Structural and Biophysical Analysis of the CLCA1 VWA Domain Suggests Mode of TMEM16A Engagement

Cell Reports - Tập 30 - Trang 1141-1151.e3 - 2020
Kayla N. Berry1,2, Tom J. Brett2,3,4,5
1Immunology Program and Medical Scientist Training Program, Washington University School of Medicine, St. Louis, MO 63110, USA
2Department of Internal Medicine, Division of Pulmonary and Critical Care, Washington University School of Medicine, St. Louis, MO 63110, USA
3Center for the Investigation of Membrane Excitability Diseases (CIMED), Washington University School of Medicine, St. Louis, MO 63110, USA
4Department of Cell Biology and Physiology, Washington University School of Medicine, St. Louis, MO 63110 USA
5Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, MO 63110, USA

Tài liệu tham khảo

Adams, 2010, PHENIX: a comprehensive Python-based system for macromolecular structure solution, Acta Crystallogr. D Biol. Crystallogr., 66, 213, 10.1107/S0907444909052925 Ajroud, 2004, Binding Affinity of Metal Ions to the CD11b A-domain Is Regulated by Integrin Activation and Ligands, J. Biol. Chem., 279, 25483, 10.1074/jbc.M402901200 Aricescu, 2006, A time- and cost-efficient system for high-level protein production in mammalian cells, Acta Crystallogr. D Biol. Crystallogr., 62, 1243, 10.1107/S0907444906029799 Baldwin, 1998, Cation binding to the integrin CD11b I domain and activation model assessment, Structure, 6, 923, 10.1016/S0969-2126(98)00093-8 Becker, 2014, A structure of a collagen VI VWA domain displays N and C termini at opposite sides of the protein, Structure, 22, 199, 10.1016/j.str.2013.06.028 Benedetto, 2017, Epithelial Chloride Transport by CFTR Requires TMEM16A, Sci. Rep., 7, 12397, 10.1038/s41598-017-10910-0 Bhattacharya, 2004, Crystal structure of the A domain from complement factor B reveals an integrin-like open conformation, Structure, 12, 371, 10.1016/j.str.2004.02.012 Blom, 2004, Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence, Proteomics, 4, 1633, 10.1002/pmic.200300771 Briot, 2018, A three-way inter-molecular network accounts for the CaVα2δ1-induced functional modulation of the pore-forming CaV1.2 subunit, J. Biol. Chem., 293, 7176, 10.1074/jbc.RA118.001902 Dang, 2017, Cryo-EM structures of the TMEM16A calcium-activated chloride channel, Nature, 552, 426, 10.1038/nature25024 Dolphin, 2016, Voltage-gated calcium channels and their auxiliary subunits: physiology and pathophysiology and pharmacology, J. Physiol., 594, 5369, 10.1113/JP272262 Drozdetskiy, 2015, JPred4: a protein secondary structure prediction server, Nucleic Acids Res., 43, W389, 10.1093/nar/gkv332 Dyer, 2014, High-throughput SAXS for the characterization of biomolecules in solution: a practical approach, Methods Mol. Biol., 1091, 245, 10.1007/978-1-62703-691-7_18 Emsley, 2010, Features and development of Coot, Acta Crystallogr. D Biol. Crystallogr., 66, 486, 10.1107/S0907444910007493 Franke, 2009, DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering, J. Appl. Cryst., 42, 342, 10.1107/S0021889809000338 Franke, 2017, ATSAS 2.8: a comprehensive data analysis suite for small-angle scattering from macromolecular solutions, J. Appl. Cryst., 50, 1212, 10.1107/S1600576717007786 Fu, 2010, The structure of tumor endothelial marker 8 (TEM8) extracellular domain and implications for its receptor function for recognizing anthrax toxin, PLoS One, 5, e11203, 10.1371/journal.pone.0011203 Gruber, 1999, Molecular cloning and transmembrane structure of hCLCA2 from human lung, trachea, and mammary gland, Am. J. Physiol., 276, C1261, 10.1152/ajpcell.1999.276.6.C1261 Holm, 2016, Dali server update, Nucleic Acids Res., 44, W351, 10.1093/nar/gkw357 Hubbard, 1993 Kabsch, 2010, Xds, Acta Crystallogr. D Biol. Crystallogr., 66, 125, 10.1107/S0907444909047337 Kober, 2015, Efficient Mammalian Cell Expression and Single-step Purification of Extracellular Glycoproteins for Crystallization, J. Vis. Exp., 