, doi: 10.1073/pnas.0430973100 (2003).
22. Rao, R. et al. HDAC6 inhibition enhances 17-AAG-mediated abrogation of hsp90 chaperone function in human leukemia cells. Blood 112, 1886-1893, doi: 10.1182/blood-2008-03-143644 (2008).
23. Hassoun, P. M. et al. Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol 54, S10-19, doi: 10.1016/j.jacc.2009.04.006 (2009).
24. Namdar, M., Perez, G., Ngo, L. & Marks, P. A. Selective inhibition of histone deacetylase 6 (HDAC6) induces DNA damage and sensitizes transformed cells to anticancer agents. Proc Natl Acad Sci USA 107, 20003-20008, doi: 10.1073/pnas.1013754107 (2010).
25. Chaudhary, N. et al. SMAR1 coordinates HDAC6-induced deacetylation of Ku70 and dictates cell fate upon irradiation. Cell death & disease 5, e1447, doi: 10.1038/cddis.2014.397 (2014).
26. Chen, C.-S. et al. Histone Deacetylase Inhibitors Sensitize Prostate Cancer Cells to Agents that Produce DNA Double-Strand Breaks by Targeting Ku70 Acetylation. Cancer Research 67, 5318-5327, doi: 10.1158/0008-5472.can-06-3996 (2007).
27. Iwata, A., Riley, B. E., Johnston, J. A. & Kopito, R. R. HDAC6 and Microtubules Are Required for Autophagic Degradation of Aggregated Huntingtin. Journal of Biological Chemistry 280, 40282-40292, doi: 10.1074/jbc.M508786200 (2005).
28. Kawaguchi, Y. et al. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress. Cell 115, 727-738 (2003).
29. McLendon, P. M. et al. Tubulin hyperacetylation is adaptive in cardiac proteotoxicity by promoting autophagy. Proceedings of the National Academy of Sciences 111, E5178-E5186, doi: 10.1073/pnas.1415589111 (2014).
30. Trepel, J., Mollapour, M., Giaccone, G. & Neckers, L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 10, 537-549 (2010).
31. Jochems, J. et al. Antidepressant-Like Properties of Novel HDAC6-Selective Inhibitors with Improved Brain Bioavailability. Neuropsychopharmacology 39, 389-400, doi: 10.1038/npp.2013.207 (2014).
32. Butler, K. V. et al. Rational Design and Simple Chemistry Yield a Superior, Neuroprotective HDAC6 Inhibitor, Tubastatin A. Journal of the American Chemical Society 132, 10842-10846, doi: 10.1021/ja102758v (2010).
33. Sawada, M. et al. Ku70 suppresses the apoptotic translocation of Bax to mitochondria. Nat Cell Biol 5, 320-329, doi: 10.1038/ncb950 (2003).
34. Cohen, H. Y. et al. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Molecular cell 13, 627-638 (2004).
35. Gomez, J. A. et al. Bax-inhibiting peptides derived from Ku70 and cell-penetrating pentapeptides. Biochemical Society transactions 35, 797-801, doi: 10.1042/bst0350797 (2007).
36. Falkenberg, K. J. & Johnstone, R. W. Histone deacetylases and their inhibitors in cancer, neurological diseases and immune disorders. Nat Rev Drug Discov 13, 673-691, doi: 10.1038/nrd4360 (2014).
37. Cavasin, M. A. et al. Selective Class I HDAC Inhibition Suppresses Hypoxia-Induced Cardiopulmonary Remodeling Through an Anti-Proliferative Mechanism. Circulation research 110, 739-748, doi: 10.1161/CIRCRESAHA.111.258426 (2012).
38. Zhao, L. et al. Histone deacetylation inhibition in pulmonary hypertension: therapeutic potential of valproic acid (VPA) and suberoylanilide hydroxamic acid (SAHA). Circulation 126, 455-467, doi: 10.1161/CIRCULATIONAHA.112.103176 (2012).
39. De Raaf, M. A. et al. Histone deacetylase inhibition with trichostatin A does not reverse severe angioproliferative pulmonary hypertension in rats (2013 Grover Conference series). Pulmonary Circulation 4, 237-243, doi: 10.1086/675986 (2014).
