The 1.59Å resolution structure of the minor pseudopilin EpsH of Vibrio cholerae reveals a long flexible loop

Kannan Raghunathan1,2, Frank S. Vago1,2, David Grindem1,2, Terry Ball2,3, William J. Wedemeyer2,3,4, Michael Bagdasarian1,2, Dennis N. Arvidson1,2
1Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA
2Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA
3Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA
4Department of Physics and Astronomy, Michigan State University, East Lansing, MI 48824, USA

Tài liệu tham khảo

Pohlschroder, 2005, Diversity and evolution of protein translocation, Annu. Rev. Microbiol., 59, 91, 10.1146/annurev.micro.59.030804.121353 Papanikou, 2007, Bacterial protein secretion through the translocase nanomachine, Nat. Rev. Microbiol., 5, 839, 10.1038/nrmicro1771 Sargent, 2007, The twin-arginine transport system: moving folded proteins across membranes, Biochem. Soc. Trans., 35, 835, 10.1042/BST0350835 Filloux, 2004, The underlying mechanisms of type II protein secretion, Biochim. Biophys. Acta, 1694, 163, 10.1016/j.bbamcr.2004.05.003 Sandkvist, 2001, Type II secretion and pathogenesis, Infect. Immun., 69, 3523, 10.1128/IAI.69.6.3523-3535.2001 Sandkvist, 2001, Biology of type II secretion, Mol. Microbiol., 40, 271, 10.1046/j.1365-2958.2001.02403.x Sikora, 2011, Proteomic analysis of the Vibrio cholerae type II secretome reveals new proteins, including three related serine proteases, J. Biol. Chem., 286, 16555, 10.1074/jbc.M110.211078 Douzi, 2012, On the path to uncover the bacterial type II secretion system, Philos. Trans. R. Soc. Lond. B Biol. Sci., 367, 1059, 10.1098/rstb.2011.0204 Campos, 2013, The type II secretion system—a dynamic fiber assembly nanomachine, Res. Microbiol., 164, 545, 10.1016/j.resmic.2013.03.013 McLaughlin, 2012, Structural insights into the type II secretion nanomachine, Curr. Opin. Struct. Biol., 22, 208, 10.1016/j.sbi.2012.02.005 Korotkov, 2012, The type II secretion system: biogenesis, molecular architecture and mechanism, Nat. Rev. Microbiol., 10, 336, 10.1038/nrmicro2762 Sandkvist, 1997, General secretion pathway (eps) genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae, J. Bacteriol., 179, 6994, 10.1128/jb.179.22.6994-7003.1997 Peabody, 2003, Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella, Microbiology, 149, 3051, 10.1099/mic.0.26364-0 Campos, 2010, Detailed structural and assembly model of the type II secretion pilus from sparse data, Proc. Natl. Acad. Sci. U. S. A., 107, 13081, 10.1073/pnas.1001703107 Marsh, 1998, Identification of the Vibrio cholerae type 4 prepilin peptidase required for cholera toxin secretion and pilus formation, Mol. Microbiol., 29, 1481, 10.1046/j.1365-2958.1998.01031.x Hobbs, 1993, Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes, Mol. Microbiol., 10, 233, 10.1111/j.1365-2958.1993.tb01949.x Nunn, 1999, Bacterial type II protein export and pilus biogenesis: more than just homologies?, Trends Cell Biol., 9, 402, 10.1016/S0962-8924(99)01634-7 Shevchik, 1997, Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins, EMBO J., 16, 3007, 10.1093/emboj/16.11.3007 Durand, 2003, Type II protein secretion in Pseudomonas aeruginosa: the pseudopilus is a multifibrillar and adhesive structure, J. Bacteriol., 185, 2749, 10.1128/JB.185.9.2749-2758.2003 Durand, 2011, The assembly mode of the pseudopilus: a hallmark to distinguish a novel secretion system subtype, J. Biol. Chem., 286, 24407, 10.1074/jbc.M111.234278 Kohler, 2004, Structure and assembly of the pseudopilin PulG, Mol. Microbiol., 54, 647, 10.1111/j.1365-2958.2004.04307.x Yanez, 2008, Structure of the minor pseudopilin EpsH from the type 2 secretion system of Vibrio cholerae, J. Mol. Biol., 377, 91, 10.1016/j.jmb.2007.08.041 Craig, 2003, Type IV pilin structure and assembly. X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin, Mol. Cell, 11, 1139, 10.1016/S1097-2765(03)00170-9 Keizer, 2001, Structure of a pilin monomer from Pseudomonas aeruginosa: implications for the assembly of pili, J. Biol. Chem., 276, 24186, 10.1074/jbc.M100659200 Parge, 1995, Structure of the fibre-forming protein pilin at 2.6 A resolution, Nature, 378, 32, 10.1038/378032a0 Korotkov, 2008, Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system, Nat. Struct. Mol. Biol., 15, 462, 10.1038/nsmb.1426 Reichow, 2010, Structure of the cholera toxin secretion channel in its closed state, Nat. Struct. Mol. Biol., 17, 1226, 10.1038/nsmb.1910 Douzi, 2009, The XcpV/GspI pseudopilin