دورية أكاديمية
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Structure and Function of Calcium-Activated Chloride Channels and Phospholipid Scramblases in the TMEM16 Family.

التفاصيل البيبلوغرافية
العنوان: Structure and Function of Calcium-Activated Chloride Channels and Phospholipid Scramblases in the TMEM16 Family.
المؤلفون: Nguyen DM; Center for Neuroscience, University of California, Davis, CA, USA. dunguyen@som.umaryland.edu.; Department of Physiology, University of Maryland School of Medicine, Baltimore, MD, USA. dunguyen@som.umaryland.edu., Chen TY; Department of Neurology, Center for Neuroscience, University of California, Davis, CA, USA. tycchen@ucdavis.edu.
المصدر: Handbook of experimental pharmacology [Handb Exp Pharmacol] 2024; Vol. 283, pp. 153-180.
نوع المنشور: Review; Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 7902231 Publication Model: Print Cited Medium: Print ISSN: 0171-2004 (Print) Linking ISSN: 01712004 NLM ISO Abbreviation: Handb Exp Pharmacol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Berlin, New York, Springer-Verlag.
مواضيع طبية MeSH: Chloride Channels*/chemistry , Chloride Channels*/metabolism , Phospholipid Transfer Proteins*/metabolism, Humans ; Animals ; Anoctamins/metabolism ; Ion Transport ; Phospholipids/metabolism ; Calcium/chemistry ; Mammals/metabolism
مستخلص: The transmembrane protein 16 (TMEM16) family consists of Ca 2+ -activated chloride channels and phospholipid scramblases. Ten mammalian TMEM16 proteins, TMEM16A-K (with no TMEM16I), and several non-mammalian TMEM16 proteins, such as afTMEM16 and nhTMEM16, have been discovered. All known TMEM16 proteins are homodimeric proteins containing two subunits. Each subunit consists of ten transmembrane helices with Ca 2+ -binding sites and a single ion-permeation/phospholipid transport pathway. The ion-permeation pathway and the phospholipid transport pathway of TMEM16 proteins have a wide intracellular vestibule, a narrow neck, and a smaller extracellular vestibule. Interestingly, the lining wall of the ion-permeation/phospholipid transport pathway may be formed, at least partially, by membrane phospholipids, though the degree of pore-wall forming by phospholipids likely varies among TMEM16 proteins. Thus, the biophysical properties and activation mechanisms of TMEM16 proteins could differ from each other accordingly. Here we review the current understanding of the structure and function of TMEM16 molecules.
(© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.)
References: 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. J Clin Invest 122:4555–4568. https://doi.org/10.1172/JCI64896. (PMID: 10.1172/JCI64896231871303533556)
Alvadia C, Lim NK, Clerico Mosina V, Oostergetel GT, Dutzler R, Paulino C (2019) Cryo-EM structures and functional characterization of the murine lipid scramblase TMEM16F. Elife 8:e44365. https://doi.org/10.7554/eLife.44365. (PMID: 10.7554/eLife.44365307853996414204)
Arreola J, Perez-Cornejo P, Segura-Covarrubias G, Corral-Fernandez N, Leon-Aparicio D, Guzman-Hernandez ML (2022) Function and regulation of the calcium-activated chloride channel anoctamin 1 (TMEM16A). In: Fahlke C (ed) Anion channels. Accompanying Chapter.
Berry KN, Brett TJ (2020) Structural and biophysical analysis of the CLCA1 VWA domain suggests mode of TMEM16A engagement. Cell Rep 30:1141–1151.e3. https://doi.org/10.1016/j.celrep.2019.12.059. (PMID: 10.1016/j.celrep.2019.12.059319957327050472)
Bethel NP, Grabe M (2016) Atomistic insight into lipid translocation by a TMEM16 scramblase. Proc Natl Acad Sci U S A 113:14049–14054. https://doi.org/10.1073/pnas.1607574113. (PMID: 10.1073/pnas.1607574113278723085150362)
Betto G, Cherian OL, Pifferi S, Cenedese V, Boccaccio A, Menini A (2014) Interactions between permeation and gating in the TMEM16B/anoctamin2 calcium-activated chloride channel. J Gen Physiol 143:703–718. https://doi.org/10.1085/jgp.201411182. (PMID: 10.1085/jgp.201411182248639314035747)
Bill A, Popa MO, van Diepen MT, Gutierrez A, Lilley S, Velkova M, Acheson K, Choudhury H, Renaud NA, Auld DS, Gosling M, Groot-Kormelink PJ, Gaither LA (2015) Variomics screen identifies the re-entrant loop of the calcium-activated chloride channel ANO1 that facilitates channel activation. J Biol Chem 290:889–903. https://doi.org/10.1074/jbc.M114.618140. (PMID: 10.1074/jbc.M114.61814025425649)
Boedtkjer DM, Kim S, Jensen AB, Matchkov VM, Andersson KE (2015) New selective inhibitors of calcium-activated chloride channels – T16A inh -A01, CaCC inh -A01 and MONNA – what do they inhibit? Br J Pharmacol 172:4158–4172. https://doi.org/10.1111/bph.13201. (PMID: 10.1111/bph.13201260139954543620)
Brett TJ (2015) CLCA1 and TMEM16A: the link towards a potential cure for airway diseases. Expert Rev Respir Med 9:503–506. https://doi.org/10.1586/17476348.2015.1081064. (PMID: 10.1586/17476348.2015.1081064262960944829067)
Brunner JD, Lim NK, Schenck S, Duerst A, Dutzler R (2014) X-ray structure of a calcium-activated TMEM16 lipid scramblase. Nature 516:207–212. https://doi.org/10.1038/nature13984. (PMID: 10.1038/nature1398425383531)
Bushell SR, Pike ACW, Falzone ME, Rorsman NJG, Ta CM, Corey RA, Newport TD, Christianson JC, Scofano LF, Shintre CA, Tessitore A, Chu A, Wang Q, Shrestha L, Mukhopadhyay SMM, Love JD, Burgess-Brown NA, Sitsapesan R, Stansfeld PJ, Huiskonen JT, Tammaro P, Accardi A, Carpenter EP (2019) The structural basis of lipid scrambling and inactivation in the endoplasmic reticulum scramblase TMEM16K. Nat Commun 10:3956. https://doi.org/10.1038/s41467-019-11753-1. (PMID: 10.1038/s41467-019-11753-1314776916718402)
Cabrita I, Benedetto R, Schreiber R, Kunzelmann K (2019) Niclosamide repurposed for the treatment of inflammatory airway disease. JCI Insight:4. https://doi.org/10.1172/jci.insight.128414.
