HDAC6 is overexpressed in cystic cholangiocytes and its inhibition reduces cystogenesis

American Journal of Pathology

Volumn 184, Issue 3, 2014, Pages 600-608

  Gradilone, Sergio A ^a   Habringer, Stefan ^a   Masyuk, Tatyana V ^a   Howard, Brynn N ^a   Masyuk, Anatoliy I ^a   Larusso, Nicholas F ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2-(DIPHENYLAMINO)-N-(7-(HYDROXYAMINO)-7-OXOHEPTYL)PYRIMIDINE-5-CARBOXAMIDE; ANILIDE; HDAC6 PROTEIN, HUMAN; HDAC6 PROTEIN, RAT; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; INDOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; TUBACIN; TUBASTATIN A;

ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYSTS; CYTOLOGY; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; EUKARYOTIC FLAGELLUM; FEMALE; HUMAN; INTRAHEPATIC BILE DUCT; LIVER; LIVER DISEASES; MALE; METABOLISM; PATHOLOGY; RAT; SIGNAL TRANSDUCTION; TIME FACTOR;

ANILIDES; ANIMALS; BILE DUCTS, INTRAHEPATIC; CELL PROLIFERATION; CELLS, CULTURED; CILIA; CYSTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; INDOLES; LIVER; LIVER DISEASES; MALE; PYRIMIDINES; RATS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84894135264     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.11.027     Document Type: Article

References (49)

