Secreted CLCA1 modulates TMEM16A to activate Ca2+-dependent chloride currents in human cells

eLife

Volumn 2015, Issue 4, 2015, Pages

  Sala Rabanal, Monica ^a   Yurtsever, Zeynep ^a   Nichols, Colin G ^a   Brett, Tom J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED CHLORIDE CHANNEL; CALCIUM ION; PHYCOERYTHRIN; PROTEIN; SMALL INTERFERING RNA; STREPTAVIDIN; TMEM16A PROTEIN; UNCLASSIFIED DRUG; ANO1 PROTEIN, HUMAN; CALCIUM; CHLORIDE; CHLORIDE CHANNEL; CLCA1 PROTEIN, HUMAN; PROTEIN BINDING; TUMOR PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; BIOTINYLATION; CHLORIDE CURRENT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FLOW CYTOMETRY; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING; WHOLE CELL PATCH CLAMP; CELL MEMBRANE; CHANNEL GATING; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; MEMBRANE POTENTIAL; METABOLISM; PARACRINE SIGNALING; PATCH CLAMP TECHNIQUE; RNA INTERFERENCE;

BLOTTING, WESTERN; CALCIUM; CELL MEMBRANE; CHLORIDE CHANNELS; CHLORIDES; HEK293 CELLS; HUMANS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MICROSCOPY, CONFOCAL; NEOPLASM PROTEINS; PARACRINE COMMUNICATION; PATCH-CLAMP TECHNIQUES; PROTEIN BINDING; RNA INTERFERENCE;

EID: 84925003751     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05875     Document Type: Article

References (41)