40. Bogaard, H. J. et al. Suppression of histone deacetylases worsens right ventricular dysfunction after pulmonary artery banding in rats. Am J Respir Crit Care Med 183, 1402-1410, doi: 10.1164/rccm.201007-1106OC (2011).
41. Zhang, Y. et al. Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol Cell Biol 28, 1688-1701, doi: 10.1128/mcb.01154-06 (2008).
42. Tao, H., Yang, J. J., Hu, W., Shi, K. H. & Li, J. HDAC6 Promotes Cardiac Fibrosis Progression through Suppressing RASSF1A Expression. Cardiology 133, 18-26, doi: 10.1159/000438781 (2016).
43. Demos-Davies, K. M. et al. HDAC6 contributes to pathological responses of heart and skeletal muscle to chronic angiotensin-II signaling. American journal of physiology. Heart and circulatory physiology 307, H252-258, doi: 10.1152/ajpheart.00149.2014 (2014).
44. Chen, C. S. et al. Histone deacetylase inhibitors sensitize prostate cancer cells to agents that produce DNA double-strand breaks by targeting Ku70 acetylation. Cancer Res 67, 5318-5327, doi: 10.1158/0008-5472.can-06-3996 (2007).
45. Ngo, J. et al. Bax deficiency extends the survival of Ku70 knockout mice that develop lung and heart diseases. Cell death & disease 6, e1706, doi: 10.1038/cddis.2015.11 (2015).
46. Li, M. et al. Loss of bone morphogenetic protein receptor 2 is associated with abnormal DNA repair in pulmonary arterial hypertension. American journal of respiratory cell and molecular biology 50, 1118-1128, doi: 10.1165/rcmb.2013-0349OC (2014).
47. Lee, S.-J. et al. Autophagic Protein LC3B Confers Resistance against Hypoxia-induced Pulmonary Hypertension. American Journal of Respiratory and Critical Care Medicine 183, 649-658, doi: 10.1164/rccm.201005-0746OC (2011).
48. Dalby, K. N., Tekedereli, I., Lopez-Berestein, G. & Ozpolat, B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy 6, 322-329 (2010).
49. Kovacs, J. J. et al. HDAC6 Regulates Hsp90 Acetylation and Chaperone-Dependent Activation of Glucocorticoid Receptor. Molecular cell 18, 601-607, doi: 10.1016/j.molcel.2005.04.021.
50. Riolo, M. T. et al. Histone deacetylase 6 (HDAC6) deacetylates survivin for its nuclear export in breast cancer. J Biol Chem 287, 10885-10893, doi: 10.1074/jbc.M111.308791 (2012).
51. Courboulin, A. et al. Krüppel-like Factor 5 contributes to pulmonary artery smooth muscle proliferation and resistance to apoptosis in human pulmonary arterial hypertension. Respiratory Research 12, 128, doi: 10.1186/1465-9921-12-128 (2011).
52. Mizuno, K. et al. Regulation of Pim-1 by Hsp90. Biochemical and biophysical research communications 281, 663-669, doi: 10.1006/bbrc.2001.4405 (2001).
53. Kim, H. L., Cassone, M., Otvos, L. Jr. & Vogiatzi, P. HIF-1alpha and STAT3 client proteins interacting with the cancer chaperone Hsp90: therapeutic considerations. Cancer biology & therapy 7, 10-14 (2008).
54. Inks, E. S., Josey, B. J., Jesinkey, S. R. & Chou, C. J. A Novel Class of Small Molecule Inhibitors of HDAC6. ACS Chemical Biology 7, 331-339, doi: 10.1021/cb200134p (2012).
55. Courboulin, A. et al. Plumbagin reverses proliferation and resistance to apoptosis in experimental PAH. The European respiratory journal 40, 618-629, doi: 10.1183/09031936.00084211 (2012).
56. Ruffenach, G. et al. Role for RUNX2 in Proliferative and Calcified Vascular Lesions in Pulmonary Arterial Hypertension. Am J Respir Crit Care Med, doi: 10.1164/rccm.201512-2380OC (2016).
57. Dean, A., Nilsen, M., Loughlin, L., Salt, I. P. & MacLean, M. R. Metformin Reverses Development of Pulmonary Hypertension via Aromatase Inhibition. Hypertension (Dallas, Tex.: 1979) 68, 446-454, doi: 10.1161/HYPERTENSIONAHA.116.07353 (2016).