Identification and characterization of a large family of superbinding bacterial SH2 domains

Kaneko, Tomonori; Stogios, Peter J.; Ruan, Xiang; Voss, Courtney; Evdokimova, Elena; Skarina, Tatiana; Chung, Amy; Liu, Xiaoling; Li, Lei; Savchenko, Alexei; Ensminger, Alexander W.; Li, Shawn S. -C.

doi:10.1038/s41467-018-06943-2

Title: Identification and characterization of a large family of superbinding bacterial SH2 domains

Journal Article · 31 October 2018 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-06943-2 · OSTI ID:1624120

^[1]; Stogios, Peter J. ^[2]; Ruan, Xiang ^[3]; Voss, Courtney ^[3]; Evdokimova, Elena ^[2]; Skarina, Tatiana ^[2]; Chung, Amy ^[4]; Liu, Xiaoling ^[3]; Li, Lei ^[5]; Savchenko, Alexei ^[6]; Ensminger, Alexander W. ^[4]; Li, Shawn S. -C. ^[7]

Western University, London (Canada). Department of Biochemistry, Schulich School of Medicine and Dentistry; DOE/OSTI
University of Toronto, Toronto (Canada). Department of Chemical Engineering and Applied Chemistry
Western University, London (Canada). Department of Biochemistry, Schulich School of Medicine and Dentistry
MaRS Centre, Toronto (Canada). Departments of Biochemistry and Molecular Genetics
Western University, London (Canada). Department of Biochemistry, Schulich School of Medicine and Dentistry; Qingdao University (China). Cancer institute, the Affiliated Hospital of Qingdao University, Qingdao Cancer Institute and School of Basic Medicine
University of Toronto, Toronto (Canada). Department of Chemical Engineering and Applied Chemistry; University of Calgary (Canada). Department of Microbiology, Immunology and Infectious Diseases
Western University, London (Canada). Department of Biochemistry, Schulich School of Medicine and Dentistry; Lawson Health Research Institute, London (Canada). Children’s Health Research Institute

Src homology 2 (SH2) domains play a critical role in signal transduction in mammalian cells by binding to phosphorylated Tyr (pTyr). Apart from a few isolated cases in viruses, no functional SH2 domain has been identified to date in prokaryotes. Here we identify 93 SH2 domains from Legionella that are distinct in sequence and specificity from mammalian SH2 domains. The bacterial SH2 domains are not only capable of binding proteins or peptides in a Tyr phosphorylation-dependent manner, some bind pTyr itself with micromolar affinities, a property not observed for mammalian SH2 domains. The Legionella SH2 domains feature the SH2 fold and a pTyr-binding pocket, but lack a specificity pocket found in a typical mammalian SH2 domain for recognition of sequences flanking the pTyr residue. Our work expands the boundary of phosphotyrosine signalling to prokaryotes, suggesting that some bacterial effector proteins have acquired pTyr-superbinding characteristics to facilitate bacterium-host interactions.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1624120

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 9; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (125)

