Reduced histone deacetylase 7 activity restores function to misfolded CFTR in cystic fibrosis

Nature Chemical Biology

Volumn 6, Issue 1, 2010, Pages 25-33

  Hutt, Darren M ^a   Herman, David ^a   Rodrigues, Ana P C ^b   Noel, Sabrina ^c   Pilewski, Joseph M ^c   Matteson, Jeanne ^a   Hoch, Ben ^a   Kellner, Wendy ^a   Kelly, Jeffery W ^a,d   Schmidt, Andre ^e   Thomas, Philip J ^e   Matsumura, Yoshihiro ^f   Skach, William R ^f   Gentzsch, Martina ^g   Riordan, John R ^h   Sorscher, Eric J ⁱ   Okiyoneda, Tsukasa ^j   Yates, John R ^a   Lukacs, Gergely L ^j   Frizzell, Raymond A ^c   Manning, Gerard ^b   Gottesfeld, Joel M ^a   Balch, William E ^a   more..

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d Department of Chemistry ^*  (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^g UNIVERSITY OF NORTH CAROLINA   (United States)

^h UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^j MCGILL UNIVERSITY   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

6 (1,3 DIOXO 1H,3H BENZO[DE]ISOQUINOLIN 2 YL) N HYDROXYHEXANAMIDE; CHLORIDE CHANNEL; ENTINOSTAT; HISTONE DEACETYLASE 7; TRANSMEMBRANE CONDUCTANCE REGULATOR; TRICHOSTATIN A; VORINOSTAT; CFTR PROTEIN, HUMAN; HDAC7 PROTEIN, HUMAN; HISTONE DEACETYLASE; HYDROXAMIC ACID; SMALL INTERFERING RNA;

ARTICLE; CELL CULTURE; CELL SURFACE; CYSTIC FIBROSIS; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; GENE MUTATION; GENE SILENCING; IMMUNOBLOTTING; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TRANSPORT; RESPIRATORY EPITHELIUM; ANIMAL; BRONCHUS; CELL MEMBRANE; CHEMISTRY; EPITHELIUM CELL; HAMSTER; HUMAN; METABOLISM; MUTATION; PROTEIN DENATURATION;

ANIMALS; BRONCHI; CELL MEMBRANE; CRICETINAE; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; EPITHELIAL CELLS; GENE SILENCING; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; MUTATION; PROTEIN DENATURATION; PROTEIN FOLDING;

EID: 77950428804     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.275     Document Type: Article

References (50)

