A Histone deacetylase inhibitor suppresses epithelial-mesenchymal transition and attenuates chemoresistance in biliary tract cancer

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Sakamoto, Takuya ^a   Kobayashi, Shogo ^a,b   Yamada, Daisaku ^a   Nagano, Hiroaki ^a   Tomokuni, Akira ^a   Tomimaru, Yoshito ^a   Noda, Takehiro ^a   Gotoh, Kunihito ^a   Asaoka, Tadafumi ^a   Wada, Hiroshi ^a   Kawamoto, Koichi ^a   Marubashi, Shigeru ^a   Eguchi, Hidetoshi ^a   Doki, Yuichiro ^a   Mori, Masaki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; GEMCITABINE; MESSENGER RNA; PROTEIN CDH2; SMAD4 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAI1; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; TRANSCRIPTION FACTOR ZEB2; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; VORINOSTAT; ANTINEOPLASTIC AGENT; HISTONE DEACETYLASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILIARY TRACT CANCER; BINDING AFFINITY; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CANCER SURVIVAL; CELL CYCLE REGULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR XENOGRAFT; ANIMAL; BILIARY TRACT NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BILIARY TRACT NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HISTONE DEACETYLASE INHIBITORS; HUMANS; MICE; TRANSFORMING GROWTH FACTOR BETA1; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84954053900     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145985     Document Type: Article

References (51)

1. Jang JY, Kim SW, Park DJ, Ahn YJ, Yoon YS, Choi MG, et al. Actual long-term outcome of extrahepatic bile duct cancer after surgical resection. Ann Surg. 2005; 241: 77-84. PMID: 15621994
2. Murakami S, Ajiki T, Okazaki T, Ueno K, Kido M, Matsumoto I, et al. Factors affecting survival after resection of intrahepatic cholangiocarcinoma. Surg Today. 2014; 44: 1847-54. doi: 10.1007/s00595-013-0825-9 PMID: 24452507
3. Kim HJ, Kim CY, Hur YH, Koh YS, Kim JC, Kim HJ, et al. The prognostic factors for survival after curative resection of distal cholangiocarcinoma: perineural invasion and lymphovascular invasion. Surg Today. 2014; 44: 1879-86. doi: 10.1007/s00595-014-0846-z PMID: 24535697
4. Kobayashi S, Nagano H, Marubashi S, Wada H, Eguchi H, Takeda Y, et al. Treatment of borderline cases for curative resection of biliary tract cancer. J Surg Oncol. 2011; 104: 499-503. doi: 10.1002/jso. 21971 PMID: 21538362
5. Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010; 362: 1273-81. doi: 10.1056/NEJMoa0908721 PMID: 20375404
6. Kobayashi S, Werneburg NW, Bronk SF, Kaufmann SH, Gores GJ. Interleukin-6 contributes to Mcl-1 up-regulation and TRAIL resistance via an Akt-signaling pathway in cholangiocarcinoma cells. Gastroenterology. 2005; 128: 2054-65. PMID: 15940637
7. Nitta T, Mitsuhashi T, Hatanaka Y, Miyamoto M, Oba K, Tsuchikawa T, et al. Prognostic significance of epithelial-mesenchymal transition-related markers in extrahepatic cholangiocarcinoma: comprehensive immunohistochemical study using a tissue microarray. Br J Cancer. 2014; 111: 1363-72. doi: 10. 1038/bjc.2014.415 PMID: 25077440
8. Nakashima S, Kobayashi S, Nagano H, Tomokuni A, Tomimaru Y, Asaoka T, et al. BRCA/Fanconi Anemia Pathway Implicates Chemo-resistance to Gemcitabine in Biliary Tract Cancer. Cancer Sci. 2015 doi: 10.1111/cas.12652
9. Mott JL, Kobayashi S, Bronk SF, Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene. 2007; 26: 6133-40. PMID: 17404574
