Voltage-Dependent Protonation of the Calcium Pocket Enable Activation of the Calcium-Activated Chloride Channel Anoctamin-1 (TMEM16A).


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
20 04 2020
Historique:
received: 19 02 2020
accepted: 21 03 2020
entrez: 22 4 2020
pubmed: 22 4 2020
medline: 1 12 2020
Statut: epublish

Résumé

Anoctamin-1 (ANO1 or TMEM16A) is a homo-dimeric Ca

Identifiants

pubmed: 32313203
doi: 10.1038/s41598-020-62860-9
pii: 10.1038/s41598-020-62860-9
pmc: PMC7170896
doi:

Substances chimiques

ANO1 protein, mouse 0
Anoctamin-1 0
Anthracenes 0
Cations, Divalent 0
Chlorides 0
Protons 0
Recombinant Fusion Proteins 0
Tannins 0
enhanced green fluorescent protein 0
Green Fluorescent Proteins 147336-22-9
9-anthroic acid 723-62-6
Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

6644

Références

Schroeder, B. C., Cheng, T., Jan, Y. N. & Jan, L. Y. Expression Cloning of TMEM16A as a Calcium-Activated Chloride Channel Subunit. Cell 134, 1019–1029 (2008).
doi: 10.1016/j.cell.2008.09.003
Caputo, A. et al. TMEM16A, a membrane protein associated with calcium-dependent chloride channel activity. Science (80-). 322, 590-594 (2008).
Yang, Y. D. et al. TMEM16A confers receptor-activated calcium-dependent chloride conductance. Nat. … 455, 1210–1215 (2008).
doi: 10.1038/nature07313
Hartzell, C., Putzier, I. & Arreola, J. Calcium-activated chloride channels. Annual Review of Physiology vol. 67 (2005).
Pedemonte, N. & Galietta, L. J. V. Structure and function of TMEM16 proteins (anoctamins). Physiol. Rev. 94, 419–59 (2014).
doi: 10.1152/physrev.00039.2011
Pusch, M., Ludewig, U. & Jentsch, T. J. Temperature dependence of fast and slow gating relaxations of ClC-0 chloride channels. J. Gen. Physiol. 109, 105–116 (1997).
doi: 10.1085/jgp.109.1.105
Hartzell, C., Putzier, I. & Arreola, J. Calcium-Activated Chloride Channels. Annu. Rev. Physiol. 67, 719–758 (2005).
doi: 10.1146/annurev.physiol.67.032003.154341
Duan, D. Phenomics of cardiac chloride channels: the systematic study of chloride channel function in the heart. J. Physiol. 587, 2163–2177 (2009).
doi: 10.1113/jphysiol.2008.165860
Romanenko, V. G. et al. Tmem16A encodes the Ca2+-activated Cl− channel in mouse submandibular salivary gland acinar cells. J. Biol. Chem. 285, 12990–13001 (2010).
doi: 10.1074/jbc.M109.068544
Hwang, S. J. et al. Expression of anoctamin 1/TMEM16A by interstitial cells of Cajal is fundamental for slow wave activity in gastrointestinal muscles. J Physiol 587, 4887–904 (2009).
doi: 10.1113/jphysiol.2009.176198
Heinze, C. et al. Disruption of vascular Ca 2 + -activated chloride currents lowers blood pressure. J. Clin. Invest. 124, 675–86 (2014).
doi: 10.1172/JCI70025
Crutzen, R. et al. Anoctamin 1 (Ano1) is required for glucose-induced membrane potential oscillations and insulin secretion by murine β-cells. Pflügers Arch. Eur. J. Physiol. 468, 573–91 (2016).
doi: 10.1007/s00424-015-1758-5
Huang, F. et al. Calcium-activated chloride channel TMEM16A modulates mucin secretion and airway smooth muscle contraction. Proc. Natl. Acad. Sci. USA 109, 16354–9 (2012).
doi: 10.1073/pnas.1214596109
Pietra, G., Dibattista, M., Menini, A., Reisert, J. & Boccaccio, A. The Ca2+-activated Cl− channel TMEM16B regulates action potential firing and axonal targeting in olfactory sensory neurons. J. Gen. Physiol., https://doi.org/10.1085/jgp.201611622 (2016).
Wozniak, K. L., Phelps, W. A., Tembo, M., Lee, M. T. & Carlson, A. E. The TMEM16A channel mediates the fast polyspermy block in Xenopus laevis. J. Gen. Physiol. https://doi.org/10.1085/jgp.201812071 (2018).
doi: 10.1085/jgp.201812071 pubmed: 30012842 pmcid: 6122928
Cordero-Martínez, J. et al. TMEM16A inhibition impedes capacitation and acquisition of hyperactivated motility in guinea pig sperm. J. Cell. Biochem. 119, 5944–5959 (2018).
doi: 10.1002/jcb.26789
He, M. et al. Cytoplasmic Cl− couples membrane remodeling to epithelial morphogenesis. Proc. Natl. Acad. Sci. USA 114, E11161–E11169 (2017).
doi: 10.1073/pnas.1714448115
Duvvuri, U. et al. TMEM16A induces MAPK and contributes directly to tumorigenesis and cancer progression. Cancer Res. 72, 3270–3281 (2012).
doi: 10.1158/0008-5472.CAN-12-0475-T
Qu, Z. et al. The Ca(2+) -activated Cl(−) channel, ANO1 (TMEM16A), is a double-edged sword in cell proliferation and tumorigenesis. Cancer medicine vol. 3, 453–461 (2014).
doi: 10.1002/cam4.232
Crottès, D. & Jan, L. Y. The multifaceted role of TMEM16A in cancer. Cell Calcium, https://doi.org/10.1016/j.ceca.2019.06.004 (2019).
Britschgi, A. et al. Calcium-activated chloride channel ANO1 promotes breast cancer progression by activating EGFR and CAMK signaling. Proc. Natl. Acad. Sci. USA, https://doi.org/10.1073/pnas.1217072110 (2013).
Arreola, J., Melvin, J. E. & Begenisich, T. Activation of calcium-dependent chloride channels in rat parotid acinar cells. J. Gen. Physiol. 108, 35–47 (1996).
doi: 10.1085/jgp.108.1.35
Xiao, Q. et al. Voltage- and calcium-dependent gating of TMEM16A/Ano1 chloride channels are physically coupled by the first intracellular loop. Proc. Natl. Acad. Sci. USA 108, 8891–8896 (2011).
doi: 10.1073/pnas.1102147108
Tien, J. et al. A comprehensive search for calcium binding sites critical for TMEM16A calcium-activated chloride channel activity: (A) Two competing models to explain TMEM16A calcium sensitivity have been proposed. It is unclear whether calcium directly binds to TMEM16A-. Elife 3, 1–19 (2014).