Crystal structures of the SH2 domain of grb2: highlight on the binding of a new high-affinity inhibitor Nioche, Pierre; Liu, Wang-Qing; Broutin, Isabelle Journal of Molecular Biology, Vol. 315, Issue 5 https://doi.org/10.1006/jmbi.2001.5299	journal	February 2002
Host Cell Interactome of Tyrosine-Phosphorylated Bacterial Proteins Selbach, Matthias; Paul, Florian Ernst; Brandt, Sabine Cell Host & Microbe, Vol. 5, Issue 4 https://doi.org/10.1016/j.chom.2009.03.004	journal	April 2009
Perspective: Dynamics of receptor tyrosine kinase signaling complexes Mayer, Bruce J. FEBS Letters, Vol. 586, Issue 17 https://doi.org/10.1016/j.febslet.2012.05.002	journal	May 2012
Legionella pneumophila Dot/Icm translocated substrates: a sum of parts Ensminger, Alexander W.; Isberg, Ralph R. Current Opinion in Microbiology, Vol. 12, Issue 1 https://doi.org/10.1016/j.mib.2008.12.004	journal	February 2009
Legionella pneumophila, armed to the hilt: justifying the largest arsenal of effectors in the bacterial world Ensminger, Alexander W. Current Opinion in Microbiology, Vol. 29 https://doi.org/10.1016/j.mib.2015.11.002	journal	February 2016
Disease-Causing SAP Mutants Are Defective in Ligand Binding and Protein Folding ^† Li, Chengjun; Iosef, Cristiana; Jia, Christina Y. H. Biochemistry, Vol. 42, Issue 50 https://doi.org/10.1021/bi034798l	journal	December 2003
Recognition of a high-affinity phosphotyrosyl peptide by the Src homology-2 domain of p56lck Eck, Michael J.; Shoelson, Steven E.; Harrison, Stephen C. Nature, Vol. 362, Issue 6415 https://doi.org/10.1038/362087a0	journal	March 1993
SET‐domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription Li, Ting; Lu, Qiuhe; Wang, Guolun EMBO reports, Vol. 14, Issue 8 https://doi.org/10.1038/embor.2013.86	journal	June 2013
Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells Gruenheid, Samantha; DeVinney, Rebekah; Bladt, Friedhelm Nature Cell Biology, Vol. 3, Issue 9 https://doi.org/10.1038/ncb0901-856	journal	August 2001
Defining an allosteric circuit in the cysteine protease domain of Clostridium difficile toxins Shen, Aimee; Lupardus, Patrick J.; Gersch, Malte M. Nature Structural & Molecular Biology, Vol. 18, Issue 3 https://doi.org/10.1038/nsmb.1990	journal	February 2011
Repertoire-scale determination of class II MHC peptide binding via yeast display improves antigen prediction Rappazzo, C. Garrett; Huisman, Brooke D.; Birnbaum, Michael E. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-18204-2	journal	September 2020
Receptor binding and priming of the spike protein of SARS-CoV-2 for membrane fusion Benton, Donald J.; Wrobel, Antoni G.; Xu, Pengqi Nature, Vol. 588, Issue 7837 https://doi.org/10.1038/s41586-020-2772-0	journal	September 2020
Probable Person-to-Person Transmission of Legionnaires’ Disease Correia, Ana M.; Ferreira, Joana S.; Borges, Vítor New England Journal of Medicine, Vol. 374, Issue 5 https://doi.org/10.1056/nejmc1505356	journal	February 2016
Defining the Specificity Space of the Human Src Homology 2 Domain Huang, Haiming; Li, Lei; Wu, Chenggang Molecular & Cellular Proteomics, Vol. 7, Issue 4 https://doi.org/10.1074/mcp.m700312-mcp200	journal	October 2007
Two Dictyostelium tyrosine kinase–like kinases function in parallel, stress-induced STAT activation pathways Araki, Tsuyoshi; Vu, Linh Hai; Sasaki, Norimitsu Molecular Biology of the Cell, Vol. 25, Issue 20 https://doi.org/10.1091/mbc.e14-07-1182	journal	October 2014
Earliest Holozoan Expansion of Phosphotyrosine Signaling Suga, Hiroshi; Torruella, Guifré; Burger, Gertraud Molecular Biology and Evolution, Vol. 31, Issue 3 https://doi.org/10.1093/molbev/mst241	journal	December 2013
ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement Suhre, K.; Sanejouand, Y. -H. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh368	journal	July 2004