Caputo A, Caci E, Ferrera L, Pedemonte N, Barsanti C, Sondo E, Pfeffer U, Ravazzolo R, Zegarra-Moran O, Galietta LJV (2008) TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science 322:590–594. https://doi.org/10.1126/science.1163518. (PMID: 10.1126/science.116351818772398)
Cenedese V, Betto G, Celsi F, Cherian OL, Pifferi S, Menini A (2012) The voltage dependence of the TMEM16B/anoctamin2 calcium-activated chloride channel is modified by mutations in the first putative intracellular loop. J Gen Physiol 139:285–294. https://doi.org/10.1085/jgp.201110764. (PMID: 10.1085/jgp.201110764224121913315145)
Centeio R, Cabrita I, Benedetto R, Talbi K, Ousingsawat J, Schreiber R, Sullivan JK, Kunzelmann K (2020) Pharmacological inhibition and activation of the Ca2+ activated cl− channel TMEM16A. Int J Mol Sci 21:2557. (PMID: 10.3390/ijms21072557322726867177308)
Chao AC, Mochizuki H (1992) Niflumic and flufenamic acids are potent inhibitors of chloride secretion in mammalian airway. Life Sci 51:1453–1457. https://doi.org/10.1016/0024-3205(92)90540-6. (PMID: 10.1016/0024-3205(92)90540-61383667)
Cherian OL, Menini A, Boccaccio A (2015) Multiple effects of anthracene-9-carboxylic acid on the TMEM16B/anoctamin2 calcium-activated chloride channel. Biochim Biophys Acta Biomembr 1848:1005–1013. https://doi.org/10.1016/j.bbamem.2015.01.009. (PMID: 10.1016/j.bbamem.2015.01.009)
Contreras-Vite JA, Cruz-Rangel S, De Jesús-Pérez JJ, Figueroa IAA, Rodríguez-Menchaca AA, Pérez-Cornejo P, Hartzell HC, Arreola J (2016) Revealing the activation pathway for TMEM16A chloride channels from macroscopic currents and kinetic models. Pflugers Arch 468:1241–1257. https://doi.org/10.1007/s00424-016-1830-9. (PMID: 10.1007/s00424-016-1830-9271381675556394)
Dai L, Garg V, Sanguinetti MC (2010) Activation of Slo2.1 channels by niflumic acid. J Gen Physiol 135:275–295. https://doi.org/10.1085/jgp.200910316. (PMID: 10.1085/jgp.200910316201768552828905)
Danahay HL, Lilley S, Fox R, Charlton H, Sabater J, Button B, McCarthy C, Collingwood SP, Gosling M (2020) TMEM16A potentiation: a novel therapeutic approach for the treatment of cystic fibrosis. Am J Respir Crit Care Med 201:946–954. https://doi.org/10.1164/rccm.201908-1641OC. (PMID: 10.1164/rccm.201908-1641OC318989117159426)
Dang S, Feng S, Tien J, Peters CJ, Bulkley D, Lolicato M, Zhao J, Zuberbühler K, Ye W, Qi L, Chen T, Craik CS, Jan YN, Minor DL, Cheng Y, Jan LY (2017) Cryo-EM structures of the TMEM16A calcium-activated chloride channel. Nature 552:426–429. https://doi.org/10.1038/nature25024. (PMID: 10.1038/nature25024292366845750132)
Das S, Hahn Y, Walker DA, Nagata S, Willingham MC, Peehl DM, Bera TK, Lee B, Pastan I (2008) Topology of NGEP, a prostate-specific cell:cell junction protein widely expressed in many cancers of different grade level. Cancer Res 68:6306. https://doi.org/10.1158/0008-5472.CAN-08-0870. (PMID: 10.1158/0008-5472.CAN-08-0870186768552562772)
De Jesús-Pérez JJ, Cruz-Rangel S, Espino-Saldaña ÁE, Martínez-Torres A, Qu Z, Hartzell HC, Corral-Fernandez NE, Pérez-Cornejo P, Arreola J (2018) Phosphatidylinositol 4,5-bisphosphate, cholesterol, and fatty acids modulate the calcium-activated chloride channel TMEM16A (ANO1). Biochim Biophys Acta Mol Cell Biol Lipids 1863:299–312. https://doi.org/10.1016/j.bbalip.2017.12.009. (PMID: 10.1016/j.bbalip.2017.12.00929277655)
Di Zanni E, Gradogna A, Scholz-Starke J, Boccaccio A (2018) Gain of function of TMEM16E/ANO5 scrambling activity caused by a mutation associated with gnathodiaphyseal dysplasia. Cell Mol Life Sci 75:1657–1670. https://doi.org/10.1007/s00018-017-2704-9. (PMID: 10.1007/s00018-017-2704-929124309)
Fallah G, Römer T, Detro-Dassen S, Braam U, Markwardt F, Schmalzing G (2011) TMEM16A(a)/anoctamin-1 shares a homodimeric architecture with CLC chloride channels. Mol Cell Proteomics 10:M110.004697. https://doi.org/10.1074/mcp.M110.004697. (PMID: 10.1074/mcp.M110.00469720974900)
Falzone ME, Rheinberger J, Lee B-C, Peyear T, Sasset L, Raczkowski AM, Eng ET, Di Lorenzo A, Andersen OS, Nimigean CM, Accardi A (2019) Structural basis of Ca 2+ -dependent activation and lipid transport by a TMEM16 scramblase. Elife 8:e43229. https://doi.org/10.7554/eLife.43229. (PMID: 10.7554/eLife.43229306489726355197)