10. Yamada D, Kobayashi S, Wada H, Kawamoto K, Marubashi S, Eguchi H, et al. Role of crosstalk between interleukin-6 and transforming growth factor-beta 1 in epithelial-mesenchymal transition and chemoresistance in biliary tract cancer. Eur J Cancer. 2013; 49: 1725-40. doi: 10.1016/j.ejca.2012.12. 002 PMID: 23298711
11. Zavadil J, Böttinger EP. TGF-bold italic beta and epithelial-to-mesenchymal transitions. Oncogene. 2005; 24: 5764-74. PMID: 16123809
12. Gonzalez DM, Medici D. Signaling mechanisms of the epithelial-mesenchymal transition. Sci Signal. 2014 7: re8. doi: 10.1126/scisignal.2005189 PMID: 25249658
13. Farrell J, Kelly C, Rauch J, Kida K, García-Muñoz A, Monsefi N, et al. HGF induces epithelial-to-mesenchymal transition by modulating the mammalian hippo/MST2 and ISG15 pathways. J Proteome Res. 2014; 13: 2874-86. doi: 10.1021/pr5000285 PMID: 24766643
14. Rokavec M, Öner MG, Li H, Jackstadt R, Jiang L, Lodygin D, et al. IL-6R/STAT3/miR-34a feedback loop promotes EMT-mediated colorectal cancer invasion and metastasis. J Clin Invest. 2014; 124: 1853-67. doi: 10.1172/JCI73531 PMID: 24642471
15. Ogunwobi OO, Puszyk W, Dong HJ, Liu C. Epigenetic upregulation of HGF and c-Met drives metastasis in hepatocellular carcinoma. PLoS One. 2013; 8: e63765. doi: 10.1371/journal.pone.0063765 PMID: 23723997
16. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014; 15: 178-96. doi: 10.1038/nrm3758 PMID: 24556840
17. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 2002; 3: 155-66. PMID: 11994736
18. Chanmee T, Ontong P, Mochizuki N, Kongtawelert P, Konno K, Itano N. Excessive hyaluronan production promotes acquisition of cancer stem cell signatures through the coordinated regulation of Twist and the transforming growth factor β (TGF-β)-Snail signaling axis. J Biol Chem. 2014; 289: 26038-56. doi: 10.1074/jbc.M114.564120 PMID: 25077968
19. Hotz B, Arndt M, Dullat S, Bhargava S, Buhr HJ, Hotz HG. Epithelial to mesenchymal transition: expression of the regulators snail, slug, and twist in pancreatic cancer. Clin Cancer Res. 2007; 13: 4769-76. PMID: 17699854
20. Kurahara H, Takao S, Maemura K, Mataki Y, Kuwahata T, Maeda K, et al. Epithelial-mesenchymal transition and mesenchymal-epithelial transition via regulation of ZEB-1 and ZEB-2 expression in pancreatic cancer. J Surg Oncol. 2012; 105: 655-61. doi: 10.1002/jso.23020 PMID: 22213144
21. von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, Messer M, et al. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterology. 2009; 137: 361-71. doi: 10.1053/j.gastro.2009.04.004 PMID: 19362090
22. Kaimori A, Potter JJ, Choti M, Ding Z, Mezey E, Koteish AA. Histone deacetylase inhibition suppresses the transforming growth factor beta1-induced epithelial-to-mesenchymal transition in hepatocytes. Hepatology. 2010; 52: 1033-45. doi: 10.1002/hep.23765 PMID: 20564330
23. Chung CL, Sheu JR, Chen WL, Chou YC, Hsiao CJ, Hsiao SH, et al. Histone deacetylase inhibitor mcarboxycinnamic acid bis-hydroxamide attenuates plasminogen activator inhibitor-1 expression in human pleural mesothelial cells. Am J Respir Cell Mol Biol. 2012; 46: 437-45. doi: 10.1165/rcmb. 2011-0118OC PMID: 22033265
24. Kobayashi S, Werneburg NW, Bronk SF, Kaufmann SH, Gores GJ, et al. Interleukin-6 contributes to Mcl-1 up-regulation and TRAIL resistance via an Akt-signaling pathway in cholangiocarcinoma cells. Gastroenterology. 2005; 128: 2054-65. PMID: 15940637