1. Riordan, J.R. CFTR function and prospects for therapy. Annu. Rev. Biochem. 77, 701-726 (2008).
2. Qu, B.H., Strickland, E.H. & Tomas, P.J. Localization and suppression of a kinetic defect in cystic fbrosis transmembrane conductance regulator folding. J. Biol. Chem. 272, 15739-15744 (1997). (Pubitemid 27265548)
3. Boucher, R.C. Evidence for airway surface dehydration as the initiating event in CF airway disease. J. Intern. Med. 261, 5-16 (2007). (Pubitemid 46046468)
4. Balch, W.E., Morimoto, R.I., Dillin, A. & Kelly, J.W. Adapting proteostasis for disease intervention. Science 319, 916-919 (2008). (Pubitemid 351263754)
5. Powers, E.T., Morimoto, R.I., Dillin, A., Kelly, J.W. & Balch, W.E. Biological and chemical approaches to diseases of proteostasis defciency Annu. Rev. Biochem. 78, 959-991 (2009).
6. Hutt, D.M., Powers, E.T. & Balch, W.E. Te proteostasis boundary in misfolding diseases of membrane trafc. FEBS Lett. 583, 2639-2646 (2009).
7. Gregersen, N. Protein misfolding disorders: pathogenesis and intervention. J. Inherit Metab. Dis. 29, 456-470 (2006). (Pubitemid 43880651)
8. Marks, PA. & Breslow, R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 25, 84-90 (2007). (Pubitemid 46087907)
9. Haberland, M., Montgomery R.L. & Olson, E.N. Te many roles of histone deacetylases in development and physiology: implications for disease and therapy Nat Rev. Genet. 10, 32-42 (2009).
10. Scroggins, B.T. et al An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol. Cell 25, 151-159 (2007). (Pubitemid 46049066)
11. Ozcan, U. et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140 (2006). (Pubitemid 44300242)
12. Adcock, I.M., Tsaprouni, L., Bhavsar, P. & Ito, K. Epigenetic regulation of airway infammation. Curr. Opin. Immunol. 19, 694-700 (2007).
13. Lin, H.S. et al. Anti-rheumatic activities of histone deacetylase (HDAC) inhibitors in vivo in collagen-induced arthritis in rodents. Br. J. Pharmacol. 150, 862-872 (2007).
14. Westerheide, S.D., Anckar, J., Stevens, S.M. Jr., Sistonen, L. & Morimoto, R.I. Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323, 1063-1066 (2009).
15. Fischle, W. et al Human HDAC7 histone deacetylase activity is associated with HDAC3 in vivo. J. Biol. Chem. 276, 35826-35835 (2001).
16. Wang, X. et al Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fbrosis. Cell 127, 803-815 (2006). (Pubitemid 44716255)
17. Kovacs, J.J. et al. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18, 601-607 (2005). (Pubitemid 40726236)
18. Bebok, Z. et al. Failure of cAMP agonists to activate rescued deltaF508 CFTR in CFBE41o-airway epithelial monolayers. J. Physiol. (Lond.) 569, 601-615 (2005). (Pubitemid 41830125)
19. Lukacs, G.L. et al Conformational maturation of CFTR but not its mutant counterpart (delta F508) occurs in the endoplasmic reticulum and requires ATP. EMBO J. 13, 6076-6086 (1994).
20. Gentzsch, M. et al Endocytic trafcking routes of wild type and DeltaF508 cystic fbrosis transmembrane conductance regulator. Mol. Biol. Cell 15, 2684-2696 (2004). (Pubitemid 38691858)
21. Lahm, A. et al. Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl. Acad. Sci. USA 104, 17335-17340 (2007). (Pubitemid 350219843)
22. Marks, P.A. & Dokmanovic, M. Histone deacetylase inhibitors: discovery and development as anticancer agents. Expert Opin. Investig. Drugs 14, 1497-1511 (2005). (Pubitemid 41749195)
23. Blander, G. & Guarente, L. Te Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73, 417-435 (2004).
24. Milne, J.C. & Denu, J.M. Te Sirtuin family: therapeutic targets to treat diseases of aging. Curr. Opin. Chem. Biol. 12, 11-17 (2008).
25. Caci, E. et al. Evidence for direct CFTR inhibition by CFTR(inh)-172 based on Arg347 mutagenesis. Biochem. J. 413, 135-142 (2008). (Pubitemid 351946869)
26. Ekins, S., Nikolsky, Y., Bugrim, A., Kirillov, E. & Nikolskaya, T. Pathway mapping tools for analysis of high content data. Methods Mol. Biol. 356, 319-350 (2007).
27. Sun, F. et al. Derlin-1 promotes the efcient degradation of cystic fbrosis transmembrane conductance regulator (CFTR) and CFTR folding mutants. J. Biol. Chem. 281, 36856-36863 (2006). (Pubitemid 46042153)
28. Wang, X., Koulov, A.V., Kellner, W.A., Riordan, J.R. & Balch, W.E. Chemical and biological folding contribute to temperature-sensitive DeltaF508 CFTR trafcking. Trafc 9, 1878-1893 (2008).