Ferrera L, Caputo A, Galietta LJ (2010) TMEM16A protein: a new identity for Ca2+-dependent Cl - channels. Physiology (Bethesda) 25:357–363. https://doi.org/10.1152/physiol.00030.2010. (PMID: 10.1152/physiol.00030.201021186280)
Ferrera L, Caputo A, Ubby I, Bussani E, Zegarra-Moran O, Ravazzolo R, Pagani F, Galietta LJV (2009) Regulation of TMEM16A chloride channel properties by alternative splicing. J Biol Chem. 284:33360–33368. https://doi.org/10.1074/jbc.M109.046607. (PMID: 10.1074/jbc.M109.046607198198742785179)
Feng S, Dang S, Han TW, Ye W, Jin P, Cheng T, Li J, Jan YN, Jan LY, Cheng Y (2019) Cryo-EM studies of TMEM16F calcium-activated ion channel suggest features important for lipid scrambling. Cell Rep 28:567–579.e4. https://doi.org/10.1016/j.celrep.2019.06.023. (PMID: 10.1016/j.celrep.2019.06.023312915896684876)
Gibson A, Lewis AP, Affleck K, Aitken AJ, Meldrum E, Thompson N (2005) hCLCA1 and mCLCA3 are secreted non-integral membrane proteins and therefore are not ion channels. J Biol Chem 280:27205–27212. https://doi.org/10.1074/jbc.M504654200. (PMID: 10.1074/jbc.M50465420015919655)
Grubb S, Poulsen KA, Juul CA, Kyed T, Klausen TK, Larsen EH, Hoffmann EK (2013) TMEM16F (Anoctamin 6), an anion channel of delayed Ca 2+ activation. J Gen Physiol 141:585–600. https://doi.org/10.1085/jgp.201210861. (PMID: 10.1085/jgp.201210861236303413639583)
Gruber AD, Elble RC, Ji HL, Schreur KD, Fuller CM, Pauli BU (1998) Genomic cloning, molecular characterization, and functional analysis of human CLCA1, the first human member of the family of Ca2+-activated Cl- channel proteins. Genomics 54:200–214. https://doi.org/10.1006/geno.1998.5562. (PMID: 10.1006/geno.1998.55629828122)
Halling DB, Liebeskind BJ, Hall AW, Aldrich RW (2016) Conserved properties of individual Ca 2+ -binding sites in calmodulin. Proc Natl Acad Sci U S A 113:E1216–E1225. https://doi.org/10.1073/pnas.1600385113. (PMID: 10.1073/pnas.1600385113268841974780646)
Hartzell C, Putzier I, Arreola J (2005) Calcium-activated chloride channels. Annu Rev Physiol 67:719–758. https://doi.org/10.1146/annurev.physiol.67.032003.154341. (PMID: 10.1146/annurev.physiol.67.032003.15434115709976)
Hogg RC, Wang Q, Large WA (1994) Action of niflumic acid on evoked and spontaneous calcium-activated chloride and potassium currents in smooth muscle cells from rabbit portal vein. Br J Pharmacol 112:977–984. https://doi.org/10.1111/j.1476-5381.1994.tb13177.x. (PMID: 10.1111/j.1476-5381.1994.tb13177.x79216281910202)
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 BLM, Finkbeiner WE, Li M, Jan Y-N, Jan LY, Rock JR (2012) Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc Natl Acad Sci U S A 109:16354–16359. https://doi.org/10.1073/pnas.1214596109. (PMID: 10.1073/pnas.1214596109229881073479591)
Jeng G, Aggarwal M, Yu W-P, Chen T-Y (2016) Independent activation of distinct pores in dimeric TMEM16A channels. J Gen Physiol 148:393–404. https://doi.org/10.1085/jgp.201611651. (PMID: 10.1085/jgp.201611651277993195089935)
Jha A, Chung WY, Vachel L, Maleth J, Lake S, Zhang G, Ahuja M, Muallem S (2019) Anoctamin 8 tethers endoplasmic reticulum and plasma membrane for assembly of Ca 2+ signaling complexes at the ER/PM compartment. EMBO J 38:e101452. https://doi.org/10.15252/embj.2018101452. (PMID: 10.15252/embj.2018101452310611736576175)
Jia Z, Chen J (2021) Specific PIP2 binding promotes calcium activation of TMEM16A chloride channels. Commun Biol 4:259. https://doi.org/10.1038/s42003-021-01782-2. (PMID: 10.1038/s42003-021-01782-2336379647910439)
Jiang T, Yu K, Hartzell HC, Tajkhorshid E (2017) Lipids and ions traverse the membrane by the same physical pathway in the nhTMEM16 scramblase. Elife 6:e28671. https://doi.org/10.7554/eLife.28671. (PMID: 10.7554/eLife.28671289170605628016)
Jung J, Nam JH, Park HW, Oh U, Yoon J-H, Lee MG (2013) Dynamic modulation of ANO1/TMEM16A HCO 3 − permeability by Ca 2+ /calmodulin. Proc Natl Acad Sci U S A 110:360–365. https://doi.org/10.1073/pnas.1211594110. (PMID: 10.1073/pnas.121159411023248295)
Jüschke C, Wächter A, Schwappach B, Seedorf M (2005) SEC18/NSF-independent, protein-sorting pathway from the yeast cortical ER to the plasma membrane. J Cell Biol 169:613–622. https://doi.org/10.1083/jcb.200503033. (PMID: 10.1083/jcb.200503033159118782171690)