1. T. Masyuk, A. Masyuk, and N. LaRusso Cholangiociliopathies: genetics, molecular mechanisms and potential therapies Curr Opin Gastroenterol 25 2009 265 271
2. J.P. Drenth, R.H. te Morsche, R. Smink, J.S. Bonifacino, and J.B. Jansen Germline mutations in PRKCSH are associated with autosomal dominant polycystic liver disease Nat Genet 33 2003 345 347 (Pubitemid 36278850)
3. S. Davila, L. Furu, A.G. Gharavi, X. Tian, T. Onoe, Q. Qian, A. Li, Y. Cai, P.S. Kamath, B.F. King, P.J. Azurmendi, P. Tahvanainen, H. Kaariainen, K. Hockerstedt, O. Devuyst, Y. Pirson, R.S. Martin, R.P. Lifton, E. Tahvanainen, V.E. Torres, and S. Somlo Mutations in SEC63 cause autosomal dominant polycystic liver disease Nat Genet 36 2004 575 577 (Pubitemid 38715981)
4. E. Woollatt, K.A. Pine, J. Shine, G.R. Sutherland, and T.P. Iismaa Human Sec63 endoplasmic reticulum membrane protein, map position 6q21 Chromosome Res 7 1999 77
5. H. Gao, Y. Wang, T. Wegierski, K. Skouloudaki, M. Putz, X. Fu, C. Engel, C. Boehlke, H. Peng, E.W. Kuehn, E. Kim, A. Kramer-Zucker, and G. Walz PRKCSH/80K-H, the protein mutated in polycystic liver disease, protects polycystin-2/TRPP2 against HERP-mediated degradation Hum Mol Genet 19 2010 16 24
6. J. Hughes, C.J. Ward, B. Peral, R. Aspinwall, K. Clark, J.L. San Millan, V. Gamble, and P.C. Harris The polycystic kidney disease 1 (PKD1) gene encodes a novel protein with multiple cell recognition domains Nat Genet 10 1995 151 160
7. T. Mochizuki, G. Wu, T. Hayashi, S.L. Xenophontos, B. Veldhuisen, J.J. Saris, D.M. Reynolds, Y. Cai, P.A. Gabow, A. Pierides, W.J. Kimberling, M.H. Breuning, C.C. Deltas, D.J. Peters, and S. Somlo PKD2, a gene for polycystic kidney disease that encodes an integral membrane protein Science 272 1996 1339 1342 (Pubitemid 26199975)
8. L.F. Onuchic, L. Furu, Y. Nagasawa, X. Hou, T. Eggermann, Z. Ren, C. Bergmann, J. Senderek, E. Esquivel, R. Zeltner, S. Rudnik-Schoneborn, M. Mrug, W. Sweeney, E.D. Avner, K. Zerres, L.M. Guay-Woodford, S. Somlo, and G.G. Germino PKHD1, the polycystic kidney and hepatic disease 1 gene, encodes a novel large protein containing multiple immunoglobulin-like plexin-transcription- factor domains and parallel beta-helix 1 repeats Am J Hum Genet 70 2002 1305 1317 (Pubitemid 34450580)
9. C.J. Ward, M.C. Hogan, S. Rossetti, D. Walker, T. Sneddon, X. Wang, V. Kubly, J.M. Cunningham, R. Bacallao, M. Ishibashi, D.S. Milliner, V.E. Torres, and P.C. Harris The gene mutated in autosomal recessive polycystic kidney disease encodes a large, receptor-like protein Nat Genet 30 2002 259 269
10. M. Lal, X. Song, J.L. Pluznick, V. Di Giovanni, D.M. Merrick, N.D. Rosenblum, V. Chauvet, C.J. Gottardi, Y. Pei, and M.J. Caplan Polycystin-1 C-terminal tail associates with beta-catenin and inhibits canonical Wnt signaling Hum Mol Genet 17 2008 3105 3117
11. T. Yamaguchi, S.J. Hempson, G.A. Reif, A.M. Hedge, and D.P. Wallace Calcium restores a normal proliferation phenotype in human polycystic kidney disease epithelial cells J Am Soc Nephrol 17 2006 178 187
12. T. Yamaguchi, S. Nagao, D.P. Wallace, F.A. Belibi, B.D. Cowley, J.C. Pelling, and J.J. Grantham Cyclic AMP activates B-Raf and ERK in cyst epithelial cells from autosomal-dominant polycystic kidneys Kidney Int 63 2003 1983 1994 (Pubitemid 36605809)
13. J.M. Banales, T.V. Masyuk, S.A. Gradilone, A.I. Masyuk, J.F. Medina, and N.F. LaRusso The cAMP effectors Epac and protein kinase a (PKA) are involved in the hepatic cystogenesis of an animal model of autosomal recessive polycystic kidney disease (ARPKD) Hepatology 49 2009 160 174
14. T.V. Masyuk, B.Q. Huang, C.J. Ward, A.I. Masyuk, D. Yuan, P.L. Splinter, R. Punyashthiti, E.L. Ritman, V.E. Torres, P.C. Harris, and N.F. LaRusso Defects in cholangiocyte fibrocystin expression and ciliary structure in the PCK rat Gastroenterology 125 2003 1303 1310 (Pubitemid 37409750)
15. J.M. Banales, T.V. Masyuk, P.S. Bogert, B.Q. Huang, S.A. Gradilone, S.O. Lee, A.J. Stroope, A.I. Masyuk, J.F. Medina, and N.F. LaRusso Hepatic cystogenesis is associated with abnormal expression and location of ion transporters and water channels in an animal model of autosomal recessive polycystic kidney disease Am J Pathol 173 2008 1637 1646
