Structural Variability of EspG Chaperones from Mycobacterial ESX-1, ESX-3, and ESX-5 Type VII Secretion Systems

Tuukkanen, Anne T.; Freire, Diana; Chan, Sum; Arbing, Mark A.; Reed, Robert W.; Evans, Timothy J.; Zenkeviciutė, Grasilda; Kim, Jennifer; Kahng, Sara; Sawaya, Michael R.; Chaton, Catherine T.; Wilmanns, Matthias; Eisenberg, David; Parret, Annabel H.A.; Korotkov, Konstantin V.

doi:10.1016/j.jmb.2018.11.003

Title: Structural Variability of EspG Chaperones from Mycobacterial ESX-1, ESX-3, and ESX-5 Type VII Secretion Systems

Journal Article · 09 November 2018 · Journal of Molecular Biology

DOI: https://doi.org/10.1016/j.jmb.2018.11.003 · OSTI ID:1506496

Tuukkanen, Anne T. ^[1]; Freire, Diana ^[1]; Chan, Sum ^[2]; Arbing, Mark A. ^[2]; Reed, Robert W. ^[3]; Evans, Timothy J. ^[3]; Zenkeviciutė, Grasilda ^[1]; Kim, Jennifer ^[2]; Kahng, Sara ^[2]; Sawaya, Michael R. ^[2]; Chaton, Catherine T. ^[3]; Wilmanns, Matthias ^[1]; Eisenberg, David ^[2];

^[1];

^[3]

European Molecular Biology Lab. (EMBL), Hamburg (France)
Univ. of California, Los Angeles, CA (United States). UCLA-DOE Inst.
Univ. of Kentucky, Lexington, KY (United States). Center for Structural Biology

Type VII secretion systems (ESX) are responsible for transport of multiple proteins in mycobacteria. How different ESX systems achieve specific secretion of cognate substrates remains elusive. In the ESX systems, the cytoplasmic chaperone EspG forms complexes with heterodimeric PE–PPE substrates that are secreted from the cells or remain associated with the cell surface. Here we report the crystal structure of the EspG₁ chaperone from the ESX-1 system determined using a fusion strategy with T4 lysozyme. EspG₁ adopts a quasi 2-fold symmetric structure that consists of a central β-sheet and two α-helical bundles. In addition, we describe the structures of EspG₃ chaperones from four different crystal forms. Alternate conformations of the putative PE–PPE binding site are revealed by comparison of the available EspG₃ structures. Analysis of EspG₁, EspG₃, and EspG₅ chaperones using small-angle X-ray scattering reveals that EspG₁ and EspG₃ chaperones form dimers in solution, which we observed in several of our crystal forms. Finally, we propose a model of the ESX-3 specific EspG₃–PE5–PPE4 complex based on the small-angle X-ray scattering analysis.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Howard Hughes Medical Institute (HHMI); National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: FC02-02ER63421; W-31109-ENG-38

OSTI ID:: 1506496

Journal Information:: Journal of Molecular Biology, Journal Name: Journal of Molecular Biology Journal Issue: 2 Vol. 431; ISSN 0022-2836

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (85)