Kalienkova V, Clerico Mosina V, Bryner L, Oostergetel GT, Dutzler R, Paulino C (2019) Stepwise activation mechanism of the scramblase nhTMEM16 revealed by cryo-EM. Elife 8:e44364. https://doi.org/10.7554/eLife.44364. (PMID: 10.7554/eLife.44364307853986414200)
Kim H, Kim H, Lee J, Lee B, Kim H-R, Jung J, Lee M-O, Oh U (2018) Anoctamin 9/TMEM16J is a cation channel activated by cAMP/PKA signal. Cell Calcium 71:75–85. https://doi.org/10.1016/j.ceca.2017.12.003. (PMID: 10.1016/j.ceca.2017.12.00329604966)
Kostritskii AY, Machtens J-P (2021) Molecular mechanisms of ion conduction and ion selectivity in TMEM16 lipid scramblases. Nat Commun 12:2826. https://doi.org/10.1038/s41467-021-22724-w. (PMID: 10.1038/s41467-021-22724-w339905558121942)
Lam AKM, Dutzler R (2018) Calcium-dependent electrostatic control of anion access to the pore of the calcium-activated chloride channel TMEM16A. Elife 7:e39122. https://doi.org/10.7554/eLife.39122. (PMID: 10.7554/eLife.39122303119106195346)
Lam AKM, Rheinberger J, Paulino C, Dutzler R (2021) Gating the pore of the calcium-activated chloride channel TMEM16A. Nat Commun 12:785. https://doi.org/10.1038/s41467-020-20787-9. (PMID: 10.1038/s41467-020-20787-9335422237862301)
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. https://doi.org/10.1093/bioinformatics/btm404. (PMID: 10.1093/bioinformatics/btm40417846036)
Lavieu G, Orci L, Shi L, Geiling M, Ravazzola M, Wieland F, Cosson P, Rothman JE (2010) Induction of cortical endoplasmic reticulum by dimerization of a coatomer-binding peptide anchored to endoplasmic reticulum membranes. Proc Natl Acad Sci U S A 107:6876. https://doi.org/10.1073/pnas.1002536107. (PMID: 10.1073/pnas.1002536107203512642872465)
Le SC, Yang H (2020) An additional Ca 2+ binding site allosterically controls TMEM16A activation. Cell Rep 33:108570. https://doi.org/10.1016/j.celrep.2020.108570. (PMID: 10.1016/j.celrep.2020.108570333786697786149)
Le SC, Jia Z, Chen J, Yang H (2019a) Molecular basis of PIP2-dependent regulation of the Ca 2+ -activated chloride channel TMEM16A. Nat Commun 10:3769. https://doi.org/10.1038/s41467-019-11784-8. (PMID: 10.1038/s41467-019-11784-8314349066704070)
Le T, Jia Z, Le SC, Zhang Y, Chen J, Yang H (2019b) An inner activation gate controls TMEM16F phospholipid scrambling. Nat Commun 10:1846. https://doi.org/10.1038/s41467-019-09778-7. (PMID: 10.1038/s41467-019-09778-7310154646478717)
Le T, Le SC, Yang H (2019c) Drosophila subdued is a moonlighting transmembrane protein 16 (TMEM16) that transports ions and phospholipids. J Biol Chem 294:4529–4537. https://doi.org/10.1074/jbc.AC118.006530. (PMID: 10.1074/jbc.AC118.006530307005526433057)
Lee B-C, Menon Anant K, Accardi A (2016) The nhTMEM16 scramblase is also a nonselective ion channel. Biophys J 111:1919–1924. https://doi.org/10.1016/j.bpj.2016.09.032. (PMID: 10.1016/j.bpj.2016.09.032278062735103024)
Lee B-C, Khelashvili G, Falzone M, Menon AK, Weinstein H, Accardi A (2018) Gating mechanism of the extracellular entry to the lipid pathway in a TMEM16 scramblase. Nat Commun 9:3251. https://doi.org/10.1038/s41467-018-05724-1. (PMID: 10.1038/s41467-018-05724-1301082176092359)
Lentz BR (2003) Exposure of platelet membrane phosphatidylserine regulates blood coagulation. Prog Lipid Res 42:423–438. https://doi.org/10.1016/S0163-7827(03)00025-0. (PMID: 10.1016/S0163-7827(03)00025-012814644)
Liantonio A, Giannuzzi V, Picollo A, Babini E, Pusch M, Conte Camerino D (2007) Niflumic acid inhibits chloride conductance of rat skeletal muscle by directly inhibiting the CLC-1 channel and by increasing intracellular calcium. Br J Pharmacol 150:235–247. https://doi.org/10.1038/sj.bjp.0706954. (PMID: 10.1038/sj.bjp.070695417128287)
Lim NK, Lam AKM, Dutzler R (2016) Independent activation of ion conduction pores in the double-barreled calcium-activated chloride channel TMEM16A. J Gen Physiol 148:375–392. https://doi.org/10.1085/jgp.201611650. (PMID: 10.1085/jgp.201611650277993185089934)
Malvezzi M, Chalat M, Janjusevic R, Picollo A, Terashima H, Menon AK, Accardi A (2013) Ca 2+ -dependent phospholipid scrambling by a reconstituted TMEM16 ion channel. Nat Commun 4:2367. https://doi.org/10.1038/ncomms3367. (PMID: 10.1038/ncomms336723996062)