25. Shimizu Y, Demetris AJ, Gollin SM, Storto PD, Bedford HM, Altarac S, et al. Two new human cholangiocarcinoma cell lines and their cytogenetics and responses to growth factors, hormones, cytokines or immunologic effector cells. Int J Cancer. 1992; 52: 252-60 PMID: 1355757
26. Murakami T, Yano H, Maruiwa M, Sugihara S, Kojiro M. Establishment and characterization of a human combined hepatocholangiocarcinoma cell line and its heterologous transplantation in nude mice. Hepatology. 1987; 7: 551-6 PMID: 3032760
27. Knuth A, Gabbert H, Dippold W, Klein O, Sachsse W, Bitter-Suermann D, et al. Biliary adenocarcinoma. Characterisation of three new human tumor cell lines. J Hepatol. 1985; 1: 579-96 PMID: 4056357
28. Yamada D, Kobayashi S, Yamamoto H, Tomimaru Y, Noda T, Uemura M, et al. Role of the hypoxiarelated gene, JMJD1A, in hepatocellular carcinoma: clinical impact on recurrence after hepatic resection. Ann Surg Oncol. 2012; 19 Suppl 3: S355-64 doi: 10.1245/s10434-011-1797-x PMID: 21607773
29. Miyoshi N, Ishii H, Nagai K, Hoshino H, Mimori K, Tanaka F, et al. Defined factors induce reprogramming of gastrointestinal cancer cells. Proc Natl Acad Sci USA. 2010; 107: 40-5 doi: 10.1073/pnas. 0912407107 PMID: 20018687
30. Imhof A, Wolffe AP. Transcription: gene control by targeted histone acetylation. Curr Biol. 1998; 8: R422-4. PMID: 9637914
31. Jenuwein T, Allis CD. Translating the histone code. Science. 2001; 293: 1074-80. PMID: 11498575
32. Irvine RA, Lin IG, Hsieh CL. DNA methylation has a local effect on transcription and histone acetylation. Mol Cell Biol. 2002; 22: 6689-96. PMID: 12215526
33. Sui X, Zhu J, Zhou J, Wang X, Li D, Han W, et al. Epigenetic modifications as regulatory elements of autophagy in cancer. Cancer Lett. 2015; 360: 106-13. doi: 10.1016/j.canlet.2015.02.009 PMID: 25687886
34. Rodrigues MF, Carvalho Á, Pezzuto P, Rumjanek FD, Amoêdo ND. Reciprocal modulation of histone deacetylase inhibitors sodium butyrate and trichostatin a on the energy metabolism of breast cancer cells. J Cell Biochem. 2015; 116: 797-808. doi: 10.1002/jcb.25036 PMID: 25510910
35. Munster PN, Thurn KT, Thomas S, Raha P, Lacevic M, Miller A, et al. A phase II study of the histone deacetylase inhibitor vorinostat combined with tamoxifen for the treatment of patients with hormone therapy-resistant breast cancer. Br J Cancer. 2011; 104: 1828-35 doi: 10.1038/bjc.2011.156 PMID: 21559012
36. Ramaswamy B, Fiskus W, Cohen B, Pellegrino C, Hershman DL, Chuang E, et al. Phase I-II study of vorinostat plus paclitaxel and bevacizumab in metastatic breast cancer: evidence for vorinostatinduced tubulin acetylation and Hsp90 inhibition in vivo. Breast Cancer Res Treat. 2012; 132: 1063-72 doi: 10.1007/s10549-011-1928-x PMID: 22200869
37. Fakih MG, Groman A, McMahon J, Wilding G, Muindi JR. A randomized phase II study of two doses of vorinostat in combination with 5-FU/LV in patients with refractory colorectal cancer. Cancer Chemother Pharmacol. 2012; 69: 743-51 doi: 10.1007/s00280-011-1762-1 PMID: 22020318
38. Tu Y, Hershman DL, Bhalla K, Fiskus W, Pellegrino CM, Andreopoulou E, et al. A phase I-II study of the histone deacetylase inhibitor vorinostat plus sequential weekly paclitaxel and doxorubicin-cyclophosphamide in locally advanced breast cancer. Breast Cancer Res Treat. 2014; 146: 145-52. doi: 10. 1007/s10549-014-3008-5 PMID: 24903226