16. D. Alvaro, P. Onori, G. Alpini, A. Franchitto, D.M. Jefferson, A. Torrice, V. Cardinale, F. Stefanelli, M.G. Mancino, M. Strazzabosco, M. Angelico, A. Attili, and E. Gaudio Morphological and functional features of hepatic cyst epithelium in autosomal dominant polycystic kidney disease Am J Pathol 172 2008 321 332 (Pubitemid 351282020)
17. Y. Cao, N. Semanchik, S.H. Lee, S. Somlo, P.E. Barbano, R. Coifman, and Z. Sun Chemical modifier screen identifies HDAC inhibitors as suppressors of PKD models Proc Natl Acad Sci U S A 106 2009 21819 21824
18. L.X. Fan, X. Li, B. Magenheimer, J.P. Calvet, and X. Li Inhibition of histone deacetylases targets the transcription regulator Id2 to attenuate cystic epithelial cell proliferation Kidney Int 81 2012 76 85
19. Y. Li, X. Zhang, R.D. Polakiewicz, T.P. Yao, and M.J. Comb HDAC6 is required for epidermal growth factor-induced beta-catenin nuclear localization J Biol Chem 283 2008 12686 12690
20. S.A. Gradilone, B.N. Radtke, P.S. Bogert, B.Q. Huang, G.B. Gajdos, and N.F. Larusso HDAC6 inhibition restores ciliary expression and decreases tumor growth Cancer Res 73 2013 2259 2270
21. B. Vroman, and N.F. LaRusso Development and characterization of polarized primary cultures of rat intrahepatic bile duct epithelial cells Lab Invest 74 1996 303 313 (Pubitemid 26041031)
22. A.I. Masyuk, B.Q. Huang, C.J. Ward, S.A. Gradilone, J.M. Banales, T.V. Masyuk, B. Radtke, P.L. Splinter, and N.F. Larusso Biliary exosomes influence cholangiocyte regulatory mechanisms and proliferation through interaction with primary cilia Am J Physiol Gastrointest Liver Physiol 299 2010 G990 G999
23. S.P. O'Hara, P.L. Splinter, C.E. Trussoni, G.B. Gajdos, P.N. Lineswala, and N.F. LaRusso Cholangiocyte N-Ras protein mediates lipopolysaccharide-induced interleukin 6 secretion and proliferation J Biol Chem 286 2011 30352 30360
24. J.M. Banales, E. Saez, M. Uriz, S. Sarvide, A.D. Urribarri, P. Splinter, P.S. Tietz Bogert, L. Bujanda, J. Prieto, J.F. Medina, and N.F. Larusso Up-regulation of microRNA 506 leads to decreased Cl(-)/HCO(3) (-) anion exchanger 2 expression in biliary epithelium of patients with primary biliary cirrhosis Hepatology 56 2012 687 697
25. M.A. Muff, T.V. Masyuk, A.J. Stroope, B.Q. Huang, P.L. Splinter, S.O. Lee, and N.F. Larusso Development and characterization of a cholangiocyte cell line from the PCK rat, an animal model of autosomal recessive polycystic kidney disease Lab Invest 86 2006 940 950 (Pubitemid 44268168)
26. T.V. Masyuk, A.I. Masyuk, V.E. Torres, P.C. Harris, and N.F. Larusso Octreotide inhibits hepatic cystogenesis in a rodent model of polycystic liver disease by reducing cholangiocyte adenosine 3',5'-cyclic monophosphate Gastroenterology 132 2007 1104 1116 (Pubitemid 46440866)
27. S.O. Lee, T. Masyuk, P. Splinter, J.M. Banales, A. Masyuk, A. Stroope, and N. Larusso MicroRNA15a modulates expression of the cell-cycle regulator Cdc25A and affects hepatic cystogenesis in a rat model of polycystic kidney disease J Clin Invest 118 2008 3714 3724
28. S.A. Gradilone, T.V. Masyuk, B.Q. Huang, J.M. Banales, G.L. Lehmann, B.N. Radtke, A. Stroope, A.I. Masyuk, P.L. Splinter, and N.F. LaRusso Activation of Trpv4 reduces the hyperproliferative phenotype of cystic cholangiocytes from an animal model of ARPKD Gastroenterology 139 2010 304 314.e2
29. Y. Zhang, B. Gilquin, S. Khochbin, and P. Matthias Two catalytic domains are required for protein deacetylation J Biol Chem 281 2006 2401 2404 (Pubitemid 43845699)
30. A.B. Mak, A.M. Nixon, S. Kittanakom, J.M. Stewart, G.I. Chen, J. Curak, A.C. Gingras, R. Mazitschek, B.G. Neel, I. Stagljar, and J. Moffat Regulation of CD133 by HDAC6 promotes beta-catenin signaling to suppress cancer cell differentiation Cell Rep 2 2012 951 963
31. L. Santo, T. Hideshima, A.L. Kung, J.C. Tseng, D. Tamang, M. Yang, M. Jarpe, J.H. van Duzer, R. Mazitschek, W.C. Ogier, D. Cirstea, S. Rodig, H. Eda, T. Scullen, M. Canavese, J. Bradner, K.C. Anderson, S.S. Jones, and N. Raje Preclinical activity, pharmacodynamic, and pharmacokinetic properties of a selective HDAC6 inhibitor, ACY-1215, in combination with bortezomib in multiple myeloma Blood 119 2012 2579 2589