Scalable molecular dynamics with NAMD Phillips, James C.; Braun, Rosemary; Wang, Wei Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802 https://doi.org/10.1002/jcc.20289	journal	January 2005
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
Enzymatic Assembly of Overlapping DNA Fragments Gibson, Daniel G. Methods in Enzymology https://doi.org/10.1016/B978-0-12-385120-8.00015-2	book	May 2011
Take five — Type VII secretion systems of Mycobacteria Houben, Edith N. G.; Korotkov, Konstantin V.; Bitter, Wilbert Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1843, Issue 8 https://doi.org/10.1016/j.bbamcr.2013.11.003	journal	August 2014
Substrates Control Multimerization and Activation of the Multi-Domain ATPase Motor of Type VII Secretion Rosenberg, Oren S.; Dovala, Dustin; Li, Xueming Cell, Vol. 161, Issue 3 https://doi.org/10.1016/j.cell.2015.03.040	journal	April 2015
Strong Immunogenicity and Cross-Reactivity of Mycobacterium tuberculosis ESX-5 Type VII Secretion -Encoded PE-PPE Proteins Predicts Vaccine Potential Sayes, Fadel; Sun, Lin; Di Luca, Mariagrazia Cell Host & Microbe, Vol. 11, Issue 4 https://doi.org/10.1016/j.chom.2012.03.003	journal	April 2012
Linked Domain Architectures Allow for Specialization of Function in the FtsK/SpoIIIE ATPases of ESX Secretion Systems Ramsdell, Talia L.; Huppert, Laura A.; Sysoeva, Tatyana A. Journal of Molecular Biology, Vol. 427, Issue 5 https://doi.org/10.1016/j.jmb.2014.06.013	journal	March 2015
Structural Characterization of Flexible Proteins Using Small-Angle X-ray Scattering Bernadó, Pau; Mylonas, Efstratios; Petoukhov, Maxim V. Journal of the American Chemical Society, Vol. 129, Issue 17 https://doi.org/10.1021/ja069124n	journal	May 2007
All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins ^† MacKerell, A. D.; Bashford, D.; Bellott, M. The Journal of Physical Chemistry B, Vol. 102, Issue 18 https://doi.org/10.1021/jp973084f	journal	April 1998
Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Cole, S. T.; Brosch, R.; Parkhill, J. Nature, Vol. 396, Issue 6707 https://doi.org/10.1038/24206	journal	November 1998
Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence Cole, S. T.; Brosch, R.; Parkhill, J. Nature, Vol. 393, Issue 6685 https://doi.org/10.1038/31159	journal	June 1998
Correlation Map, a goodness-of-fit test for one-dimensional X-ray scattering spectra Franke, Daniel; Jeffries, Cy M.; Svergun, Dmitri I. Nature Methods, Vol. 12, Issue 5 https://doi.org/10.1038/nmeth.3358	journal	April 2015
Structure of the mycobacterial ESX-5 type VII secretion system membrane complex by single-particle analysis Beckham, Katherine S. H.; Ciccarelli, Luciano; Bunduc, Catalin M. Nature Microbiology, Vol. 2, Issue 6 https://doi.org/10.1038/nmicrobiol.2017.47	journal	April 2017
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7 Langer, Gerrit; Cohen, Serge X.; Lamzin, Victor S. Nature Protocols, Vol. 3, Issue 7 https://doi.org/10.1038/nprot.2008.91	journal	June 2008
Tuberculosis Pai, Madhukar; Behr, Marcel A.; Dowdy, David Nature Reviews Disease Primers, Vol. 2, Issue 1 https://doi.org/10.1038/nrdp.2016.76	journal	October 2016
ESX secretion systems: mycobacterial evolution to counter host immunity Gröschel, Matthias I.; Sayes, Fadel; Simeone, Roxane Nature Reviews Microbiology, Vol. 14, Issue 11 https://doi.org/10.1038/nrmicro.2016.131	journal	September 2016
Type VII secretion — mycobacteria show the way Abdallah, Abdallah M.; Gey van Pittius, Nicolaas C.; DiGiuseppe Champion, Patricia A. Nature Reviews Microbiology, Vol. 5, Issue 11 https://doi.org/10.1038/nrmicro1773	journal	November 2007
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
NELL2-Robo3 complex structure reveals mechanisms of receptor activation for axon guidance Pak, Joseph S.; DeLoughery, Zachary J.; Wang, Jing Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15211-1	journal	March 2020
Mechanism of pore opening in the calcium-activated chloride channel TMEM16A Lam, Andy K. M.; Dutzler, Raimund Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-020-20788-8	journal	February 2021
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Identification of a substrate domain that determines system specificity in mycobacterial type VII secretion systems Phan, Trang H.; Ummels, Roy; Bitter, Wilbert Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep42704	journal	February 2017
