Downregulation of Ca2+-activated Cl- channel TMEM16A by the inhibition of histone deacetylase in TMEM16A-expressing cancer cells

Journal of Pharmacology and Experimental Therapeutics

Volumn 351, Issue 3, 2014, Pages 510-518

  Matsuba, Sayo ^a   Niwa, Satomi ^a   Muraki, Katsuhiko ^b   Kanatsuka, Saki ^a   Nakazono, Yurika ^a   Hatano, Noriyuki ^b   Fujii, Masanori ^a   Zhan, Peng ^c   Suzuki, Takayoshi ^c   Ohya, Susumu ^a  

^a KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^b AICHI GAKUIN UNIVERSITY   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4 (ACETYLAMINO) N [2 AMINO 5 (2 THIENYL)PHENYL] BENZAMIDE; CALCIUM ACTIVATED CHLORIDE CHANNEL; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; PACLITAXEL; SMALL INTERFERING RNA; TRANSMEMBRANE PROTEINS WITH UNKNOWN FUNCTION 16 A; UNCLASSIFIED DRUG; VORINOSTAT; ANO1 PROTEIN, HUMAN; CHLORIDE CHANNEL; HYDROXAMIC ACID; TUMOR PROTEIN;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER; CANCER CELL; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; EPIGENETIC REPRESSION; GENE ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MALE; PROSTATE CANCER; TRANSCRIPTION REGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; MCF 7 CELL LINE; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; CHLORIDE CHANNELS; DOWN-REGULATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; MCF-7 CELLS; NEOPLASM PROTEINS;

EID: 84908297934     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.217315     Document Type: Article

References (51)

