Structure of thrombospondin type 3 repeats in bacterial outer membrane protein A reveals its intra-repeat disulfide bond-dependent calcium-binding capability

Cell Calcium - Tập 66 - Trang 78-89 - 2017
Shuyan Dai1, Cancan Sun1,2, Kemin Tan3, Sheng Ye1, Rongguang Zhang1,4
1National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, People’s Republic of China
2University of Chinese Academy of Sciences, Beijing 100049, People’s Republic of China
3Structural Biology Center, Biosciences, Argonne National Laboratory, 9700 S Cass Avenue, Argonne, IL 60439, USA
4National Center for Protein Science Shanghai, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 201203, People’s Republic of China

Tài liệu tham khảo

Permyakov, 2009, Cell signaling: beyond cytosolic calcium in eukaryotes, J. Inorg. Biochem., 103, 77, 10.1016/j.jinorgbio.2008.09.006 Berridge, 2003, Calcium signalling: dynamics: homeostasis and remodelling, Nat. Rev. Mol. Cell Biol., 4, 517, 10.1038/nrm1155 Dominguez, 2015, Calcium binding proteins and calcium signaling in prokaryotes, Cell Calcium, 57, 151, 10.1016/j.ceca.2014.12.006 Gangola, 1987, Maintenance of intracellular calcium in Escherichia coli, J. Biol. Chem., 262, 12570, 10.1016/S0021-9258(18)45243-X Jones, 1999, Slow changes in cytosolic free Ca2+ in Escherichia coli highlight two putative influx mechanisms in response to changes in extracellular calcium, Cell Calcium, 25, 265, 10.1054/ceca.1999.0028 Torrecilla, 2000, Use of recombinant aequorin to study calcium homeostasis and monitor calcium transients in response to heat and cold shock in cyanobacteria, Plant Physiol., 123, 161, 10.1104/pp.123.1.161 Clapham, 2007, Calcium signaling, Cell, 131, 1047, 10.1016/j.cell.2007.11.028 Chang, 1986, Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells, J. Bacteriol., 167, 935, 10.1128/jb.167.3.935-939.1986 Jones, 2002, Direct measurement of free Ca(2+) shows different regulation of Ca(2+) between the periplasm and the cytosol of Escherichia coli, Cell Calcium, 32, 183, 10.1016/S0143416002001537 Tossavainen, 2003, NMR solution structure of calerythrin: an EF-hand calcium-binding protein from Saccharopolyspora erythraea, Eur. J. Biochem., 270, 2505, 10.1046/j.1432-1033.2003.03623.x Lytle, 2001, Solution structure of a type I dockerin domain a novel prokaryotic, extracellular calcium-binding domain, J. Mol. Biol., 307, 745, 10.1006/jmbi.2001.4522 Aghajari, 2003, Crystal structures of a psychrophilic metalloprotease reveal new insights into catalysis by cold-adapted proteases, Proteins, 50, 636, 10.1002/prot.10264 Barnwal, 2009, Solution structure and calcium-binding properties of M-crystallin: a primordial betagamma-crystallin from archaea, J. Mol. Biol., 386, 675, 10.1016/j.jmb.2008.12.058 Kvansakul, 2004, Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats, EMBO J., 23, 1223, 10.1038/sj.emboj.7600166 Rigden, 2004, The DxDxDG motif for calcium binding: multiple structural contexts and implications for evolution, J. Mol. Biol., 343, 971, 10.1016/j.jmb.2004.08.077 Armstrong, 2003, Thrombospondins 1 and 2 function as inhibitors of angiogenesis, Matrix Biol., 22, 63, 10.1016/S0945-053X(03)00005-2 Adams, 2011, The thrombospondins, Cold Spring Harb. Perspect. Biol., 3, a009712, 10.1101/cshperspect.a009712 Tan, 2009, The crystal structure of the signature domain of cartilage oligomeric matrix protein: implications for collagen, glycosaminoglycan and integrin binding, FASEB J., 23, 2490, 10.1096/fj.08-128090 Carlson, 2005, Structure of the calcium-rich signature domain of human thrombospondin-2, Nat. Struct. Mol. Biol., 12, 910, 10.1038/nsmb997 Feller, 2003, Psychrophilic enzymes: hot topics in cold adaptation, Nat. Rev. Microbiol., 1, 200, 10.1038/nrmicro773 Violot, 2005, Structure of a full length psychrophilic cellulase from Pseudoalteromonas haloplanktis revealed by X-ray diffraction and small angle X-ray scattering, J. Mol. Biol., 348, 1211, 10.1016/j.jmb.2005.03.026 Sonan, 2007, The linker region plays a key role in the adaptation to cold of the cellulase from an Antarctic bacterium, Biochem. J, 407, 