Manford Andrew G, Stefan Christopher J, Yuan Helen L, MacGurn Jason A, Emr Scott D (2012) ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Dev Cell 23:1129–1140. https://doi.org/10.1016/j.devcel.2012.11.004. (PMID: 10.1016/j.devcel.2012.11.00423237950)
Milenkovic VM, Brockmann M, Stöhr H, Weber BHF, Strauss O (2010) Evolution and functional divergence of the anoctamin family of membrane proteins. BMC Evol Biol 10:319. https://doi.org/10.1186/1471-2148-10-319. (PMID: 10.1186/1471-2148-10-319209648442974728)
Miner K, Labitzke K, Liu B, Wang P, Henckels K, Gaida K, Elliott R, Chen JJ, Liu L, Leith A, Trueblood E, Hensley K, Xia X-Z, Homann O, Bennett B, Fiorino M, Whoriskey J, Yu G, Escobar S, Wong M, Born TL, Budelsky A, Comeau M, Smith D, Phillips J, Johnston JA, McGivern JG, Weikl K, Powers D, Kunzelmann K, Mohn D, Hochheimer A, Sullivan JK (2019) Drug repurposing: the anthelmintics niclosamide and nitazoxanide are potent TMEM16A antagonists that fully bronchodilate airways. Front Pharmacol 10. https://doi.org/10.3389/fphar.2019.00051.
Namkung W, Phuan P-W, Verkman AS (2011a) TMEM16A inhibitors reveal TMEM16A as a Minor component of calcium-activated chloride channel conductance in airway and intestinal epithelial cells. J Biol Chem 286:2365–2374. https://doi.org/10.1074/jbc.M110.175109. (PMID: 10.1074/jbc.M110.17510921084298)
Namkung W, Yao Z, Finkbeiner WE, Verkman AS (2011b) Small-molecule activators of TMEM16A, a calcium-activated chloride channel, stimulate epithelial chloride secretion and intestinal contraction. FASEB J 25:4048–4062. https://doi.org/10.1096/fj.11-191627. (PMID: 10.1096/fj.11-191627218360253205834)
Nguyen DM, Chen LS, Yu W-P, Chen T-Y (2019) Comparison of ion transport determinants between a TMEM16 chloride channel and phospholipid scramblase. J Gen Physiol 151:518–531. https://doi.org/10.1085/jgp.201812270. (PMID: 10.1085/jgp.201812270306704766445582)
Nguyen DM, Chen LS, Jeng G, Yu WP, Chen TY (2020) Cobalt ion interaction with TMEM16A calcium-activated chloride channel: inhibition and potentiation. PLoS One 15:e0231812. https://doi.org/10.1371/journal.pone.0231812. (PMID: 10.1371/journal.pone.0231812323023657164836)
Nguyen DM, Kwon HC, Chen T-Y (2021) Divalent cation modulation of ion permeation in TMEM16 proteins. Int J Mol Sci 22:2209. (PMID: 10.3390/ijms22042209336722607926781)
Ni Y-L, Kuan A-S, Chen T-Y (2014) Activation and inhibition of TMEM16A calcium-activated chloride channels. PLoS One 9:e86734. https://doi.org/10.1371/journal.pone.0086734. (PMID: 10.1371/journal.pone.0086734244897803906059)
Oh S-J, Hwang SJ, Jung J, Yu K, Kim J, Choi JY, Hartzell HC, Roh EJ, Lee CJ (2013) MONNA, a potent and selective blocker for transmembrane protein with unknown function 16/Anoctamin-1. Mol Pharmacol 84:726–735. https://doi.org/10.1124/mol.113.087502. (PMID: 10.1124/mol.113.087502239971173807079)
O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, Astashyn A, Badretdin A, Bao Y, Blinkova O, Brover V, Chetvernin V, Choi J, Cox E, Ermolaeva O, Farrell CM, Goldfarb T, Gupta T, Haft D, Hatcher E, Hlavina W, Joardar VS, Kodali VK, Li W, Maglott D, Masterson P, McGarvey KM, Murphy MR, O'Neill K, Pujar S, Rangwala SH, Rausch D, Riddick LD, Schoch C, Shkeda A, Storz SS, Sun H, Thibaud-Nissen F, Tolstoy I, Tully RE, Vatsan AR, Wallin C, Webb D, Wu W, Landrum MJ, Kimchi A, Tatusova T, DiCuccio M, Kitts P, Murphy TD, Pruitt KD (2016) Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 44:D733–D745. https://doi.org/10.1093/nar/gkv1189. (PMID: 10.1093/nar/gkv118926553804)
Ottolia M, Toro L (1994) Potentiation of large conductance KCa channels by niflumic, flufenamic, and mefenamic acids. Biophys J 67:2272–2279. https://doi.org/10.1016/S0006-3495(94)80712-X. (PMID: 10.1016/S0006-3495(94)80712-X75351111225611)
Patel AC, Brett TJ, Holtzman MJ (2009) The role of CLCA proteins in inflammatory airway disease. Annu Rev Physiol 71:425–449. https://doi.org/10.1146/annurev.physiol.010908.163253. (PMID: 10.1146/annurev.physiol.010908.163253189542824017675)