1. Akervall JA, Jin Y, Wennerberg JP, Zätterström UK, Kjellén E, Mertens F, Willén R, Mandahl N, Heim S, and Mitelman F (1995) Chromosomal abnormalities involving 11q13 are associated with poor prognosis in patients with squamous cell carcinoma of the head and neck. Cancer 76:853-859.
2. Alenghat T, Osborne LC, Saenz SA, Kobuley D, Ziegler CG, Mullican SE, Choi I, Grunberg S, Sinha R, and Wynosky-Dolfi M, et al. (2013) Histone deacetylase 3 coordinates commensal-bacteria-dependent intestinal homeostasis. Nature 504:153-157.
3. Ayoub C, Wasylyk C, Li Y, Thomas E, Marisa L, Robé A, Roux M, Abecassis J, de Reyniès A, and Wasylyk B (2010) ANO1 amplification and expression in HNSCC with a high propensity for future distant metastasis and its functions in HNSCC cell lines. Br J Cancer 103:715-726.
4. Britschgi A, Bill A, Brinkhaus H, Rothwell C, Clay I, Duss S, Rebhan M, Raman P, Guy CT, and Wetzel K, et al. (2013) Calcium-activated chloride channel ANO1 promotes breast cancer progression by activating EGFR and CAMK signaling. Proc Natl Acad Sci USA 110:E1026-E1034.
5. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, and Galietta LJ (2008) TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322:590-594.
6. Chen X, Barozzi I, Termanini A, Prosperini E, Recchiuti A, Dalli J, Mietton F, Matteoli G, Hiebert S, and Natoli G (2012) Requirement for the histone deacetylase Hdac3 for the inflammatory gene expression program in macrophages. Proc Natl Acad Sci USA 109:E2865-E2874.
7. Cheong A, Bingham AJ, Li J, Kumar B, Sukumar P, Munsch C, Buckley NJ, Neylon CB, Porter KE, and Beech DJ, et al. (2005) Downregulated REST transcription factor is a switch enabling critical potassium channel expression and cell proliferation. Mol Cell 20:45-52.
8. Chini CCS, Escande C, Nin V, and Chini EN (2010) HDAC3 is negatively regulated by the nuclear protein DBC1. J Biol Chem 285:40830-40837.
9. Chou CJ, Herman D, and Gottesfeld JM (2008) Pimelic diphenylamide 106 is a slow, tight-binding inhibitor of class I histone deacetylases. J Biol Chem 283:35402-35409.
10. Duran C and Hartzell HC (2011) Physiological roles and diseases of Tmem16/Anoctamin proteins: are they all chloride channels? Acta Pharmacol Sin 32:685-692.
11. Duvvuri U, Shiwarski DJ, Xiao D, Bertrand C, Huang X, Edinger RS, Rock JR, Harfe BD, Henson BJ, and Kunzelmann K, et al. (2012) TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression. Cancer Res 72:3270-3281.
12. Ellis L, Hammers H, and Pili R (2009) Targeting tumor angiogenesis with histone deacetylase inhibitors. Cancer Lett 280:145-153.
13. WAF1 involves changes in promoter-associated proteins, including HDAC1. Proc Natl Acad Sci USA 101:1241-1246.
14. Hatano N, Suzuki H, Muraki Y, and Muraki K (2013) Stimulation of human TRPA1 channels by clinical concentrations of the antirheumatic drug auranofin. Am J Physiol Cell Physiol 304:C354-C361.
15. Huang X, Gollin SM, Raja S, and Godfrey TE (2002) High-resolution mapping of the 11q13 amplicon and identification of a gene, TAOS1, that is amplified and overexpressed in oral cancer cells. Proc Natl Acad Sci USA 99:11369-11374.
16. Itoh Y, Suzuki T, Kouketsu A, Suzuki N, Maeda S, Yoshida M, Nakagawa H, and Miyata N (2007) Design, synthesis, structure - selectivity relationship, and effect on human cancer cells of a novel series of histone deacetylase 6-selective inhibitors. J Med Chem 50:5425-5438.
17. Iwamoto M, Friedman EJ, Sandhu P, Agrawal NG, Rubin EH, and Wagner JA (2013) Clinical pharmacology profile of vorinostat, a histone deacetylase inhibitor. Cancer Chemother Pharmacol 72:493-508.
18. Jacobsen KS, Zeeberg K, Sauter DR, Poulsen KA, Hoffmann EK, and Schwab A (2013) The role of TMEM16A (ANO1) and TMEM16F (ANO6) in cell migration. Pflugers Arch 465:1753-1762.
19. Kim HC, Choi KC, Choi HK, Kang HB, Kim MJ, Lee YH, Lee OH, Lee J, Kim YJ, and Jun W, et al. (2010) HDAC3 selectively represses CREB3-mediated transcription and migration of metastatic breast cancer cells. Cell Mol Life Sci 67:3499-3510.
20. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW, Moon EJ, Kim HS, Lee SK, and Chung HY, et al. (2001) Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 7:437-443.
21. Komatsu Y, Hibi K, Kodera Y, Akiyama S, Ito K, and Nakao A (2006) TAOS1, a novel marker for advanced esophageal squamous cell carcinoma. Anticancer Res 26 (3A):2029-2032.
22. Lang F and Stournaras C (2014) Ion channels in cancer: future perspectives and clinical potential. Philos Trans R Soc Lond B Biol Sci 369:20130108.
23. Li J, Li G, and Xu W (2013) Histone deacetylase inhibitors: an attractive strategy for cancer therapy. Curr Med Chem 20:1858-1886.
24. Lin H, Li Z, Chen C, Luo X, Xiao J, Dong D, Lu Y, Yang B, and Wang Z (2011) Transcriptional and post-transcriptional mechanisms for oncogenic overexpression of ether à go-go K1 channel. PLoS ONE 6:e20362.
25. Liu W, Lu M, Liu B, Huang Y, and Wang K (2012) Inhibition of Ca(2+)-activated Cl(-) channel ANO1/TMEM16A expression suppresses tumor growth and invasiveness in human prostate carcinoma. Cancer Lett 326:41-51.
26. Marks PA (2007) Discovery and development of SAHA as an anticancer agent. Oncogene 26:1351-1356.
27. Martin-Trujillo A, Iglesias-Platas I, Coto E, Corral-Juan M, San Nicolás H, Corral J, Volpini V, Matilla-Dueñas A, and Monk D (2011) Genotype of an individual single nucleotide polymorphism regulates DNA methylation at the TRPC3 alternative promoter. Epigenetics 6:1236-1241.
28. Methot JL, Chakravarty PK, Chenard M, Close J, Cruz JC, Dahlberg WK, Fleming J, Hamblett CL, Hamill JE, and Harrington P, et al. (2008) Exploration of the internal cavity of histone deacetylase (HDAC) with selective HDAC1/HDAC2 inhibitors (SHI-1:2). Bioorg Med Chem Lett 18:973-978.
29. Miao LJ, Huang FX, Sun ZT, Zhang RX, Huang SF, and Wang J (2014) Stat3 inhibits Beclin 1 expression through recruitment of HDAC3 in nonsmall cell lung cancer cells. Tumour Biol 35:7097-7103.
30. Minami J, Suzuki R, Mazitschek R, Gorgun G, Ghosh B, Cirstea D, Hu Y, Mimura N, Ohguchi H, and Cottini F, et al. (2014) Histone deacetylase 3 as a novel therapeutic target in multiple myeloma. Leukemia 28:680-689.
31. Müller BM, Jana L, Kasajima A, Lehmann A, Prinzler J, Budczies J, Winzer KJ, Dietel M, Weichert W, and Denkert C (2013) Differential expression of histone deacetylases HDAC1, 2 and 3 in human breast cancer - overexpression of HDAC2 and HDAC3 is associated with clinicopathological indicators of disease progression. BMC Cancer 13:215.
32. Munster PN, Marchion D, Thomas S, Egorin M, Minton S, Springett G, Lee JH, Simon G, Chiappori A, and Sullivan D, et al. (2009) Phase I trial of vorinostat and doxorubicin in solid tumours: histone deacetylase 2 expression as a predictive marker. Br J Cancer 101:1044-1050.
33. Narlikar GJ, Fan HY, and Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487.
34. Nwaobi SE, Lin E, Peramsetty SR, and Olsen ML (2014) DNA methylation functions as a critical regulator of Kir4.1 expression during CNS development. Glia 62:411-427.
35. - channels via homo- and hetero-dimer formation of TMEM16A splicing variants in murine portal vein. Biochem Biophys Res Commun 443:518-523.
36. +-channel subtypes in human prostate cancer. J Pharmacol Sci 109:148-151.
37. + channel in auricular lymph node CD4+ T-lymphocyte function of the delayed-type hypersensitivity model. Br J Pharmacol 169:1011-1023.
38. Ca3.1, as a novel therapeutic target for benign prostatic hyperplasia. J Pharmacol Exp Ther 338:528-536.
39. Pardo LA and Stühmer W (2014) The roles of K(+) channels in cancer. Nat Rev Cancer 14:39-48.
40. Ropero S and Esteller M (2007) The role of histone deacetylases (HDACs) in human cancer. Mol Oncol 1:19-25.
41. Ruiz C, Martins JR, Rudin F, Schneider S, Dietsche T, Fischer CA, Tornillo L, Terracciano LM, Schreiber R, and Bubendorf L, et al. (2012) Enhanced expression of ANO1 in head and neck squamous cell carcinoma causes cell migration and correlates with poor prognosis. PLoS ONE 7:e43265.
42. Schroeder BC, Cheng T, Jan YN, and Jan LY (2008) Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019-1029.
43. - channel Ano1/TMEM16A. J Biol Chem 286:1381-1388.
44. Suzuki T, Kasuya Y, Itoh Y, Ota Y, Zhan P, Asamitsu K, Nakagawa H, Okamoto T, and Miyata N (2013) Identification of highly selective and potent histone deacetylase 3 inhibitors using click chemistry-based combinatorial fragment assembly. PLoS ONE 8:e68669.
45. Taylor P, Fangusaro J, Rajaram V, Goldman S, Helenowski IB, MacDonald T, Hasselblatt M, Riedemann L, Laureano A, and Cooper L, et al. (2012) REST is a novel prognostic factor and therapeutic target for medulloblastoma. Mol Cancer Ther 11:1713-1723.
46. Uchida H, Sasaki K, Ma L, and Ueda H (2010) Neuron-restrictive silencer factor causes epigenetic silencing of Kv4.3 gene after peripheral nerve injury. Neuroscience 166:1-4.
47. Venkatraman A, Hu YS, Didonna A, Cvetanovic M, Krbanjevic A, Bilesimo P, and Opal P (2014) The histone deacetylase HDAC3 is essential for Purkinje cell function, potentially complicating the use of HDAC inhibitors in SCA1. Hum Mol Genet 23:3733-3745.
48. + channel in enhanced cell proliferation by ATP in brain endothelial cells. J Biol Chem 281:38430-38439.
49. Yang M and Brackenbury WJ (2013) Membrane potential and cancer progression. Front Physiol 4:185.
50. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, and Kim BM, et al. (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210-1215.
51. Zhu J, Wan H, Xue C, Jiang T, Qian C, and Zhang Y (2013) Histone deacetylase 3 implicated in the pathogenesis of children glioma by promoting glioma cell proliferation and migration. Brain Res 1520:15-22.