293, 10.1042/BJ20070640 Koebnik, 2000, Structure and function of bacterial outer membrane proteins: barrels in a nutshell, Mol. Microbiol., 37, 239, 10.1046/j.1365-2958.2000.01983.x Krishnan, 2012, Outer membrane protein A and OprF: versatile roles in Gram-negative bacterial infections, FEBS J., 279, 919, 10.1111/j.1742-4658.2012.08482.x Confer, 2013, The OmpA family of proteins: roles in bacterial pathogenesis and immunity, Vet. Microbiol., 163, 207, 10.1016/j.vetmic.2012.08.019 Pautsch, 1998, Structure of the outer membrane protein A transmembrane domain, Nat. Struct. Biol., 5, 1013, 10.1038/2983 Pautsch, 2000, High-resolution structure of the OmpA membrane domain, J. Mol. Biol., 298, 273, 10.1006/jmbi.2000.3671 Park, 2012, Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane, FASEB J., 26, 219, 10.1096/fj.11-188425 Abergel, 2001, Crystallization and preliminary crystallographic study of the peptidoglycan-associated lipoprotein from Escherichia coli, Acta Crystallogr. D Biol. Crystallogr., 57, 317, 10.1107/S0907444900019739 Leadbetter, 1979, Capnocytophaga: new genus of gram-negative gliding bacteria. I. General characteristics: taxonomic considerations and significance, Arch. Microbiol., 122, 9, 10.1007/BF00408040 Zheng, 2014, Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server, Nat. Protoc., 9, 156, 10.1038/nprot.2013.172 Krissinel, 2007, Inference of macromolecular assemblies from crystalline state, J. Mol. Biol., 372, 774, 10.1016/j.jmb.2007.05.022 Zondlo, 2013, Aromatic-proline interactions: electronically tunable CH/pi interactions, Acc. Chem. Res., 46, 1039, 10.1021/ar300087y Adams, 2004, Functions of the conserved thrombospondin carboxy-terminal cassette in cell-extracellular matrix interactions and signaling, Int. J. Biochem. Cell Biol., 36, 1102, 10.1016/j.biocel.2004.01.022 Lawler, 1982, Evidence for calcium-sensitive structure in platelet thrombospondin: isolation and partial characterization of thrombospondin in the presence of calcium, J. Biol. Chem., 257, 12257, 10.1016/S0021-9258(18)33709-8 Lawler, 1985, The structure of human platelet thrombospondin, J. Biol. Chem., 260, 3762, 10.1016/S0021-9258(19)83689-X Misenheimer, 1995, Calcium ion binding to thrombospondin 1, J. Biol. Chem., 270, 1729, 10.1074/jbc.270.4.1729 Womack, 1989, Calcium requirement for gliding motility in myxobacteria, J. Bacteriol., 171, 6093, 10.1128/jb.171.11.6093-6096.1989 Lauritzen, 1991, BPTI and N-terminal extended analogues generated by factor Xa cleavage and cathepsin C trimming of a fusion protein expressed in Escherichia coli, Protein Expr. Purif., 2, 372, 10.1016/1046-5928(91)90096-2 Minor, 2006, HKL-3000: the integration of data reduction and structure solution--from diffraction images to an initial model in minutes Acta crystallographica. Section D, Biological crystallography., 62, 859, 10.1107/S0907444906019949 McCoy, 2007, Phaser crystallographic software, J. Appl. Crystallogr., 40, 658, 10.1107/S0021889807021206 Emsley, 2004, Coot: model-building tools for molecular graphics Acta crystallographica. Section D, Biological crystallography., 60, 2126, 10.1107/S0907444904019158 Afonine, 2012, Towards automated crystallographic structure refinement with phenix.refine, Acta Crystallogr. D Biol. Crystallogr., 68, 352, 10.1107/S0907444912001308 Phillips, 2005, Scalable molecular dynamics with NAMD, J. Comput. Chem., 26, 1781, 10.1002/jcc.20289 Humphrey, 1996, VMD: visual molecular dynamics, J. Mol. Graph., 14, 33, 10.1016/0263-7855(96)00018-5 Mackerell, 2000, Development and current status of the CHARMM force field for nucleic acids, Biopolymers, 56, 257, 10.1002/1097-0282(2000)56:4<257::AID-BIP10029>3.0.CO;2-W MacKerell, 1998, All-Atom empirical potential for molecular modeling and dynamics studies of proteins, J. Phys. Chem. B, 102, 3586, 10.1021/jp973084f Price, 2004, A modified TIP3P water potential for simulation with Ewald summation, J. Chem. Phys., 121, 10096, 10.1063/1.1808117 Darden, 1993, Particle mesh Ewald: an N⋅log(N) method for Ewald sums in large systems, J. Chem. Phys., 98, 10089, 10.1063/1.464397