Paulino C, Kalienkova V, Lam AKM, Neldner Y, Dutzler R (2017a) Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM. Nature 552:421–425. https://doi.org/10.1038/nature24652. (PMID: 10.1038/nature2465229236691)
Paulino C, Neldner Y, Lam AK, Kalienkova V, Brunner JD, Schenck S, Dutzler R (2017b) Structural basis for anion conduction in the calcium-activated chloride channel TMEM16A. Elife 6:e26232. https://doi.org/10.7554/eLife.26232. (PMID: 10.7554/eLife.26232285617335470873)
Pedemonte N, Galietta LJV (2014) Structure and function of TMEM16 proteins (Anoctamins). Physiol Rev 94:419–459. https://doi.org/10.1152/physrev.00039.2011. (PMID: 10.1152/physrev.00039.201124692353)
Pelz T, Drose DR, Fleck D, Henkel B, Ackels T, Spehr M, Neuhaus EM (2018) An ancestral TMEM16 homolog from Dictyostelium discoideum forms a scramblase. PLoS One 13:e0191219. https://doi.org/10.1371/journal.pone.0191219. (PMID: 10.1371/journal.pone.0191219294441175812556)
Peters CJ, Yu H, Tien J, Jan YN, Li M, Jan LY (2015) Four basic residues critical for the ion selectivity and pore blocker sensitivity of TMEM16A calcium-activated chloride channels. Proc Natl Acad Sci U S A 112:3547. https://doi.org/10.1073/pnas.1502291112. (PMID: 10.1073/pnas.1502291112257338974371966)
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612. https://doi.org/10.1002/jcc.20084. (PMID: 10.1002/jcc.2008415264254)
Pettersen EF, Goddard TD, Huang CC, Meng EC, Couch GS, Croll TI, Morris JH, Ferrin TE (2021) UCSF ChimeraX: structure visualization for researchers, educators, and developers. Protein Sci 30:70–82. https://doi.org/10.1002/pro.3943. (PMID: 10.1002/pro.394332881101)
Pifferi S (2017) Permeation mechanisms in the TMEM16B calcium-activated chloride channels. PLoS One 12:e0169572. https://doi.org/10.1371/journal.pone.0169572. (PMID: 10.1371/journal.pone.0169572280461195207786)
Pifferi S, Dibattista M, Menini A (2009) TMEM16B induces chloride currents activated by calcium in mammalian cells. Pflugers Arch 458:1023–1038. https://doi.org/10.1007/s00424-009-0684-9. (PMID: 10.1007/s00424-009-0684-919475416)
Pomorski TG, Menon AK (2016) Lipid somersaults: uncovering the mechanisms of protein-mediated lipid flipping. Prog Lipid Res 64:69–84. https://doi.org/10.1016/j.plipres.2016.08.003. (PMID: 10.1016/j.plipres.2016.08.003275281895127727)
Robertson BE (1998) Inhibition of calcium-activated chloride channels by niflumic acid dilates rat cerebral arteries. Acta Physiol Scand 163:417–418. https://doi.org/10.1046/j.1365-201X.1998.t01-1-00366.x. (PMID: 10.1046/j.1365-201X.1998.t01-1-00366.x9789585)
Sala-Rabanal M, Yurtsever Z, Nichols CG, Brett TJ (2015) Secreted CLCA1 modulates TMEM16A to activate Ca 2+ -dependent chloride currents in human cells. eLife 4:e05875. https://doi.org/10.7554/eLife.05875. (PMID: 10.7554/eLife.05875257813444360653)
Sala-Rabanal M, Yurtsever Z, Berry KN, Nichols CG, Brett TJ (2017) Modulation of TMEM16A channel activity by the von Willebrand factor type A (VWA) domain of the calcium-activated chloride channel regulator 1 (CLCA1). J Biol Chem 292:9164–9174. https://doi.org/10.1074/jbc.M117.788232. (PMID: 10.1074/jbc.M117.788232284207325454099)
Schroeder BC, Cheng T, Jan YN, Jan LY (2008) Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134:1019–1029. https://doi.org/10.1016/j.cell.2008.09.003. (PMID: 10.1016/j.cell.2008.09.003188050942651354)
Scudieri P, Caci E, Venturini A, Sondo E, Pianigiani G, Marchetti C, Ravazzolo R, Pagani F, Galietta LJV (2015) Ion channel and lipid scramblase activity associated with expression of TMEM16F/ANO6 isoforms. J Physiol 593:3829–3848. https://doi.org/10.1113/jp270691. (PMID: 10.1113/jp270691261084574575572)
Segura-Covarrubias G, Aréchiga-Figueroa IA, De Jesús-Pérez JJ, Sánchez-Solano A, Pérez-Cornejo P, Arreola J (2020) Voltage-dependent protonation of the calcium pocket enable activation of the calcium-activated chloride channel anoctamin-1 (TMEM16A). Sci Rep 10:6644. https://doi.org/10.1038/s41598-020-62860-9. (PMID: 10.1038/s41598-020-62860-9323132037170896)
Seo Y, Lee HK, Park J, D-k J, Jo S, Jo M, Namkung W (2016) Ani9, a novel potent small-molecule ANO1 inhibitor with negligible effect on ANO2. PLoS One 11:e0155771. https://doi.org/10.1371/journal.pone.0155771. (PMID: 10.1371/journal.pone.0155771272190124878759)