Prediction of phosphotyrosine signaling networks using a scoring matrix-assisted ligand identification approach Li, Lei; Wu, Chenggang; Huang, Haiming Nucleic Acids Research, Vol. 36, Issue 10 https://doi.org/10.1093/nar/gkn161	journal	April 2008
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
20 years of the SMART protein domain annotation resource Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx922	journal	October 2017
Evolution of SH2 domains and phosphotyrosine signalling networks Liu, Bernard A.; Nash, Piers D. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1602 https://doi.org/10.1098/rstb.2012.0107	journal	September 2012
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/s0907444906019949	journal	July 2006
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
Two substrate-targeting sites in the Yersinia protein tyrosine phosphatase co-operate to promote bacterial virulence: Mechanism of substrate targeting by Yersinia YopH Ivanov, Maya I.; Stuckey, Jeanne A.; Schubert, Heidi L. Molecular Microbiology, Vol. 55, Issue 5 https://doi.org/10.1111/j.1365-2958.2005.04477.x	journal	January 2005
The E Block motif is associated with Legionella pneumophila translocated substrates: Legionella C-terminal Signal Huang, Li; Boyd, Dana; Amyot, Whitney M. Cellular Microbiology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1462-5822.2010.01531.x	journal	November 2010
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
A Bacterial Tyrosine Phosphatase Inhibits Plant Pattern Recognition Receptor Activation Macho, A. P.; Schwessinger, B.; Ntoukakis, V. Science, Vol. 343, Issue 6178 https://doi.org/10.1126/science.1248849	journal	March 2014
Loops Govern SH2 Domain Specificity by Controlling Access to Binding Pockets Kaneko, T.; Huang, H.; Zhao, B. Science Signaling, Vol. 3, Issue 120 https://doi.org/10.1126/scisignal.2000796	journal	May 2010
Superbinder SH2 Domains Act as Antagonists of Cell Signaling Kaneko, T.; Huang, H.; Cao, X. Science Signaling, Vol. 5, Issue 243 https://doi.org/10.1126/scisignal.2003021	journal	September 2012
Heterogeneity in the Attachment and Uptake Mechanisms of the Legionnaires’ Disease Bacterium, Legionella pneumophila, by Protozoan Hosts Harb, Omar S.; Venkataraman, Chandrasekar; Haack, Bradley J. Applied and Environmental Microbiology, Vol. 64, Issue 1 https://doi.org/10.1128/aem.64.1.126-132.1998	journal	January 1998
E3 Ubiquitin Ligase Activity and Targeting of BAT3 by Multiple Legionella pneumophila Translocated Substrates Ensminger, A. W.; Isberg, R. R. Infection and Immunity, Vol. 78, Issue 9 https://doi.org/10.1128/iai.00344-10	journal	June 2010
DNA sequence of the viral and cellular src gene of chickens. II. Comparison of the src genes of two strains of avian sarcoma virus and of the cellular homolog. Takeya, T.; Hanafusa, H. Journal of Virology, Vol. 44, Issue 1 https://doi.org/10.1128/jvi.44.1.12-18.1982	journal	January 1982
Cell Regulation by Phosphotyrosine-Targeted Ubiquitin Ligases Cooper, Jonathan A.; Kaneko, Tomonori; Li, Shawn S. C. Molecular and Cellular Biology, Vol. 35, Issue 11 https://doi.org/10.1128/mcb.00098-15	journal	March 2015
Modulation of Host Cell Function by Legionella pneumophila Type IV Effectors Hubber, Andree; Roy, Craig R. Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1 https://doi.org/10.1146/annurev-cellbio-100109-104034	journal	November 2010
Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling Clarke, Michael; Lohan, Amanda J.; Liu, Bernard Genome Biology, Vol. 14, Issue 2 https://doi.org/10.1186/gb-2013-14-2-r11	journal	January 2013
Short linear motifs – ex nihilo evolution of protein regulation Davey, Norman E.; Cyert, Martha S.; Moses, Alan M. Cell Communication and Signaling, Vol. 13, Issue 1 https://doi.org/10.1186/s12964-015-0120-z	journal	November 2015