32. W. Liu, L.X. Fan, X. Zhou, W.E. Sweeney Jr., E.D. Avner, and X. Li HDAC6 regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation in renal epithelial cells PLoS One 7 2012 e49418
33. T.H. Hsieh, C.F. Tsai, C.Y. Hsu, P.L. Kuo, J.N. Lee, C.Y. Chai, S.C. Wang, and E.M. Tsai Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway FASEB J 26 2012 778 787
34. A.I. Masyuk, T.V. Masyuk, and N.F. LaRusso Cholangiocyte primary cilia in liver health and disease Dev Dyn 237 2008 2007 2012
35. T.V. Masyuk, B.N. Radtke, A.J. Stroope, J.M. Banales, A.I. Masyuk, S.A. Gradilone, G.B. Gajdos, N. Chandok, J.L. Bakeberg, C.J. Ward, E.L. Ritman, H. Kiyokawa, and N.F. LaRusso Inhibition of Cdc25A Suppresses hepato-renal cystogenesis in rodent models of polycystic kidney and liver disease Gastroenterology 142 2012 622 633.e4
36. T.V. Masyuk, B.N. Radtke, A.J. Stroope, J.M. Banales, S.A. Gradilone, B. Huang, A.I. Masyuk, M.C. Hogan, V.E. Torres, and N.F. Larusso Pasireotide is more effective than octreotide in reducing hepatorenal cystogenesis in rodents with polycystic kidney and liver diseases Hepatology 58 2013 409 421
37. M.C. Hogan, T.V. Masyuk, L. Page, D.R. Holmes 3rd, X. Li, E.J. Bergstralh, M.V. Irazabal, B. Kim, B.F. King, J.F. Glockner, N.F. Larusso, and V.E. Torres Somatostatin analog therapy for severe polycystic liver disease: results after 2 years Nephrol Dial Transplant 27 2012 3532 3539
38. M.C. Hogan, T.V. Masyuk, L.J. Page, V.J. Kubly, E.J. Bergstralh, X. Li, B. Kim, B.F. King, J. Glockner, D.R. Holmes 3rd, S. Rossetti, P.C. Harris, N.F. LaRusso, and V.E. Torres Randomized clinical trial of long-acting somatostatin for autosomal dominant polycystic kidney and liver disease J Am Soc Nephrol 21 2010 1052 1061
39. J.J. Grantham Polycystic kidney disease: neoplasia in disguise Am J Kidney Dis 15 1990 110 116
40. J.Y. Park, W.E. Schutzer, J.N. Lindsley, S.P. Bagby, T.T. Oyama, S. Anderson, and R.H. Weiss p21 is decreased in polycystic kidney disease and leads to increased epithelial cell cycle progression: roscovitine augments p21 levels BMC Nephrol 8 2007 12
41. T. Masyuk, and N. LaRusso Polycystic liver disease: new insights into disease pathogenesis Hepatology 43 2006 906 908 (Pubitemid 43724613)
42. T.V. Masyuk, B.Q. Huang, A.I. Masyuk, E.L. Ritman, V.E. Torres, X. Wang, P.C. Harris, and N.F. Larusso Biliary dysgenesis in the PCK rat, an orthologous model of autosomal recessive polycystic kidney disease Am J Pathol 165 2004 1719 1730 (Pubitemid 39435169)
43. M.S. Finnin, J.R. Donigian, A. Cohen, V.M. Richon, R.A. Rifkind, P.A. Marks, R. Breslow, and N.P. Pavletich Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors Nature 401 1999 188 193 (Pubitemid 29436325)
44. Y. Zhang, S. Kwon, T. Yamaguchi, F. Cubizolles, S. Rousseaux, M. Kneissel, C. Cao, N. Li, H.L. Cheng, K. Chua, D. Lombard, A. Mizeracki, G. Matthias, F.W. Alt, S. Khochbin, and P. Matthias Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally Mol Cell Biol 28 2008 1688 1701
45. M. Haberland, R.L. Montgomery, and E.N. Olson The many roles of histone deacetylases in development and physiology: implications for disease and therapy Nat Rev Genet 10 2009 32 42
46. F. Lin, T. Hiesberger, K. Cordes, A.M. Sinclair, L.S. Goldstein, S. Somlo, and P. Igarashi Kidney-specific inactivation of the KIF3A subunit of kinesin-II inhibits renal ciliogenesis and produces polycystic kidney disease Proc Natl Acad Sci U S A 100 2003 5286 5291 (Pubitemid 36542697)
47. M.A. Lancaster, and J.G. Gleeson Cystic kidney disease: the role of Wnt signaling Trends Mol Med 16 2010 349 360
48. A. Wuebken, and K.M. Schmidt-Ott WNT/beta-catenin signaling in polycystic kidney disease Kidney Int 80 2011 135 138
49. C. Spirli, L. Locatelli, C.M. Morell, R. Fiorotto, S.D. Morton, M. Cadamuro, L. Fabris, and M. Strazzabosco Protein kinase a-dependent pSer -beta-catenin, a novel signaling defect in a mouse model of congenital hepatic fibrosis Hepatology 58 2013 1713 1723