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. J Biol Chem 286:1381–1388. https://doi.org/10.1074/jbc.M110.174847. (PMID: 10.1074/jbc.M110.17484721056985)
Shimizu T, Iehara T, Sato K, Fujii T, Sakai H, Okada Y (2013) TMEM16F is a component of a Ca 2+ -activated Cl − channel but not a volume-sensitive outwardly rectifying Cl − channel. Am J Physiol Cell Physiol 304:C748–C759. https://doi.org/10.1152/ajpcell.00228.2012. (PMID: 10.1152/ajpcell.00228.201223426967)
Sinkkonen ST, Mansikkamäki S, Möykkynen T, Lüddens H, Uusi-Oukari M, Korpi ER (2003) Receptor subtype-dependent positive and negative modulation of GABA A receptor function by niflumic acid, a nonsteroidal anti-inflammatory drug. Mol Pharmacol 64:753–763. https://doi.org/10.1124/mol.64.3.753. (PMID: 10.1124/mol.64.3.75312920213)
Stephan AB, Shum EY, Hirsh S, Cygnar KD, Reisert J, Zhao H (2009) ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proc Natl Acad Sci U S A 106:11776. https://doi.org/10.1073/pnas.0903304106. (PMID: 10.1073/pnas.0903304106195613022702256)
Suzuki J, Umeda M, Sims PJ, Nagata S (2010) Calcium-dependent phospholipid scrambling by TMEM16F. Nature 468:834–838. https://doi.org/10.1038/nature09583. (PMID: 10.1038/nature0958321107324)
Suzuki J, Fujii T, Imao T, Ishihara K, Kuba H, Nagata S (2013) Calcium-dependent phospholipid scramblase activity of TMEM16 protein family members. J Biol Chem 288:13305–13316. https://doi.org/10.1074/jbc.M113.457937. (PMID: 10.1074/jbc.M113.457937235328393650369)
Ta CM, Adomaviciene A, Rorsman NJG, Garnett H, Tammaro P (2016) Mechanism of allosteric activation of TMEM16A/ANO1 channels by a commonly used chloride channel blocker. Br J Pharmacol 173:511–528. https://doi.org/10.1111/bph.13381. (PMID: 10.1111/bph.13381265620724728427)
Ta CM, Acheson KE, Rorsman NJG, Jongkind RC, Tammaro P (2017) Contrasting effects of phosphatidylinositol 4,5-bisphosphate on cloned TMEM16A and TMEM16B channels. Br J Pharmacol 174:2984–2999. https://doi.org/10.1111/bph.13913. (PMID: 10.1111/bph.13913286168635573538)
Terashima H, Picollo A, Accardi A (2013) Purified TMEM16A is sufficient to form Ca 2+ -activated Cl − channels. Proc Natl Acad Sci U S A 110:19354–19359. https://doi.org/10.1073/pnas.1312014110. (PMID: 10.1073/pnas.1312014110241672643845129)
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 J 25:1058–1068. https://doi.org/10.1096/fj.10-166884. (PMID: 10.1096/fj.10-16688421115851)
Tian Y, Schreiber R, Kunzelmann K (2012) Anoctamins are a family of Ca 2+ -activated Cl − channels. J Cell Sci 125:4991–4998. https://doi.org/10.1242/jcs.109553. (PMID: 10.1242/jcs.10955322946059)
Tien J, Peters CJ, Wong XM, Cheng T, Jan YN, Jan LY, Yang H (2014) A comprehensive search for calcium binding sites critical for TMEM16A calcium-activated chloride channel activity. Elife 3:e02772. https://doi.org/10.7554/eLife.02772. (PMID: 10.7554/eLife.02772249807014112547)
Tsutsumi S, Kamata N, Vokes TJ, Maruoka Y, Nakakuki K, Enomoto S, Omura K, Amagasa T, Nagayama M, Saito-Ohara F, Inazawa J, Moritani M, Yamaoka T, Inoue H, Itakura M (2004) The novel gene encoding a putative transmembrane protein is mutated in Gnathodiaphyseal dysplasia (GDD). Am J Hum Genet 74:1255–1261. https://doi.org/10.1086/421527. (PMID: 10.1086/421527151241031182089)
Vocke K, Dauner K, Hahn A, Ulbrich A, Broecker J, Keller S, Frings S, Möhrlen F (2013) Calmodulin-dependent activation and inactivation of anoctamin calcium-gated chloride channels. J Gen Physiol 142:381–404. https://doi.org/10.1085/jgp.201311015. (PMID: 10.1085/jgp.201311015240819813787769)
White MM, Aylwin M (1990) Niflumic and flufenamic acids are potent reversible blockers of Ca 2+ -activated Cl − channels in Xenopus oocytes. Mol Pharmacol 37:720–724. (PMID: 1692608)
Whitlock JM, Hartzell HC (2017) Anoctamins/TMEM16 proteins: chloride channels flirting with lipids and extracellular vesicles. Annu Rev Physiol 79:119–143. https://doi.org/10.1146/annurev-physiol-022516-034031. (PMID: 10.1146/annurev-physiol-022516-03403127860832)
Whitlock JM, Yu K, Cui YY, Hartzell HC (2018) Anoctamin 5/TMEM16E facilitates muscle precursor cell fusion. J Gen Physiol 150:1498–1509. https://doi.org/10.1085/jgp.201812097. (PMID: 10.1085/jgp.201812097302579286219693)