1. Alevy YG, Patel AC, Romero AG, Patel DA, Tucker J, Roswit WT, Miller CA, Heier RF, Byers DE, Brett TJ, Holtzman MJ. 2012. IL-13-induced airway mucus production is attenuated by MAPK13 inhibition. The Journal of Clinical Investigation 122:4555–4568. doi: 10.1172/JCI64896.
2. Altman JD, Moss PA, Goulder PJ, Barouch DH, Mcheyzer-Williams MG, Bell JI, Mcmichael AJ, Davis MM. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274:94–96. doi: 10.1126/science.274.5284.94.
3. Aricescu AR, Lu W, Jones EY. 2006. A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallographica Section D, Biological Crystallography 62:1243–1250. doi: 10.1107/ S0907444906029799.
4. Britton FC, Ohya S, Horowitz B, Greenwood IA. 2002. Comparison of the properties of CLCA1 generated currents and I(Cl(Ca)) in murine portal vein smooth muscle cells. The Journal of Physiology 539:107–117. doi: 10.1113/ jphysiol.2001.013170.
5. Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJ. 2008. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322:590–594. doi: 10.1126/science.1163518.
6. Cunningham SA, Awayda MS, Bubien JK, Ismailov II, Arrate MP, Berdiev BK, Benos DJ, Fuller CM. 1995. Cloning of an epithelial chloride channel from bovine trachea. The Journal of Biological Chemistry 270:31016–31026. doi: 10.1074/jbc.270.52.31016.
7. Duran C, Qu Z, Osunkoya AO, Cui Y, Hartzell HC. 2012. ANOs 3-7 in the anoctamin/Tmem16 Cl- channel family are intracellular proteins. American Journal of Physiology Cell Physiology 302:C482–C493. doi: 10.1152/ajpcell. 00140.2011.
8. Dutertre M, Lacroix-Triki M, Driouch K, de La Grange P, Gratadou L, Beck S, Millevoi S, Tazi J, Lidereau R, Vagner S, Auboeuf D. 2010. Exon-based clustering of murine breast tumor transcriptomes reveals alternative exons whose expression is associated with metastasis. Cancer Research 70:896–905. doi: 10.1158/0008-5472.CAN-09-2703.
9. Duvvuri U, Shiwarski DJ, Xiao D, Bertrand C, Huang X, Edinger RS, Rock JR, Harfe BD, Henson BJ, Kunzelmann K, Schreiber R, Seethala RS, Egloff AM, Chen X, Lui VW, Grandis JR, Gollin SM. 2012. TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression. Cancer Research 72:3270–3281. doi: 10.1158/ 0008-5472.CAN-12-0475-T.
10. Elble RC, Ji G, Nehrke K, DeBiasio J, Kingsley PD, Kotlikoff MI, Pauli BU. 2002. Molecular and functional characterization of a murine calcium-activated chloride channel expressed in smooth muscle. The Journal of Biological Chemistry 277:18586–18591. doi: 10.1074/jbc.M200829200.
11. Fallah G, Romer T, Detro-Dassen S, Braam U, Markwardt F, Schmalzing G. 2011. TMEM16A(a)/anoctamin-1 shares a homodimeric architecture with CLC chloride channels. Molecular & Cellular Proteomics 10:M110.004697. doi: 10.1074/mcp.M110.004697.
12. Gandhi R, Elble RC, Gruber AD, Schreur KD, Ji HL, Fuller CM, Pauli BU. 1998. Molecular and functional characterization of a calcium-sensitive chloride channel from mouse lung. The Journal of Biological Chemistry 273:32096–32101. doi: 10.1074/jbc.273.48.32096.
13. Gibson A, Lewis AP, Affleck K, Aitken AJ, Meldrum E, Thompson N. 2005. hCLCA1 and mCLCA3 are secreted nonintegral membrane proteins and therefore are not ion channels. The Journal of Biological Chemistry 280: 27205–27212. doi: 10.1074/jbc.M504654200.
14. Greenwood IA, Miller LJ, Ohya S, Horowitz B. 2002. The large conductance potassium channel beta-subunit can interact with and modulate the functional properties of a calcium-activated chloride channel, CLCA1. The Journal of Biological Chemistry 277:22119–22122. doi: 10.1074/jbc.C200215200.
15. Hamann M, Gibson A, Davies N, Jowett A, Walhin JP, Partington L, Affleck K, Trezise D, Main M. 2009. Human ClCa1 modulates anionic conduction of calcium-dependent chloride currents. The Journal of Physiology 587: 2255–2274. doi: 10.1113/jphysiol.2009.170159.
16. Huang F, Zhang H, Wu M, Yang H, Kudo M, Peters CJ, Woodruff PG, Solberg OD, Donne ML, Huang X, Sheppard D, Fahy JV, Wolters PJ, Hogan BL, Finkbeiner WE, Li M, Jan YN, Jan LY, Rock JR. 2012. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proceedings of the National Academy of Sciences of USA 109:16354–16359. doi: 10.1073/pnas.1214596109.
17. Jeong SM, Park HK, Yoon IS, Lee JH, Kim JH, Jang CG, Lee CJ, Nah SY. 2005. Cloning and expression of Ca2+ -activated chloride channel from rat brain. Biochemical and Biophysical Research Communications 334:569–576. doi: 10.1016/j.bbrc.2005.06.122.
18. Kunzelmann K, Kongsuphol P, Aldehni F, Tian Y, Ousingsawat J, Warth R, Schreiber R. 2009. Bestrophin and TMEM16-Ca(2+) activated Cl(-) channels with different functions. Cell Calcium 46:233–241. doi: 10.1016/j.ceca. 2009.09.003.
19. Liu W, Lu M, Liu B, Huang Y, Wang K. 2012. Inhibition of Ca(2+)-activated Cl(-) channel ANO1/TMEM16A expression suppresses tumor growth and invasiveness in human prostate carcinoma. Cancer Letters 326:41–51. doi: 10.1016/j.canlet.2012.07.015.
20. Patel AC, Brett TJ, Holtzman MJ. 2009. The role of CLCA proteins in inflammatory airway disease. Annual Review of Physiology 71:425–449. doi: 10.1146/annurev.physiol.010908.163253.
21. Pedemonte N, Galietta LJ. 2014. Structure and function of TMEM16 proteins (anoctamins). Physiological Reviews 94:419–459. doi: 10.1152/physrev.00039.2011.