23, e53445 Kolbe, 2013, CLCA4 variants determine the manifestation of the cystic fibrosis basic defect in the intestine, Eur. J. Hum. Genet., 21, 691, 10.1038/ejhg.2012.234 Konarev, 2003, PRIMUS: a Windows PC-based system for small-angle scattering data analysis, J. Appl. Cryst., 36, 1277, 10.1107/S0021889803012779 Lacy, 2004, Structure of heptameric protective antigen bound to an anthrax toxin receptor: a role for receptor in pH-dependent pore formation, Proc. Natl. Acad. Sci. USA, 101, 13147, 10.1073/pnas.0405405101 Lacy, 2004, Crystal structure of the von Willebrand factor A domain of human capillary morphogenesis protein 2: an anthrax toxin receptor, Proc. Natl. Acad. Sci. USA, 101, 6367, 10.1073/pnas.0401506101 Laskowski, 2011, LigPlot+: multiple ligand-protein interaction diagrams for drug discovery, J. Chem. Inf. Model., 51, 2778, 10.1021/ci200227u Lee, 1995, Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18), Cell, 80, 631, 10.1016/0092-8674(95)90517-0 Li, 1998, Two functional states of the CD11b A-domain: correlations with key features of two Mn2+-complexed crystal structures, J. Cell Biol., 143, 1523, 10.1083/jcb.143.6.1523 Li, 2017, Bypassing CFTR dysfunction in cystic fibrosis with alternative pathways for anion transport, Curr. Opin. Pharmacol., 34, 91, 10.1016/j.coph.2017.10.002 Luo, 2007, Structural basis of integrin regulation and signaling, Annu. Rev. Immunol., 25, 619, 10.1146/annurev.immunol.25.022106.141618 Mahalingam, 2011, Stable coordination of the inhibitory Ca2+ ion at the metal ion-dependent adhesion site in integrin CD11b/CD18 by an antibody-derived ligand aspartate: implications for integrin regulation and structure-based drug design, J. Immunol., 187, 6393, 10.4049/jimmunol.1102394 Mall, 2015, Targeting ion channels in cystic fibrosis, J. Cyst. Fibros., 14, 561, 10.1016/j.jcf.2015.06.002 Mall, 2018, Emerging Concepts and Therapies for Mucoobstructive Lung Disease, Ann. Am. Thorac. Soc., 15, S216, 10.1513/AnnalsATS.201806-368AW McCleverty, 2003, Engineered allosteric mutants of the integrin alphaMbeta2 I domain: structural and functional studies, Biochem. J., 372, 121, 10.1042/bj20021273 Meyer, 2016, Data publication with the structural biology data grid supports live analysis, Nat. Commun., 7, 10882, 10.1038/ncomms10882 Morin, 2013, Cutting edge: Collaboration gets the most out of software, eLife, 2, e01456, 10.7554/eLife.01456 Mundhenk, 2018, Interspecies diversity of chloride channel regulators, calcium-activated 3 genes, PLoS One, 13, e0191512, 10.1371/journal.pone.0191512 Nolte, 1999, Crystal structure of the alpha1beta1 integrin I-domain: insights into integrin I-domain function, FEBS Lett., 452, 379, 10.1016/S0014-5793(99)00666-3 Patel, 2009, The role of CLCA proteins in inflammatory airway disease, Annu. Rev. Physiol., 71, 425, 10.1146/annurev.physiol.010908.163253 Paulino, 2017, Activation mechanism of the calcium-activated chloride channel TMEM16A revealed by cryo-EM, Nature, 552, 421, 10.1038/nature24652 Paulsson, 2018, Matrilins, Methods Cell Biol., 143, 429, 10.1016/bs.mcb.2017.08.018 Rambo, 2015, Resolving Individual Components in Protein-RNA Complexes Using Small-Angle X-ray Scattering Experiments, Methods Enzymol., 558, 363, 10.1016/bs.mie.2015.02.004 Robert, 2014, Deciphering key features in protein structures with the new ENDscript server, Nucleic Acids Res., 42, W320, 10.1093/nar/gku316 Romani, 2017, Thymosin α1 represents a potential potent single-molecule-based therapy for cystic fibrosis, Nat. Med., 23, 590, 10.1038/nm.4305 Rossmann, 1974, Chemical and biological evolution of nucleotide-binding protein, Nature, 250, 194, 10.1038/250194a0 Ruffin, 2013, Anoctamin 1 dysregulation alters bronchial epithelial repair in cystic fibrosis, Biochim. Biophys. Acta, 1832, 2340, 10.1016/j.bbadis.2013.09.012 Sala-Rabanal, 2015, Novel Roles for Chloride Channels, Exchangers, and Regulators in Chronic Inflammatory