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Analysis of the Legionella longbeachae Genome and Transcriptome Uncovers Unique Strategies to Cause Legionnaires' Disease Cazalet, Christel; Gomez-Valero, Laura; Rusniok, Christophe PLoS Genetics, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pgen.1000851	journal	February 2010
Non-Opsonic Phagocytosis of Legionella pneumophila by Macrophages Is Mediated by Phosphatidylinositol 3-Kinase Tachado, Souvenir D.; Samrakandi, Mustapha M.; Cirillo, Jeffrey D. PLoS ONE, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pone.0003324	journal	October 2008
The Legionella pneumophila IcmSW Complex Interacts with Multiple Dot/Icm Effectors to Facilitate Type IV Translocation Cambronne, Eric D.; Roy, Craig R. PLoS Pathogens, Vol. 3, Issue 12 https://doi.org/10.1371/journal.ppat.0030188	journal	January 2007
Interactions of Bacterial Proteins with Host Eukaryotic Ubiquitin Pathways Perrett, Charlotte Averil; Lin, David Yin-Wei; Zhou, Daoguo Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00143	journal	January 2011
Comparative and Functional Genomics of Legionella Identified Eukaryotic Like Proteins as Key Players in Host?Pathogen Interactions Gomez-Valero, Laura; Rusniok, Christophe; Cazalet, Christel Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00208	journal	January 2011
Cross-phosphorylation of bacterial serine/threonine and tyrosine protein kinases on key regulatory residues Shi, Lei; Pigeonneau, Nathalie; Ravikumar, Vaishnavi Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00495	journal	September 2014
Conformational flexibility in a small globular hormone: X-ray analysis of avian pancreatic polypeptide at 0.98-Å resolution: CONFORMATION OF SMALL GLOBULAR HORMONE Glover, Ian; Haneef, Illyas; Pitts, Jim Biopolymers, Vol. 22, Issue 1 https://doi.org/10.1002/bip.360220138	journal	January 1983
A method for simultaneous alignment of multiple protein structures Shatsky, Maxim; Nussinov, Ruth; Wolfson, Haim J. Proteins: Structure, Function, and Bioinformatics, Vol. 56, Issue 1 https://doi.org/10.1002/prot.10628	journal	April 2004
Investigation of phosphotyrosine recognition by the SH2 domain of the Src kinase 1 1Edited by P. E. Wright Bradshaw, J. Michael; Mitaxov, Vesselin; Waksman, Gabriel Journal of Molecular Biology, Vol. 293, Issue 4 https://doi.org/10.1006/jmbi.1999.3190	journal	November 1999
Crystal structures of the SH2 domain of grb2: highlight on the binding of a new high-affinity inhibitor Nioche, Pierre; Liu, Wang-Qing; Broutin, Isabelle Journal of Molecular Biology, Vol. 315, Issue 5 https://doi.org/10.1006/jmbi.2001.5299	journal	February 2002
Protein Structure Modeling with MODELLER Webb, Benjamin; Sali, Andrej Methods in Molecular Biology https://doi.org/10.1007/978-1-4939-0366-5_1	book	January 2014
MAFFT: Iterative Refinement and Additional Methods Katoh, Kazutaka; Standley, Daron M. Methods in Molecular Biology https://doi.org/10.1007/978-1-62703-646-7_8	book	January 2013
Computational studies of polyurethanases from Pseudomonas do Canto, Vanessa Petry; Thompson, Claudia Elizabeth; Netz, Paulo Augusto Journal of Molecular Modeling, Vol. 27, Issue 2 https://doi.org/10.1007/s00894-021-04671-x	journal	January 2021
Specificity in Signal Transduction Pawson, Tony Cell, Vol. 116, Issue 2 https://doi.org/10.1016/S0092-8674(03)01077-8	journal	January 2004
Insulin receptor-like proteins in Tetrahymena thermophila ciliary membranes Christensen, Søren T.; Guerra, Charles F.; Awan, Aashir Current Biology, Vol. 13, Issue 2 https://doi.org/10.1016/S0960-9822(02)01425-2	journal	January 2003