doi: 10.7554/eLife.02772
Paulino, C., Kalienkova, V., Lam, A. K. M., Neldner, Y. & Dutzler, R. Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM. Nature 552, 421–425 (2017).
doi: 10.1038/nature24652
Yu, K., Duran, C., Qu, Z., Cui, Y. Y. & Hartzell, H. C. Explaining calcium-dependent gating of anoctamin-1 chloride channels requires a revised topology. Circ. Res. 110, 990–999 (2012).
doi: 10.1161/CIRCRESAHA.112.264440
Tien, J. et al. A comprehensive search for calcium binding sites critical for TMEM16A calcium-activated chloride channel activity. Elife 3, 1–19 (2014).
doi: 10.7554/eLife.02772
Parker, I. & Miledi, R. Changes in intracellular calcium and in membrane currents evoked by injection of inositol trisphosphate into Xenopus oocytes. Proc. R. Soc. London - Biol. Sci. 228, 307–315 (1986).
doi: 10.1098/rspb.1986.0057
Ni, Y. L., Kuan, A. S. & Chen, T. Y. Activation and inhibition of TMEM16A calcium-activated chloride channels. PLoS One 9, 4–6 (2014).
doi: 10.1371/annotation/70d3c7b0-9718-4bb1-abed-d0defc3b7fc4
Lam, A. K. M. & Dutzler, R. Calcium-dependent electrostatic control of anion access to the pore of the calcium-activated chloride channel TMEM16A. Elife 7 (2018).
Romani, A. M. P. Intracellular magnesium homeostasis. Magnesium in the Central Nervous System (2011).
Chun, H. et al. Protons inhibit anoctamin 1 by competing with calcium. Cell Calcium 58, 431–441 (2015).
doi: 10.1016/j.ceca.2015.06.011
Arreola, J., Melvin, J. E. & Begenisich, T. Inhibition of Ca2+-dependent Cl− channels from secretory epithelial cells by low internal pH. J. Membr. Biol., https://doi.org/10.1007/BF00235400 (1995).
Namkung, W., Thiagarajah, J. R., Phuan, P. W. & Verkman, A. S. Inhibition of Ca2+-activated Cl− channels by gallotannins as a possible molecular basis for health benefits of red wine and green tea. FASEB J. 24, 4178–4186 (2010).
doi: 10.1096/fj.10-160648
Ta, C. M., Adomaviciene, A., Rorsman, N. J. G., Garnett, H. & Tammaro, P. Mechanism of allosteric activation of TMEM16A/ANO1 channels by a commonly used chloride channel blocker. Br. J. Pharmacol. 173, 511–528 (2016).
doi: 10.1111/bph.13381
Cho, H. et al. The calcium-activated chloride channel anoctamin 1 acts as a heat sensor in nociceptive neurons. Nat. Neurosci. 15, 1015–1021 (2012).
doi: 10.1038/nn.3111
Peters, C. J. et al. The Sixth Transmembrane Segment is a Major Gating Component of the TMEM16A Calcium-Activated Chloride Channel. Neuron 97, 1063–1077.e4 (2018).
Cruz-Rangel, S. et al. Gating modes of calcium-activated chloride channels TMEM16A and TMEM16B. J. Physiol. 593 (2015).
Avdonin, V., Tang, X. D. & Hoshi, T. Stimulatory action of internal protons on Slo1 BK channels. Biophys. J. 84, 2969–2980 (2003).
doi: 10.1016/S0006-3495(03)70023-X
Pahari, S., Sun, L. & Alexov, E. PKAD: a database of experimentally measured pKa values of ionizable groups in proteins. Database (Oxford). 2019 (2019).
Tembo, M., Wozniak, K. L., Bainbridge, R. E. & Carlson, A. E. Phosphatidylinositol 4,5-bisphosphate (PIP2) and Ca2 are both required to open the Cl channel TMEM16A. J. Biol. Chem. 294, 12556–12564 (2019).
doi: 10.1074/jbc.RA118.007128
De Jesús-Pérez, J. J. et al. 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 (2018).
doi: 10.1016/j.bbalip.2017.12.009
Arreola, J. & Hartzell, H. C. Wasted TMEM16A channels are rescued by phosphatidylinositol 4,5-bisphosphate. Cell Calcium 84 (2019).
Cruz-Rangel, S. et al. Extracellular protons enable activation of the calcium-dependent chloride channel TMEM16A. J. Physiol. 595, 1515–1531 (2017).
doi: 10.1113/JP273111
Chiche, J., Brahimi-Horn, M. C. & Pouysségur, J. Tumour hypoxia induces a metabolic shift causing acidosis: A common feature in cancer. J. Cell. Mol. Med., https://doi.org/10.1111/j.1582-4934.2009.00994.x (2010).
Persi, E. et al. Systems analysis of intracellular pH vulnerabilities for cancer therapy. Nat. Commun. 9 (2018).
Cho, C. et al. TMEM16A expression in cholinergic neurons of the medial habenula mediates anxiety‐related behaviors. EMBO Rep., https://doi.org/10.15252/embr.201948097 (2019).
Dayal, A., Ng, S. F. J. & Grabner, M. Ca 2+ -activated Cl− channel TMEM16A/ANO1 identified in zebrafish skeletal muscle is crucial for action potential acceleration. Nat. Commun. 10 (2019).
Faria, D. et al. The calcium-activated chloride channel Anoctamin 1 contributes to the regulation of renal function. Kidney Int. 85, 1369–1381 (2014).
doi: 10.1038/ki.2013.535
Traverso, S., Zifarelli, G., Aiello, R. & Pusch, M. Proton sensing of CLC-0 mutant E166D. J. Gen. Physiol. 127, 51–65 (2006).
doi: 10.1085/jgp.200509340
Cruz-Rangel, S. et al. Gating modes of calcium-activated chloride channels TMEM16A and TMEM16B. J. Physiol. 593, 5283–5298 (2015).
doi: 10.1113/JP271256
Hernández-Carballo, C. Y., De Santiago-Castillo, J. A., Rosales-Saavedra, T., Pérez-Cornejo, P. & Arreola, J. Control of volume-sensitive chloride channel inactivation by the coupled action of intracellular chloride and extracellular protons. Pflugers Arch. Eur. J. Physiol. 460, 633–644 (2010).
doi: 10.1007/s00424-010-0842-0
Woodhull, A. M. Ionic Blockage of Sodium Channels in Nerve. J. Gen. Physiol. 61, 687–708 (1973).
doi: 10.1085/jgp.61.6.687
Hille, B. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J. Gen. Physiol. 50, 1287–1302 (1967).
doi: 10.1085/jgp.50.5.1287
Hille, B. Ion Channels of Excitable Membranes. (Sinauer Associates Is an Imprint of Oxford University Press, 2001).