Airway Diseases, Mediators Inflamm., 2015, 497387, 10.1155/2015/497387 Sala-Rabanal, 2015, Secreted CLCA1 modulates TMEM16A to activate Ca(2+)-dependent chloride currents in human cells, eLife, 4, e05875, 10.7554/eLife.05875 Sala-Rabanal, 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, 10.1074/jbc.M117.788232 San Sebastian, 2006, On the affinity regulation of the metal-ion-dependent adhesion sites in integrins, J. Am. Chem. Soc., 128, 3554, 10.1021/ja054142a Santelli, 2004, Crystal structure of a complex between anthrax toxin and its host cell receptor, Nature, 430, 905, 10.1038/nature02763 Shimaoka, 2002, Conformational regulation of integrin structure and function, Annu. Rev. Biophys. Biomol. Struct., 31, 485, 10.1146/annurev.biophys.31.101101.140922 Shimaoka, 2003, Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation, Cell, 112, 99, 10.1016/S0092-8674(02)01257-6 Sievers, 2011, Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega, Mol. Syst. Biol., 7, 539, 10.1038/msb.2011.75 Sondo, 2014, The TMEM16A chloride channel as an alternative therapeutic target in cystic fibrosis, Int. J. Biochem. Cell Biol., 52, 73, 10.1016/j.biocel.2014.03.022 Song, 2014, Structures of the Toxoplasma gliding motility adhesin, Proc. Natl. Acad. Sci. USA, 111, 4862, 10.1073/pnas.1403059111 Song, 2012, Shape change in the receptor for gliding motility in Plasmodium sporozoites, Proc. Natl. Acad. Sci. USA, 109, 21420, 10.1073/pnas.1218581109 Sonneville, 2017, MicroRNA-9 downregulates the ANO1 chloride channel and contributes to cystic fibrosis lung pathology, Nat. Commun., 8, 710, 10.1038/s41467-017-00813-z Springer, 2006, Complement and the multifaceted functions of VWA and integrin I domains, Structure, 14, 1611, 10.1016/j.str.2006.10.001 Svergun, 1992, Determination of the Regularization Parameter in Indirect-Transform Methods Using Perceptual Criteria, J. Appl. Cryst., 25, 495, 10.1107/S0021889892001663 van der Doef, 2010, Association of the CLCA1 p.S357N variant with meconium ileus in European patients with cystic fibrosis, J. Pediatr. Gastroenterol. Nutr., 50, 347, 10.1097/MPG.0b013e3181afce6c Veit, 2012, Proinflammatory cytokine secretion is suppressed by TMEM16A or CFTR channel activity in human cystic fibrosis bronchial epithelia, Mol. Biol. Cell, 23, 4188, 10.1091/mbc.e12-06-0424 Volkov, 2003, Uniqueness of ab initio shape determination in small-angle scattering, J. Appl. Cryst., 36, 860, 10.1107/S0021889803000268 Vorup-Jensen, 2003, Structure and allosteric regulation of the alpha X beta 2 integrin I domain, Proc. Natl. Acad. Sci. USA, 100, 1873, 10.1073/pnas.0237387100 Vorup-Jensen, 2007, The connection between metal ion affinity and ligand affinity in integrin I domains, Biochim. Biophys. Acta, 1774, 1148, 10.1016/j.bbapap.2007.06.014 Whittaker, 2002, Distribution and evolution of von Willebrand/integrin A domains: widely dispersed domains with roles in cell adhesion and elsewhere, Mol. Biol. Cell, 13, 3369, 10.1091/mbc.e02-05-0259 Wriggers, 2001, Using Situs for the registration of protein structures with low-resolution bead models from X-ray solution scattering, J. Appl. Cryst., 34, 773, 10.1107/S0021889801012869 Wu, 2015, Structure of the voltage-gated calcium channel Cav1.1 complex, Science, 350, aad2395, 10.1126/science.aad2395 Wu, 2016, Structure of the voltage-gated calcium channel Ca(v)1.1 at 3.6 Å resolution, Nature, 537, 191, 10.1038/nature19321 Young, 2007, Amelioration of cystic fibrosis intestinal mucous disease in mice by restoration of mCLCA3, Gastroenterology, 133, 1928, 10.1053/j.gastro.2007.10.007 Yurtsever, 2012, Self-cleavage of human CLCA1 protein by a novel internal metalloprotease domain controls calcium-activated chloride channel activation, J. Biol. Chem., 287, 42138, 10.1074/jbc.M112.410282 Zhang, 2009, Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor, Proc. Natl. Acad. Sci. USA, 106, 9226, 10.1073/pnas.0903679106