Are the PE-PGRS proteins of Mycobacterium tuberculosis variable surface antigens?: Role of PE-PGRS proteins of M. tuberculosis Banu, Sayera; Honoré, Nadine; Saint-Joanis, Brigitte Molecular Microbiology, Vol. 44, Issue 1 https://doi.org/10.1046/j.1365-2958.2002.02813.x	journal	April 2002
Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis: RD1 genes affect secretion and virulence of M. tuberculosis Guinn, Kristi M.; Hickey, Mark J.; Mathur, Sanjeev K. Molecular Microbiology, Vol. 51, Issue 2 https://doi.org/10.1046/j.1365-2958.2003.03844.x	journal	January 2004
La diffraction des rayons X aux très petits angles : application à l'étude de phénomènes ultramicroscopiques Guinier, André Annales de Physique, Vol. 11, Issue 12 https://doi.org/10.1051/anphys/193911120161	journal	January 1939
Comparison of simple potential functions for simulating liquid water Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D. The Journal of Chemical Physics, Vol. 79, Issue 2 https://doi.org/10.1063/1.445869	journal	July 1983
Mutually dependent secretion of proteins required for mycobacterial virulence Fortune, S. M.; Jaeger, A.; Sarracino, D. A. Proceedings of the National Academy of Sciences, Vol. 102, Issue 30 https://doi.org/10.1073/pnas.0504922102	journal	July 2005
Toward the structural genomics of complexes: Crystal structure of a PE/PPE protein complex from Mycobacterium tuberculosis Strong, M.; Sawaya, M. R.; Wang, S. Proceedings of the National Academy of Sciences, Vol. 103, Issue 21 https://doi.org/10.1073/pnas.0602606103	journal	May 2006
General secretion signal for the mycobacterial type VII secretion pathway Daleke, M. H.; Ummels, R.; Bawono, P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 28 https://doi.org/10.1073/pnas.1119453109	journal	June 2012
Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion Ekiert, D. C.; Cox, J. S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1409345111	journal	October 2014
Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system Stanley, S. A.; Raghavan, S.; Hwang, W. W. Proceedings of the National Academy of Sciences, Vol. 100, Issue 22 https://doi.org/10.1073/pnas.2235593100	journal	October 2003
Stabilization of phage T4 lysozyme by engineered disulfide bonds Matsumura, M.; Becktel, W. J.; Levitt, M. Proceedings of the National Academy of Sciences, Vol. 86, Issue 17 https://doi.org/10.1073/pnas.86.17.6562	journal	September 1989
Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) Protein Domains Target LipY Lipases of Pathogenic Mycobacteria to the Cell Surface via the ESX-5 Pathway Daleke, Maria H.; Cascioferro, Alessandro; de Punder, Karin Journal of Biological Chemistry, Vol. 286, Issue 21 https://doi.org/10.1074/jbc.M110.204966	journal	April 2011
Specific Chaperones for the Type VII Protein Secretion Pathway Daleke, Maria H.; van der Woude, Aniek D.; Parret, Annabel H. A. Journal of Biological Chemistry, Vol. 287, Issue 38 https://doi.org/10.1074/jbc.M112.397596	journal	July 2012
Structural basis of the PE–PPE protein interaction in Mycobacterium tuberculosis Chen, Xin; Cheng, Hiu-fu; Zhou, Junwei Journal of Biological Chemistry, Vol. 292, Issue 41 https://doi.org/10.1074/jbc.M117.802645	journal	August 2017
Deletion of RD1 from Mycobacterium tuberculosis Mimics Bacille Calmette‐Guérin Attenuation Lewis, Kaeryn N.; Liao, Reiling; Guinn, Kristi M. The Journal of Infectious Diseases, Vol. 187, Issue 1 https://doi.org/10.1086/345862	journal	January 2003
ZDOCK server: interactive docking prediction of protein-protein complexes and symmetric multimers Pierce, B. G.; Wiehe, K.; Hwang, H. Bioinformatics, Vol. 30, Issue 12 https://doi.org/10.1093/bioinformatics/btu097	journal	February 2014
Bacterial secretion chaperones: the mycobacterial type VII case Phan, Trang H.; Houben, Edith N. G. FEMS Microbiology Letters, Vol. 365, Issue 18 https://doi.org/10.1093/femsle/fny197	journal	August 2018
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew Nucleic Acids Research, Vol. 42, Issue W1 https://doi.org/10.1093/nar/gku340	journal	April 2014
Inhibiting Mycobacterium tuberculosis within and without Cole, Stewart T. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 371, Issue 1707 https://doi.org/10.1098/rstb.2015.0506	journal	November 2016