Wong XM, Younger S, Peters CJ, Jan YN, Jan LY (2013) Subdued, a TMEM16 family Ca 2+ -activated cl − channel in Drosophila melanogaster with an unexpected role in host defense. Elife 2:e00862. https://doi.org/10.7554/eLife.00862. (PMID: 10.7554/eLife.00862241920343814000)
Woodruff PG, Boushey HA, Dolganov GM, Barker CS, Yang YH, Donnelly S, Ellwanger A, Sidhu SS, Dao-Pick TP, Pantoja C, Erle DJ, Yamamoto KR, Fahy JV (2007) Genome-wide profiling identifies epithelial cell genes associated with asthma and with treatment response to corticosteroids. Proc Natl Acad Sci U S A 104:15858–15863. https://doi.org/10.1073/pnas.0707413104. (PMID: 10.1073/pnas.0707413104178981692000427)
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. Proc Natl Acad Sci U S A 108:8891–8896. https://doi.org/10.1073/pnas.1102147108. (PMID: 10.1073/pnas.1102147108215555823102354)
Yang H, Jan LY (2016) Chapter 7 – TMEM16 membrane proteins in health and disease. In: Pitt GS (ed) Ion channels in health and disease. Academic Press, Boston, pp 165–197. (PMID: 10.1016/B978-0-12-802002-9.00007-8)
Yang YD, Cho H, Koo JY, Tak MH, Cho Y, Shim W-S, Park SP, Lee J, Lee B, Kim B-M, Raouf R, Shin YK, Oh U (2008) TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nature 455:1210–1215. https://doi.org/10.1038/nature07313. (PMID: 10.1038/nature0731318724360)
Yang H, Kim A, David T, Palmer D, Jin T, Tien J, Huang F, Cheng T, Coughlin Shaun R, Jan Yuh N, Jan Lily Y (2012) TMEM16F forms a Ca 2+ -activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 151:111–122. https://doi.org/10.1016/j.cell.2012.07.036. (PMID: 10.1016/j.cell.2012.07.036230212193582364)
Ye W, Han TW, Nassar LM, Zubia M, Jan YN, Jan LY (2018) Phosphatidylinositol-(4,5)-bisphosphate regulates calcium gating of small-conductance cation channel TMEM16F. Proc Natl Acad Sci U S A 115:E1667–E1674. https://doi.org/10.1073/pnas.1718728115. (PMID: 10.1073/pnas.1718728115293827635816197)
Ye W, Han TW, He M, Jan YN, Jan LY (2019) Dynamic change of electrostatic field in TMEM16F permeation pathway shifts its ion selectivity. Elife 8:e45187. https://doi.org/10.7554/eLife.45187. (PMID: 10.7554/eLife.45187313183306690719)
Yu K, Duran C, Qu Z, Cui Y-Y, Hartzell HC (2012) Explaining calcium-dependent gating of anoctamin-1 chloride channels requires a revised topology. Circ Res 110:990–999. https://doi.org/10.1161/CIRCRESAHA.112.264440. (PMID: 10.1161/CIRCRESAHA.112.264440223945183558997)
Yu Y, Kuan A-S, Chen T-Y (2014) Calcium-calmodulin does not alter the anion permeability of the mouse TMEM16A calcium-activated chloride channel. J Gen Physiol 144:115–124. https://doi.org/10.1085/jgp.201411179. (PMID: 10.1085/jgp.201411179249812324076522)
Yu K, Whitlock JM, Lee K, Ortlund EA, Cui YY, Hartzell HC (2015) Identification of a lipid scrambling domain in ANO6/TMEM16F. eLife 4:e06901. https://doi.org/10.7554/eLife.06901. (PMID: 10.7554/eLife.06901260578294477620)
Yu K, Jiang T, Cui Y, Tajkhorshid E, Hartzell HC (2019) A network of phosphatidylinositol 4,5-bisphosphate binding sites regulates gating of the Ca 2+ -activated Cl − channel ANO1 (TMEM16A). Proc Natl Acad Sci U S A 116:19952–19962. https://doi.org/10.1073/pnas.1904012116. (PMID: 10.1073/pnas.1904012116315154516778221)
Yuan H, Gao C, Chen Y, Jia M, Geng J, Zhang H, Zhan Y, Boland LM, An H (2013) Divalent cations modulate TMEM16A calcium-activated chloride channels by a common mechanism. J Membr Biol 246:893–902. https://doi.org/10.1007/s00232-013-9589-9. (PMID: 10.1007/s00232-013-9589-923996050)
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. J Biol Chem 287:42138–42149. https://doi.org/10.1074/jbc.M112.410282. (PMID: 10.1074/jbc.M112.410282231120503516759)
فهرسة مساهمة: Keywords: Calcium-activated chloride channels; Gating; Permeation; Phospholipid scramblases; TMEM16
المشرفين على المادة: 0 (Chloride Channels)
0 (Phospholipid Transfer Proteins)
0 (Anoctamins)
0 (Phospholipids)
SY7Q814VUP (Calcium)
تواريخ الأحداث: Date Created: 20220706 Date Completed: 20240105 Latest Revision: 20240105
رمز التحديث: 20240105
DOI: 10.1007/164_2022_595
PMID: 35792944
قاعدة البيانات: MEDLINE
الوصف
تدمد:0171-2004
DOI:10.1007/164_2022_595