29. Wang, X. et al COPII-dependent export of cystic fbrosis transmembrane conductance regulator from the ER uses a di-acidic exit code. J. Cell Biol. 167, 65-74 (2004). (Pubitemid 39363415)
30. Wiseman, R.L., Powers, E.T., Buxbaum, J.N., Kelly, J.W. & Balch, W.E. An adaptable standard for protein export from the endoplasmic reticulum. Cell 131, 809-821 (2007). (Pubitemid 350087203)
31. Guggino, W.B. & Stanton, B.A. New insights into cystic fbrosis: molecular switches that regulate CFTR. Nat Rev. Mol. Cell Biol. 7, 426-436 (2006). (Pubitemid 44050096)
32. Dokmanovic, M. et al. Histone deacetylase inhibitors selectively suppress expression of HDAC7. Mol. Cancer Ter. 6, 2525-2534 (2007). (Pubitemid 47480418)
33. Chang, S. et al. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126, 321-334 (2006). (Pubitemid 44092958)
34. Kasler, H.G. & Verdin, E. Histone deacetylase 7 functions as a key regulator of genes involved in both positive and negative selection of thymocytes. Mol. Cell. Biol. 27, 5184-5200 (2007). (Pubitemid 47068292)
35. Amaral, M.D. Processing of CFTR: traversing the cellular maze-how much CFTR needs to go through to avoid cystic fbrosis? Pediatr. Pulmonol. 39, 479-491 (2005). (Pubitemid 40696318)
36. Yoo, J.S. et al. Non-conventional trafcking of the cystic fbrosis transmembrane conductance regulator through the early secretory pathway J. Biol. Chem. 277, 11401-11409 (2002).
37. Mai, A. Te therapeutic uses of chromatin-modifying agents. Expert Opin. Ter. Targets 11, 835-851 (2007).
38. Herman, D. et al Histone deacetylase inhibitors reverse gene silencing in Friedreich's ataxia. Nat. Chem. Biol. 2, 551-558 (2006). (Pubitemid 44413238)
39. Mai, A. et al. Identifcation of two new synthetic histone deacetylase inhibitors that modulate globin gene expression in erythroid cells from healthy donors and patients with thalassemia. Mol. Pharmacol. 72, 1111-1123 (2007). (Pubitemid 350012585)
40. Westphal, C.H., Dipp, M.A. & Guarente, L. A therapeutic role for sirtuins in diseases of aging? Trends Biochem. Sci. 32, 555-560 (2007). (Pubitemid 350123051)
41. Bates, E.A., Victor, M., Jones, A.K., Shi, Y. & Hart, A.C. Diferential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity. J. Neurosci. 26, 2830-2838 (2006). (Pubitemid 43357867)
42. Rubenstein, R.C., Egan, M.E. & Zeitlin, P.L. In vitro pharmacologic restoration of CFTR-mediated chloride transport with sodium 4-phenylbutyrate in cystic fbrosis epithelial cells containing delta F508-CFTR. J. Clin. Invest. 100, 2457-2465 (1997). (Pubitemid 27514885)
43. Singh, O.V. et al Pharmacoproteomics of 4-phenylbutyrate-treated IB3-1 cystic fbrosis bronchial epithelial cells. J. Proteome Res. 5, 562-571 (2006). (Pubitemid 43364096)
44. Rubenstein, R.C. & Zeitlin, P.L. A pilot clinical trial of oral sodium 4-phenylbutyrate (Buphenyl) in deltaF508-homozygous cystic fbrosis patients: partial restoration of nasal epithelial CFTR function. Am. J. Respir. Crit Care Med. 157, 484-490 (1998). (Pubitemid 28090539)
45. Mroz, R.M., Noparlik, J., Chyczewska, E., Braszko, J.J. & Holownia, A. Molecular basis of chronic infammation in lung diseases: new therapeutic approach. J. Physiol. Pharmacol. 58 (suppl. 5): 453-460 (2007). (Pubitemid 351346694)
46. Lei, D.C. et al. Episomal expression of wild-type CFTR corrects cAMP-dependent chloride transport in respiratory epithelial cells. Gene Ter. 3, 427-436 (1996). (Pubitemid 26171341)
47. Devor, D.C., Bridges, R.J. & Pilewski, J.M. Pharmacological modulation of ion transport across wild-type and DeltaF508 CFTR-expressing human bronchial epithelia. Am. J. Physiol. Cell Physiol. 279, C461-C479 (2000).
48. Butterworth, M.B., Edinger, R.S., Johnson, J.P. & Frizzell, R.A. Acute ENaC stimulation by cAMP in a kidney cell line is mediated by exocytic insertion from a recycling channel pool. J. Gen. Physiol. 125, 81-101 (2005). (Pubitemid 40130100)
49. Myerburg, M.M. et al. Airway surface liquid volume regulates ENaC by altering the serine protease-protease inhibitor balance: a mechanism for sodium hyperabsorption in cystic fbrosis. J. Biol. Chem. 281, 27942-27949 (2006). (Pubitemid 44414506)
50. Myerburg, M.M. et al. Prostasin expression is regulated by airway surface liquid volume and is increased in cystic fbrosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L932-L941 (2008).