Uniqueness of ab initio shape determination in small-angle scattering Volkov, Vladimir V.; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 36, Issue 3, p. 860-864 https://doi.org/10.1107/S0021889803000268	journal	April 2003
PRIMUS: a Windows PC-based system for small-angle scattering data analysis Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V. Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282 https://doi.org/10.1107/S0021889803012779	journal	September 2003
HKL2MAP : a graphical user interface for macromolecular phasing with SHELX programs Pape, Thomas; Schneider, Thomas R. Journal of Applied Crystallography, Vol. 37, Issue 5 https://doi.org/10.1107/S0021889804018047	journal	September 2004
TLSMD web server for the generation of multi-group TLS models Painter, Jay; Merritt, Ethan A. Journal of Applied Crystallography, Vol. 39, Issue 1 https://doi.org/10.1107/S0021889805038987	journal	January 2006
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering Franke, Daniel; Svergun, Dmitri I. Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346 https://doi.org/10.1107/S0021889809000338	journal	January 2009
New developments in the ATSAS program package for small-angle scattering data analysis Petoukhov, Maxim V.; Franke, Daniel; Shkumatov, Alexander V. Journal of Applied Crystallography, Vol. 45, Issue 2 https://doi.org/10.1107/S0021889812007662	journal	March 2012
Determination of the regularization parameter in indirect-transform methods using perceptual criteria Svergun, D. I. Journal of Applied Crystallography, Vol. 25, Issue 4, p. 495-503 https://doi.org/10.1107/S0021889892001663	journal	August 1992
CRYSOL – a Program to Evaluate X-ray Solution Scattering of Biological Macromolecules from Atomic Coordinates Svergun, D.; Barberato, C.; Koch, M. H. J. Journal of Applied Crystallography, Vol. 28, Issue 6 https://doi.org/10.1107/S0021889895007047	journal	December 1995
A short history of SHELX Sheldrick, George M. Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122 https://doi.org/10.1107/S0108767307043930	journal	December 2007
Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Painter, Jay; Merritt, Ethan A. Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 4 https://doi.org/10.1107/S0907444906005270	journal	March 2006
The Buccaneer software for automated model building. 1. Tracing protein chains Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9 https://doi.org/10.1107/S0907444906022116	journal	August 2006
Fitting molecular fragments into electron density Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S0907444907033938	journal	December 2007
Experimental phasing with SHELXC / D / E : combining chain tracing with density modification Sheldrick, George M. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444909038360	journal	March 2010
Recent developments in classical density modification Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S090744490903947X	journal	March 2010
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
Versatile sample environments and automation for biological solution X-ray scattering experiments at the P12 beamline (PETRA III, DESY) Blanchet, Clement E.; Spilotros, Alessandro; Schwemmer, Frank Journal of Applied Crystallography, Vol. 48, Issue 2 https://doi.org/10.1107/S160057671500254X	journal	March 2015
Advanced ensemble modelling of flexible macromolecules using X-ray solution scattering Tria, Giancarlo; Mertens, Haydyn D. T.; Kachala, Michael IUCrJ, Vol. 2, Issue 2 https://doi.org/10.1107/S205225251500202X	journal	February 2015
Resolution of ab initio shapes determined from small-angle scattering Tuukkanen, Anne T.; Kleywegt, Gerard J.; Svergun, Dmitri I. IUCrJ, Vol. 3, Issue 6 https://doi.org/10.1107/S2052252516016018	journal	October 2016
A specific secretion system mediates PPE41 transport in pathogenic mycobacteria Abdallah, Abdallah M.; Verboom, Theo; Hannes, Fredericke Molecular Microbiology, Vol. 62, Issue 3 https://doi.org/10.1111/j.1365-2958.2006.05409.x	journal	September 2006
PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5 Abdallah, Abdallah M.; Verboom, Theo; Weerdenburg, Eveline M. Molecular Microbiology, Vol. 73, Issue 3 https://doi.org/10.1111/j.1365-2958.2009.06783.x	journal	August 2009
Disruption of the ESX-5 system of Mycobacterium tuberculosis causes loss of PPE protein secretion, reduction of cell wall integrity and strong attenuation: ESX-5 of M. tuberculosis Bottai, Daria; Di Luca, Mariagrazia; Majlessi, Laleh Molecular Microbiology, Vol. 83, Issue 6 https://doi.org/10.1111/j.1365-2958.2012.08001.x	journal	February 2012