Kinome signaling through regulated protein–protein interactions in normal and cancer cells Pawson, Tony; Kofler, Michael Current Opinion in Cell Biology, Vol. 21, Issue 2 https://doi.org/10.1016/j.ceb.2009.02.005	journal	April 2009
The Salmonella Effector SptP Dephosphorylates Host AAA+ ATPase VCP to Promote Development of its Intracellular Replicative Niche Humphreys, Daniel; Hume, Peter J.; Koronakis, Vassilis Cell Host & Microbe, Vol. 5, Issue 3 https://doi.org/10.1016/j.chom.2009.01.010	journal	March 2009
Host Cell Interactome of Tyrosine-Phosphorylated Bacterial Proteins Selbach, Matthias; Paul, Florian Ernst; Brandt, Sabine Cell Host & Microbe, Vol. 5, Issue 4 https://doi.org/10.1016/j.chom.2009.03.004	journal	April 2009
Perspective: Dynamics of receptor tyrosine kinase signaling complexes Mayer, Bruce J. FEBS Letters, Vol. 586, Issue 17 https://doi.org/10.1016/j.febslet.2012.05.002	journal	May 2012
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Legionella pneumophila Dot/Icm translocated substrates: a sum of parts Ensminger, Alexander W.; Isberg, Ralph R. Current Opinion in Microbiology, Vol. 12, Issue 1 https://doi.org/10.1016/j.mib.2008.12.004	journal	February 2009
Legionella pneumophila, armed to the hilt: justifying the largest arsenal of effectors in the bacterial world Ensminger, Alexander W. Current Opinion in Microbiology, Vol. 29 https://doi.org/10.1016/j.mib.2015.11.002	journal	February 2016
Molecular Characterization of LubX: Functional Divergence of the U-Box Fold by Legionella pneumophila Quaile, Andrew T.; Urbanus, Malene L.; Stogios, Peter J. Structure, Vol. 23, Issue 8 https://doi.org/10.1016/j.str.2015.05.020	journal	August 2015
The Phenix software for automated determination of macromolecular structures Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Methods, Vol. 55, Issue 1 https://doi.org/10.1016/j.ymeth.2011.07.005	journal	September 2011
Disease-Causing SAP Mutants Are Defective in Ligand Binding and Protein Folding ^† Li, Chengjun; Iosef, Cristiana; Jia, Christina Y. H. Biochemistry, Vol. 42, Issue 50 https://doi.org/10.1021/bi034798l	journal	December 2003
Recognition of a high-affinity phosphotyrosyl peptide by the Src homology-2 domain of p56lck Eck, Michael J.; Shoelson, Steven E.; Harrison, Stephen C. Nature, Vol. 362, Issue 6415 https://doi.org/10.1038/362087a0	journal	March 1993
SET‐domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription Li, Ting; Lu, Qiuhe; Wang, Guolun EMBO reports, Vol. 14, Issue 8 https://doi.org/10.1038/embor.2013.86	journal	June 2013
Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells Gruenheid, Samantha; DeVinney, Rebekah; Bladt, Friedhelm Nature Cell Biology, Vol. 3, Issue 9 https://doi.org/10.1038/ncb0901-856	journal	August 2001
Genomic analysis of 38 Legionella species identifies large and diverse effector repertoires Burstein, David; Amaro, Francisco; Zusman, Tal Nature Genetics, Vol. 48, Issue 2 https://doi.org/10.1038/ng.3481	journal	January 2016
Defining an allosteric circuit in the cysteine protease domain of Clostridium difficile toxins Shen, Aimee; Lupardus, Patrick J.; Gersch, Malte M. Nature Structural & Molecular Biology, Vol. 18, Issue 3 https://doi.org/10.1038/nsmb.1990	journal	February 2011
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
Visualization of the mechanosensitive ion channel MscS under membrane tension Zhang, Yixiao; Daday, Csaba; Gu, Ruo-Xu Nature, Vol. 590, Issue 7846 https://doi.org/10.1038/s41586-021-03196-w	journal	February 2021
The oligomeric structures of plant cryptochromes Shao, Kai; Zhang, Xue; Li, Xu Nature Structural & Molecular Biology, Vol. 27, Issue 5 https://doi.org/10.1038/s41594-020-0420-x	journal	May 2020
Why does the Aβ peptide of Alzheimer share structural similarity with antimicrobial peptides? Pastore, Annalisa; Raimondi, Francesco; