Inhibition of calcium-activated chloride channel ANO1/TMEM16A suppresses tumor growth and invasion in human lung cancer

PLoS ONE

Volumn 10, Issue 8, 2015, Pages

  Jia, Linghan ^a   Liu, Wen ^a   Guan, Lizhao ^a   Lu, Min ^b   Wang, KeWei ^a,c  

^a PEKING UNIVERSITY   (China)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c QINGDAO UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; PROTEIN ANO1; PROTEIN TMEM16A; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANO1 PROTEIN, HUMAN; CALCIUM; CHLORIDE CHANNEL; SMALL INTERFERING RNA; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG CANCER; MOUSE; NONHUMAN; PROTEIN EXPRESSION; TUMOR GROWTH; TUMOR INVASION; UPREGULATION; ADENOCARCINOMA; ANIMAL; BIOSYNTHESIS; CELL MOTION; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; PATHOLOGY;

ADENOCARCINOMA; ANIMALS; CALCIUM; CELL MOVEMENT; CELL PROLIFERATION; CHLORIDE CHANNELS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MICE; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; RNA, SMALL INTERFERING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942940994     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0136584     Document Type: Article

References (54)

1. Detterbeck FC, Boffa DJ, Tanoue LT. The new lung cancer staging system. Chest. 2009; 136(1):260-71. Epub 2009/07/09. doi:10.1378/chest.08-0978 136/1/260 [pii]. PMID: 19584208
2. Pedersen SF, Stock C. Ion channels and transporters in cancer: pathophysiology, regulation, and clinical potential. Cancer Res. 2013; 73(6):1658-61. Epub 2013/01/11. doi:10.1158/0008-5472.CAN-12-4188 [pii]. PMID: 23302229.
3. Tsavaler L, Shapero MH, Morkowski S, Laus R. Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res. 2001; 61(9):3760-9. Epub 2001/04/28. PMID: 11325849.
4. Hille B, editor. Ion Channels of Excitable Membranes: Sinauer, 3rd; 2001.
5. Aryal P, Sansom MS, Tucker SJ. Hydrophobic Gating in Ion Channels. J Mol Biol. 2014. Epub 2014/08/ 12. S0022-2836(14)00397-0 [pii] doi: 10.1016/j.jmb.2014.07.030 PMID: 25106689.
6. Lang F, Foller M, Lang KS, Lang PA, Ritter M, Gulbins E, et al. Ion channels in cell proliferation and apoptotic cell death. J Membr Biol. 2005; 205(3):147-57. Epub 2005/12/20. doi:10.1007/s00232-005-0780-5 PMID: 16362503.
7. Razik MA, Cidlowski JA. Molecular interplay between ion channels and the regulation of apoptosis. Biol Res. 2002; 35(2):203-7. Epub 2002/11/06. PMID: 12415737.
8. Zhou ZL, Jiang J, Yin JA, Cai SQ. Identifying interacting proteins of a Caenorhabditis elegans voltagegated chloride channel CLH-1 using GFP-Trap and mass spectrometry. Sheng Li Xue Bao. 2014; 66 (3):341-8. Epub 2014/06/27. PMID: 24964852.
9. Duran C, Thompson CH, Xiao Q, Hartzell HC. Chloride channels: often enigmatic, rarely predictable. Annu Rev Physiol. 2010; 72:95-121. Epub 2009/10/16. doi:10.1146/annurev-physiol-021909-135811 PMID: 19827947; PubMed Central PMCID: PMC2851227.
10. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S. Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol. 2001; 532(Pt 1):3-16. Epub 2001/04/03. PHY-12151 [pii]. PMID: 11283221; PubMed Central PMCID: PMC2278524.
11. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev. 2009; 89(1):193-277. Epub 2009/01/08. doi:10.1152/physrev.00037.2007 [pii]. PMID: 19126758.
12. Haussinger D. The role of cellular hydration in the regulation of cell function. Biochem J. 1996; 313 (Pt 3):697-710. Epub 1996/02/01. PMID: 8611144; PubMed Central PMCID: PMC1216967.
13. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, et al. Functional significance of cell volume regulatory mechanisms. Physiol Rev. 1998; 78(1):247-306. Epub 1998/02/11. PMID: 9457175.
14. Furst J, Gschwentner M, Ritter M, Botta G, Jakab M, Mayer M, et al. Molecular and functional aspects of anionic channels activated during regulatory volume decrease in mammalian cells. Pflugers Arch. 2002; 444(1-2):1-25. Epub 2002/04/27. doi:10.1007/s00424-002-0805-1 PMID: 11976912.
15. Diss JK, Stewart D, Pani F, Foster CS, Walker MM, Patel A, et al. A potential novel marker for human rostate cancer: voltage-gated sodium channel expression in vivo. Prostate Cancer Prostatic Dis. 2005; 8(3):266-73. Epub 2005/08/10. 4500796 [pii] doi: 10.1038/sj.pcan.4500796 PMID: 16088330.
16. Fraser SP, Diss JK, Chioni AM, Mycielska ME, Pan H, Yamaci RF, et al. Voltage-gated sodium channel expression and potentiation of human breast cancer metastasis. Clin Cancer Res. 2005; 11(15):5381-9. Epub 2005/08/03. 11/15/5381 [pii] doi: 10.1158/1078-0432.CCR-05-0327 PMID: 16061851.
17. Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol Rev. 2005; 85(2):757-810. Epub 2005/03/25. 85/2/757 [pii] doi: 10.1152/physrev.00057.2003 PMID: 15788710.
18. Wang P, Zhang C, Yu P, Tang B, Liu T, Cui H, et al. Regulation of colon cancer cell migration and invasion by CLIC1-mediated RVD. Mol Cell Biochem. 2012; 365(1-2):313-21. Epub 2012/03/20. doi:10.1007/s11010-012-1271-5 PMID: 22426742.
19. Xu B, Jin X, Min L, Li Q, Deng L, Wu H, et al. Chloride channel-3 promotes tumor metastasis by regulating membrane ruffling and is associated with poor survival. Oncotarget. 2014. Epub 2014/12/30. 2966 [pii]. PMID: 25537517.
20. Kerrigan MJ, Hall AC. Control of chondrocyte regulatory volume decrease (RVD) by [Ca2+]i and cell shape. Osteoarthritis Cartilage. 2008; 16(3):312-22. Epub 2007/09/15. S1063-4584(07)00256-7 [pii] doi: 10.1016/j.joca.2007.07.006 PMID: 17855127.
21. Kim TH, Kim JS, Kim ZH, Huang RB, Chae YL, Wang RS. Khz (Fusion Product of Ganoderma lucidum and Polyporus umbellatus Mycelia) Induces Apoptosis in Human Colon Carcinoma HCT116 Cells, Accompanied by an Increase in Reactive Oxygen Species, Activation of Caspase 3, and Increased Intracellular Ca. J Med Food. 2014. Epub 2014/12/10. doi:10.1089/jmf.2013.3135 PMID: 25489715.
22. Huang F, Wong X, Jan LY. International Union of Basic and Clinical Pharmacology. LXXXV: calciumactivated chloride channels. Pharmacol Rev. 2012; 64(1):1-15. Epub 2011/11/18. doi:10.1124/pr.111.005009 [pii]. PMID: 22090471; PubMed Central PMCID: PMC3250081.
23. Hartzell C, Putzier I, Arreola J. Calcium-activated chloride channels. Annu Rev Physiol. 2005; 67:719-58. Epub 2005/02/16. doi:10.1146/annurev.physiol.67.032003.154341 PMID: 15709976.
24. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science. 2008; 322(5901):590-4. Epub 2008/09/06. doi:10.1126/science.1163518 [pii]. PMID: 18772398.
25. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, et al. TMEM16A confers receptor-activated calcium- dependent chloride conductance. Nature. 2008; 455(7217):1210-5. Epub 2008/08/30. doi:10.1038/nature07313 [pii]. PMID: 18724360.
26. Schroeder BC, Cheng T, Jan YN, Jan LY. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. cell. 2008; 134(6):1019-29. Epub 2008/09/23. doi:10.1016/j.cell.2008.09.003 [pii]. PMID: 18805094; PubMed Central PMCID: PMC2651354.
27. Huang X, Gollin SM, Raja S, Godfrey TE. 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 U S A. 2002; 99(17):11369-74. Epub 2002/08/13. doi:10.1073/pnas.172285799 [pii]. PMID: 12172009; PubMed Central PMCID: PMC123263.
28. Katoh M. FLJ10261 gene, located within the CCND1-EMS1 locus on human chromosome 11q13, encodes the eight-transmembrane protein homologous to C12orf3, C11orf25 and FLJ34272 gene products. Int J Oncol. 2003; 22(6):1375-81. Epub 2003/05/10. PMID: 12739008.
29. Schwab M. Amplification of oncogenes in human cancer cells. Bioessays. 1998; 20(6):473-9. Epub 1998/08/12. doi:10.1002/(SICI)1521-1878(199806)20:6〈473::AID-BIES5〉3.0.CO;2-N [pii]. PMID: 9699459.
30. Britschgi A, Bill A, Brinkhaus H, Rothwell C, Clay I, Duss S, et al. Calcium-activated chloride channel ANO1 promotes breast cancer progression by activating EGFR and CAMK signaling. Proceedings of the National Academy of Sciences. 2013; 110(11):E1026-E34.
31. Ubby I, Bussani E, Colonna A, Stacul G, Locatelli M, Scudieri P, et al. TMEM16A alternative splicing coordination in breast cancer. Mol Cancer. 2013; 12:75. Epub 2013/07/20. doi:10.1186/1476-4598-12-75 [pii]. PMID: 23866066; PubMed Central PMCID: PMC3728142.
32. Sauter DR, Novak I, Pedersen SF, Larsen EH, Hoffmann EK. ANO1 (TMEM16A) in pancreatic ductal adenocarcinoma (PDAC). Pflugers Arch. 2014. Epub 2014/08/29. doi:10.1007/s00424-014-1598-8 PMID: 25163766.
33. Liu W, Lu M, Liu B, Huang Y, Wang K. Inhibition of Ca(2+)-activated Cl(-) channel ANO1/TMEM16A expression suppresses tumor growth and invasiveness in human prostate carcinoma. Cancer Lett. 2012; 326(1):41-51. Epub 2012/07/24. doi:10.1016/j.canlet.2012.07.015 S0304-3835(12)00413-2 [pii]. PMID: 22820160.
34. Ruiz C, Martins JR, Rudin F, Schneider S, Dietsche T, Fischer CA, et al. Enhanced expression of ANO1 in head and neck squamous cell carcinoma causes cell migration and correlates with poor prognosis. PLoS One. 2012; 7(8):e43265. Epub 2012/08/23. doi:10.1371/journal.pone.0043265 PONE-D-12-13954 [pii]. PMID: 22912841; PubMed Central PMCID: PMC3422276.
35. Berglund E, Akcakaya P, Berglund D, Karlsson F, Vukojevic V, Lee L, et al. Functional role of the Caactivated Cl channel DOG1/TMEM16A in gastrointestinal stromal tumor cells. Exp Cell Res. 2014. Epub 2014/05/16. S0014-4827(14)00194-3 [pii] doi: 10.1016/j.yexcr.2014.05.003 PMID: 24825187.
36. Mazzone A, Eisenman ST, Strege PR, Yao Z, Ordog T, Gibbons SJ, et al. Inhibition of cell proliferation by a selective inhibitor of the Ca(2+)-activated Cl(-) channel, Ano1. Biochem Biophys Res Commun. 2012; 427(2):248-53. Epub 2012/09/22. doi:10.1016/j.bbrc.2012.09.022 S0006-291X(12)01762-7 [pii]. PMID: 22995309; PubMed Central PMCID: PMC3479349.
37. Duvvuri U, Shiwarski DJ, Xiao D, Bertrand C, Huang X, Edinger RS, et al. TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression. Cancer Res. 2012; 72(13):3270-81. Epub 2012/05/09. doi:10.1158/0008-5472.CAN-12-0475-T [pii]. PMID: 22564524; PubMed Central PMCID: PMC3694774.
38. Wanitchakool P, Wolf L, Koehl GE, Sirianant L, Schreiber R, Kulkarni S, et al. Role of anoctamins in cancer and apoptosis. Philos Trans R Soc Lond B Biol Sci. 2014; 369(1638):20130096. Epub 2014/02/ 05. doi:10.1098/rstb.2013.0096 [pii]. PMID: 24493744; PubMed Central PMCID: PMC3917350.
39. Perez-Cornejo P, Gokhale A, Duran C, Cui Y, Xiao Q, Hartzell HC, et al. Anoctamin 1 (Tmem16A) Ca2 +-activated chloride channel stoichiometrically interacts with an ezrin-radixin-moesin network. Proc Natl Acad Sci U S A. 2012; 109(26):10376-81. Epub 2012/06/12. doi:10.1073/pnas.1200174109 [pii]. PMID: 22685202; PubMed Central PMCID: PMC3387097.
40. Bill A, Gutierrez A, Kulkarni S, Kemp C, Bonenfant D, Voshol H, et al. ANO1 interacts with EGFR and correlates with sensitivity to EGFR-targeting therapy in head and neck cancer. Oncotarget. 2015; 6 (11):9173-88. Epub 2015/04/01. 3277 [pii]. PMID: 25823819; PubMed Central PMCID: PMC4496210.
41. Sui Y, Sun M, Wu F, Yang L, Di W, Zhang G, et al. Inhibition of TMEM16A Expression Suppresses Growth and Invasion in Human Colorectal Cancer Cells. PloS one. 2014; 9(12):e115443. Epub 2014/ 12/30. doi:10.1371/journal.pone.0115443 [pii]. PMID: 25541940; PubMed Central PMCID: PMC4277312.
42. West RB, Corless CL, Chen X, Rubin BP, Subramanian S, Montgomery K, et al. The novel marker, DOG1, is expressed ubiquitously in gastrointestinal stromal tumors irrespective of KIT or PDGFRA mutation status. American Journal of Pathology. 2004; 165(1):107-13. ISI:000222216000010. PMID: 15215166
43. Carles A, Millon R, Cromer A, Ganguli G, Lemaire F, Young J, et al. Head and neck squamous cell carcinoma transcriptome analysis by comprehensive validated differential display. Oncogene. 2006; 25 (12):1821-31. Epub 2005/11/02. 1209203 [pii] doi: 10.1038/sj.onc.1209203 PMID: 16261155.
44. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013; 63(1):11-30. Epub 2013/01/22. doi:10.3322/caac.21166 PMID: 23335087.
45. Wright JC. Update in cancer chemotherapy, Part III: Lung cancer, Part 1. J Natl Med Assoc. 1985; 77 (10):815-27. Epub 1985/10/01. PMID: 2414458; PubMed Central PMCID: PMC2571176.
46. Santos-Martinez MJ, Curull V, Blanco ML, Macia F, Mojal S, Vila J, et al. [Lung cancer at a university hospital: epidemiological and histological characteristics of a recent and a historical series]. Arch Bronconeumol. 2005; 41(6):307-12. Epub 2005/07/02. 13075998 [pii]. PMID: 15989887
47. Rowell NP, Williams CJ. Radical radiotherapy for stage I/II non-small cell lung cancer in patients not sufficiently fit for or declining surgery (medically inoperable): a systematic review. Thorax. 2001; 56 (8):628-38. Epub 2001/07/20. PMID: 11462066; PubMed Central PMCID: PMC1746110.
48. Huang F, Zhang H, Wu M, Yang H, Kudo M, Peters CJ, et al. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc Natl Acad Sci U S A. 2012; 109(40):16354-9. Epub 2012/09/19. doi:10.1073/pnas.1214596109 [pii]. PMID: 22988107; PubMed Central PMCID: PMC3479591.
49. Fan WD, Zhang XQ, Guo HL, Zeng WW, Zhang N, Wan QQ, et al. Bioinformatics analysis reveals connection of squamous cell carcinoma and adenocarcinoma of the lung. Asian Pacific journal of cancer prevention: APJCP. 2012; 13(4):1477-82. PMID: 22799351.
50. Forrest AS, Joyce TC, Huebner ML, Ayon RJ, Wiwchar M, Joyce J, et al. Increased TMEM16Aencoded calcium-activated chloride channel activity is associated with pulmonary hypertension. Am J Physiol Cell Physiol. 2012; 303(12):C1229-43. Epub 2012/10/05. doi:10.1152/ajpcell.00044.2012 [pii]. PMID: 23034390; PubMed Central PMCID: PMC3532492.
51. Akervall JA, Jin Y, Wennerberg JP, Zatterstrom UK, Kjellen E, Mertens F, et al. Chromosomal abnormalities involving 11q13 are associated with poor prognosis in patients with squamous cell carcinoma of the head and neck. Cancer. 1995; 76(5):853-9. Epub 1995/09/01. PMID: 8625189.
52. Huang X, Godfrey TE, Gooding WE, McCarty KS Jr, Gollin SM. Comprehensive genome and transcriptome analysis of the 11q13 amplicon in human oral cancer and synteny to the 7F5 amplicon in murine oral carcinoma. Genes Chromosomes Cancer. 2006; 45(11):1058-69. Epub 2006/08/15. doi:10.1002/gcc.20371 PMID: 16906560.
53. Malumbres M, Barbacid M. To cycle or not to cycle: a critical decision in cancer. Nat Rev Cancer. 2001; 1(3):222-31. Epub 2002/03/21. doi:10.1038/35106065 PMID: 11902577.
54. Malumbres M, Barbacid M. Is Cyclin D1-CDK4 kinase a bona fide cancer target? Cancer Cell. 2006; 9 (1):2-4. Epub 2006/01/18. S1535-6108(05)00402-2 [pii] doi: 10.1016/j.ccr.2005.12.026 PMID: 16413464.