22. Perez-Cornejo P, Gokhale A, Duran C, Cui Y, Xiao Q, Hartzell HC, Faundez V. 2012. Anoctamin 1 (Tmem16A) Ca2+ -activated chloride channel stoichiometrically interacts with an ezrin-radixin-moesin network. Proceedings of the National Academy of Sciences of USA 109:10376–10381. doi: 10.1073/pnas.1200174109.
23. Pritchard HA, Leblanc N, Albert AP, Greenwood IA. 2014. Inhibitory role of phosphatidylinositol 4,5 bisphosphate on TMEM16A encoded calcium-activated chloride channels in rat pulmonary artery. British Journal of Pharmacology 171:4311–4321. doi: 10.1111/bph.12778.
24. Qu Z, Yao W, Yao R, Liu X, Yu K, Hartzell C. 2014. The Ca(2+) -activated Cl(-) channel, ANO1 (TMEM16A), is a double-edged sword in cell proliferation and tumorigenesis. Cancer Medicine 3:453–461. doi: 10.1002/cam4. 232.
25. Sasaki Y, Koyama R, Maruyama R, Hirano T, Tamura M, Sugisaka J, Suzuki H, Idogawa M, Shinomura Y, Tokino T. 2012. CLCA2, a target of the p53 family, negatively regulates cancer cell migration and invasion. Cancer Biology & Therapy 13:1512–1521. doi: 10.4161/cbt.22280.
26. Schroeder BC, Cheng T, Jan YN, Jan LY. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019–1029. doi: 10.1016/j.cell.2008.09.003.
27. Scudieri P, Caci E, Bruno S, Ferrera L, Schiavon M, Sondo E, Tomati V, Gianotti A, Zegarra-Moran O, Pedemonte N, Rea F, Ravazzolo R, Galietta LJ. 2012. Association of TMEM16A chloride channel overexpression with airway goblet cell metaplasia. The Journal of Physiology 590:6141–6155. doi: 10.1113/jphysiol.2012.240838.
28. Sheridan JT, Worthington EN, Yu K, Gabriel SE, Hartzell HC, Tarran R. 2011. Characterization of the oligomeric structure of the Ca(2+)-activated Cl- channel Ano1/TMEM16A. The Journal of Biological Chemistry 286: 1381–1388. doi: 10.1074/jbc.M110.174847.
29. Terashima H, Picollo A, Accardi A. 2013. Purified TMEM16A is sufficient to form Ca2+-activated Cl- channels. Proceedings of the National Academy of Sciences of USA 110:19354–19359. doi: 10.1073/pnas.1312014110.
30. Tian Y, Kongsuphol P, Hug M, Ousingsawat J, Witzgall R, Schreiber R, Kunzelmann K. 2011. Calmodulin-dependent activation of the epithelial calcium-dependent chloride channel TMEM16A. FASEB Journal 25:1058–1068. doi: 10.1096/fj.10-166884.
31. Tien J, Lee HY, Minor DL Jr, Jan YN, Jan LY. 2013. Identification of a dimerization domain in the TMEM16A calcium-activated chloride channel (CaCC). Proceedings of the National Academy of Sciences of USA 110: 6352–6357. doi: 10.1073/pnas.1303672110.
32. van der Doef HP, Slieker MG, Staab D, Alizadeh BZ, Seia M, Colombo C, van der Ent CK, Nickel R, Witt H, Houwen RH. 2010. Association of the CLCA1 p.S357N variant with meconium ileus in European patients with cystic fibrosis. Journal of Pediatric Gastroenterology and Nutrition 50:347–349. doi: 10.1097/MPG.0b013e3181afce6c.
33. Walia V, Yu Y, Cao D, Sun M, Mclean JR, Hollier BG, Cheng J, Mani SA, Rao K, Premkumar L, Elble RC. 2012. Loss of breast epithelial marker hCLCA2 promotes epithelial-to-mesenchymal transition and indicates higher risk of metastasis. Oncogene 31:2237–2246. doi: 10.1038/onc.2011.392.
34. West RB, Corless CL, Chen X, Rubin BP, Subramanian S, Montgomery K, Zhu S, Ball CA, Nielsen TO, Patel R, Goldblum JR, Brown PO, Heinrich MC, van de Rijn M. 2004. The novel marker, DOG1, is expressed ubiquitously in gastrointestinal stromal tumors irrespective of KIT or PDGFRA mutation status. The American Journal of Pathology 165:107–113. doi: 10.1016/S0002-9440(10)63279-8.
35. Xiao Q, Yu K, Perez-Cornejo P, Cui Y, Arreola J, Hartzell HC. 2011. Voltage- and calcium-dependent gating of TMEM16A/Ano1 chloride channels are physically coupled by the first intracellular loop. Proceedings of the National Academy of Sciences of USA 108:8891–8896. doi: 10.1073/pnas.1102147108.
36. Yamazaki J, Okamura K, Ishibashi K, Kitamura K. 2005. Characterization of CLCA protein expressed in ductal cells of rat salivary glands. Biochimica Et Biophysica Acta 1715:132–144. doi: 10.1016/j.bbamem.2005.08.001.
37. Yang B, Cao L, Liu B, McCaig CD, Pu J. 2013. The transition from proliferation to differentiation in colorectal cancer is regulated by the calcium activated chloride channel A1. PLOS ONE 8:e60861. doi: 10.1371/journal.pone. 0060861.
38. Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim WS, Park SP, Lee J, Lee B, Kim BM, Raouf R, Shin YK, Oh U. 2008. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210–1215. doi: 10. 1038/nature07313.
39. Young FD, Newbigging S, Choi C, Keet M, Kent G, Rozmahel RF. 2007. Amelioration of cystic fibrosis intestinal mucous disease in mice by restoration of mCLCA3. Gastroenterology 133:1928–1937. doi: 10.1053/j.gastro. 2007.10.007.
40. Yu Y, Walia V, Elble RC. 2013. Loss of CLCA4 promotes epithelial-to-mesenchymal transition in breast cancer cells. PLOS ONE 8:e83943. doi: 10.1371/journal.pone.0083943.
41. Yurtsever Z, Sala-Rabanal M, Randolph DT, Scheaffer SM, Roswit WT, Alevy YG, Patel AC, Heier RF, Romero AG, Nichols CG, Holtzman MJ, Brett TJ. 2012. Self-cleavage of human CLCA1 protein by a novel internal metalloprotease domain controls calcium-activated chloride channel activation. The Journal of Biological Chemistry 287:42138–42149. doi: 10.1074/jbc.M112.410282.