Auteurs

Guadalupe Segura-Covarrubias (G)

Division de Biología Molecular del Instituto Potosino de Investigación Científica y Tecnológica. Camino a la Presa de San José 2055, San Luis Potosí, SLP, 78216, México.

Iván A Aréchiga-Figueroa (IA)

Department of Physiology and Biophysics, Universidad Autónoma de San Luis Potosí School of Medicine, Ave. V. Carranza 2405, San Luis Potosí, SLP, 78290, México.

José J De Jesús-Pérez (JJ)

Physics Institute, Universidad Autónoma de San Luis Potosí, Ave. Dr. Manuel Nava #6, San Luis Potosí, SLP, 78290, México.

Alfredo Sánchez-Solano (A)

Physics Institute, Universidad Autónoma de San Luis Potosí, Ave. Dr. Manuel Nava #6, San Luis Potosí, SLP, 78290, México.

Patricia Pérez-Cornejo (P)

Department of Physiology and Biophysics, Universidad Autónoma de San Luis Potosí School of Medicine, Ave. V. Carranza 2405, San Luis Potosí, SLP, 78290, México.

Jorge Arreola (J)

Physics Institute, Universidad Autónoma de San Luis Potosí, Ave. Dr. Manuel Nava #6, San Luis Potosí, SLP, 78290, México. arreola@dec1.ifisica.uaslp.mx.

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