has a central role in the assembly of a quaternary complex within the T2SS pseudopilus, J. Biol. Chem., 284, 34580, 10.1074/jbc.M109.042366 Kuo, 2005, Roles of the minor pseudopilins, XpsH, XpsI and XpsJ, in the formation of XpsG-containing pseudopilus in Xanthomonas campestris pv. campestris, J. Biomed. Sci., 12, 587, 10.1007/s11373-005-7372-3 Cisneros, 2011, Minor pseudopilin self-assembly primes type II secretion pseudopilus elongation, EMBO J., 31, 1041, 10.1038/emboj.2011.454 Douzi, 2011, Deciphering the Xcp Pseudomonas aeruginosa type II secretion machinery through multiple interactions with substrates, J. Biol. Chem., 286, 40792, 10.1074/jbc.M111.294843 Hazes, 2000, Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main- chain-dominated mode of receptor binding, J. Mol. Biol., 299, 1005, 10.1006/jmbi.2000.3801 Raghunathan, 2009, Expression, purification, crystallization and preliminary X-ray studies of Vibrio cholerae pseudopilin EpsH, Acta Crystallogr. F, 65, 702, 10.1107/S1744309109020454 Sandkvist, 1994, 293 Hirel, 1989, Extent of N-terminal methionine excision from Escherichia coli proteins is governed by the side-chain length of the penultimate amino acid, Proc. Natl. Acad. Sci. U. S. A., 86, 8247, 10.1073/pnas.86.21.8247 Otwinowski, 1997, 307, 10.1016/S0076-6879(97)76066-X Matthews, 1968, Solvent content of protein crystals, J. Mol. Biol., 33, 491, 10.1016/0022-2836(68)90205-2 Vagin, 1997, MOLREP: an automated program for molecular replacement, J. Appl. Crystallogr., 30, 1022, 10.1107/S0021889897006766 Langer, 2008, Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7, Nat. Protoc., 3, 1171, 10.1038/nprot.2008.91 Emsley, 2010, Features and development of Coot, Acta Crystallogr. D, 66, 486, 10.1107/S0907444910007493 Murshudov, 1997, Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D, 53, 240, 10.1107/S0907444996012255 N. Collaborative Computational Project, 1994, The CCP4 suite: programs for protein crystallography, Acta Crystallogr. D, 50, 760, 10.1107/S0907444994003112 Winn, 2001, Use of TLS parameters to model anisotropic displacements in macromolecular refinement, Acta Crystallogr. D, 57, 122, 10.1107/S0907444900014736 Painter, 2006, TLSMD web server for the generation of multi-group TLS models, J. Appl. Crystallogr., 39, 109, 10.1107/S0021889805038987 Chen, 2010, MolProbity: all-atom structure validation for macromolecular crystallography, Acta Crystallogr. D Biol. Crystallogr., 66, 12, 10.1107/S0907444909042073 Kabsch, 1983, Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features, Biopolymers, 22, 2577, 10.1002/bip.360221211 Poirot, 2004, 3DCoffee@igs: a web server for combining sequences and structures into a multiple sequence alignment, Nucleic Acids Res., 32, W37, 10.1093/nar/gkh382 Shi, 2001, FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties, J. Mol. Biol., 310, 243, 10.1006/jmbi.2001.4762 Bond, 2009, ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments, Acta Crystallogr. D, 65, 510, 10.1107/S0907444909007835 Bond, 2003, TopDraw: a sketchpad for protein structure topology cartoons, Bioinformatics, 19, 311, 10.1093/bioinformatics/19.2.311 The PyMol Molecular Graphics System, Version 1.5.0.3, Schrödinger, LLC. McNicholas, 2011, Presenting your structures: the CCP4mg molecular-graphics software, Acta Crystallogr. D, 67, 386, 10.1107/S0907444911007281 Kirn, 2000, Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae, Mol. Microbiol., 35, 896, 10.1046/j.1365-2958.2000.01764.x Craig, 2006, Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions, Mol. Cell, 23, 651, 10.1016/j.molcel.2006.07.004 Li, 2008, Vibrio cholerae toxin-coregulated pilus structure analyzed by hydrogen/deuterium exchange mass spectrometry, Structure, 16, 137, 10.1016/j.str.2007.10.027 Debroy, 2006, Legionella pneumophila Mip, a surface-exposed peptidylproline cis-trans-isomerase, promotes the presence of phospholipase C-like activity in culture supernatants, Infect. Immun., 74, 5152, 10.1128/IAI.00484-06 Vignon, 2003, Type IV-like pili formed by the type II secreton: specificity, composition, bundling, polar localization, and surface presentation of peptides, J. Bacteriol., 185, 3416, 10.1128/JB.185.11.3416-3428.2003 Durand, 2005, XcpX controls biogenesis of the Pseudomonas aeruginosa XcpT-containing pseudopilus, J. Biol. Chem., 280, 31378, 10.1074/jbc.M505812200 Dunker, 2008, The unfoldomics decade: an update on intrinsically disordered proteins, BMC Genomics, 9, S1, 10.1186/1471-2164-9-S2-S1