39. Krug LM, Kindler HL, Calvert H, Manegold C, Tsao AS, Fennell D, et al. Vorinostat in patients with advanced malignant pleural mesothelioma who have progressed on previous chemotherapy (VANTAGE-014): a phase 3, double-blind, randomised, placebo-controlled trial. Lancet Oncol. 2015; 16: 447-56 doi: 10.1016/S1470-2045(15)70056-2 PMID: 25800891
40. Reguart N, Rosell R, Cardenal F, Cardona AF, Isla D, Palmero R, et al. Phase I/II trial of vorinostat (SAHA) and erlotinib for non-small cell lung cancer (NSCLC) patients with epidermal growth factor receptor (EGFR) mutations after erlotinib progression. Lung Cancer. 2014; 84: 161-7. doi: 10.1016/j. lungcan.2014.02.011 PMID: 24636848
41. Kawabata M, Miyazono K. Signal transduction of the TGF-beta superfamily by Smad proteins. J Biochem. 1999; 125: 9-16. PMID: 9880789
42. Shi Y, Massagué J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 2003; 113: 685-700. PMID: 12809600
43. Cieply B, Farris J, Denvir J, Ford HL, Frisch SM, et al. Epithelial-mesenchymal transition and tumor suppression are controlled by a reciprocal feedback loop between ZEB1 and Grainyhead-like-2. Cancer Res. 2013; 73: 6299-309. doi: 10.1158/0008-5472.CAN-12-4082 PMID: 23943797
44. Talbot LJ, Bhattacharya SD, Kuo PC. Epithelial-mesenchymal transition, the tumor microenvironment, and metastatic behavior of epithelial malignancies. Int J Biochem Mol Biol. 2012; 3: 117-36. PMID: 22773954
45. Datto MB, Li Y, Panus JF, Howe DJ, Xiong Y, Wang XF. Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc Natl Acad Sci U S A. 1995; 92: 5545-9 PMID: 7777546
46. Bellucci L, Dalvai M, Kocanova S, Moutahir F, Bystricky K. Activation of p21 by HDAC inhibitors requires acetylation of H2A.Z. PLoS One. 2013; 8: e54102 (doi: 10.1371/journal.pone.0054102) PMID: 23349794
47. Li XL, Hara T, Choi Y, Subramanian M, Francis P, Bilke S, et al. A p21-ZEB1 complex inhibits epithelialmesenchymal transition through the microRNA 183-96-182 cluster. Mol Cell Biol. 2014; 34: 533-50 doi: 10.1128/MCB.01043-13 PMID: 24277930
48. Sun S, Han Y, Liu J, Fang Y, Tian Y, Zhou J, et al. Trichostatin A targets the mitochondrial respiratory chain, increasing mitochondrial reactive oxygen species production to trigger apoptosis in human breast cancer cells. PLoS One. 2014; 9: e91610. doi: 10.1371/journal.pone.0091610 PMID: 24626188
49. Abaza MS, Bahman AM, Al-Attiyah RJ. Valproic acid, an anti-epileptic drug and a histone deacetylase inhibitor, in combination with proteasome inhibitors exerts antiproliferative, pro-apoptotic and chemosensitizing effects in human colorectal cancer cells: underlying molecular mechanisms. Int J Mol Med. 2014; 34: 513-32. doi: 10.3892/ijmm.2014.1795 PMID: 24899129
50. Cassier PA, Floquet A, Penel N, Derbel O, Bui N'guyen B, Guastalla JP, et al. The histone deacetylase inhibitor panobinostat is active in patients with advanced pretreated ovarian sex-cord tumors. Ann Oncol. 2014; 25: 1074-5. doi: 10.1093/annonc/mdu045 PMID: 24651409
51. Ngamphaiboon N, Dy GK, Ma WW, Zhao Y, Reungwetwattana T, DePaolo D, et al. A phase I study of the histone deacetylase (HDAC) inhibitor entinostat, in combination with sorafenib in patients with advanced solid tumors. Invest New Drugs. 2015; 33: 225-32. doi: 10.1007/s10637-014-0174-6 PMID: 25371323