Composition of the type VII secretion system membrane complex: Composition of the T7S membrane complex Houben, Edith N. G.; Bestebroer, Jovanka; Ummels, Roy Molecular Microbiology, Vol. 86, Issue 2 https://doi.org/10.1111/j.1365-2958.2012.08206.x	journal	August 2012
A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice: PPE gene and M. avium virulence Li, Yongjun; Miltner, Elizabeth; Wu, Martin Cellular Microbiology, Vol. 7, Issue 4 https://doi.org/10.1111/j.1462-5822.2004.00484.x	journal	December 2004
Structure of the M ycobacterium tuberculosis type VII secretion system chaperone EspG ₅ in complex with PE25-PPE41 dimer : Type VII secretion chaperone and PE-PPE dimer Korotkova, Natalia; Freire, Diana; Phan, Trang H. Molecular Microbiology, Vol. 94, Issue 2 https://doi.org/10.1111/mmi.12770	journal	September 2014
GPCR Engineering Yields High-Resolution Structural Insights into 2-Adrenergic Receptor Function Rosenbaum, D. M.; Cherezov, V.; Hanson, M. A. Science, Vol. 318, Issue 5854 https://doi.org/10.1126/science.1150609	journal	October 2007
Linking Crystallographic Model and Data Quality Karplus, P. A.; Diederichs, K. Science, Vol. 336, Issue 6084 https://doi.org/10.1126/science.1218231	journal	May 2012
Evidence that Mycobacterial PE_PGRS Proteins Are Cell Surface Constituents That Influence Interactions with Other Cells Brennan, Michael J.; Delogu, Giovanni; Chen, Yiping Infection and Immunity, Vol. 69, Issue 12 https://doi.org/10.1128/IAI.69.12.7326-7333.2001	journal	December 2001
Comparative Immune Response to PE and PE_PGRS Antigens of Mycobacterium tuberculosis Delogu, Giovanni; Brennan, Michael J. Infection and Immunity, Vol. 69, Issue 9 https://doi.org/10.1128/IAI.69.9.5606-5611.2001	journal	September 2001
Mycosins Are Required for the Stabilization of the ESX-1 and ESX-5 Type VII Secretion Membrane Complexes van Winden, Vincent J. C.; Ummels, Roy; Piersma, Sander R. mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.01471-16	journal	November 2016
ESX-1-Independent Horizontal Gene Transfer by Mycobacterium tuberculosis Complex Strains Madacki, Jan; Orgeur, Mickael; Mas Fiol, Guillem mBio, Vol. 12, Issue 3 https://doi.org/10.1128/mbio.00965-21	journal	June 2021
N-Terminal T4 Lysozyme Fusion Facilitates Crystallization of a G Protein Coupled Receptor Zou, Yaozhong; Weis, William I.; Kobilka, Brian K. PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046039	journal	October 2012
Heterologous Expression of Mycobacterial Esx Complexes in Escherichia coli for Structural Studies Is Facilitated by the Use of Maltose Binding Protein Fusions Arbing, Mark A.; Chan, Sum; Harris, Liam PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0081753	journal	November 2013
WXG100 Protein Superfamily Consists of Three Subfamilies and Exhibits an α-Helical C-Terminal Conserved Residue Pattern Poulsen, Christian; Panjikar, Santosh; Holton, Simon J. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0089313	journal	February 2014
Direct Visualization by Cryo-EM of the Mycobacterial Capsular Layer: A Labile Structure Containing ESX-1-Secreted Proteins Sani, Musa; Houben, Edith N. G.; Geurtsen, Jeroen PLoS Pathogens, Vol. 6, Issue 3 https://doi.org/10.1371/journal.ppat.1000794	journal	March 2010
Automated Structure Solution With autoSHARP Vonrhein, Clemens; Blanc, Eric; Roversi, Pietro Macromolecular Crystallography Protocols, Volume 2 https://doi.org/10.1385/1-59745-266-1:215	book	January 2006
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Structure of the mycobacterial ESX-5 type VII secretion system membrane complex by single-particle analysis Beckham, Katherine S. H.; Ciccarelli, Luciano; Bunduc, Catalin M. Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2017-01665	text	January 2017
SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information Biasini, Marco; Bienert, Stefan; Waterhouse, Andrew Oxford University Press https://doi.org/10.5451/unibas-ep34396	text	January 2014

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Title: Structural Variability of EspG Chaperones from Mycobacterial ESX-1, ESX-3, and ESX-5 Type VII Secretion Systems

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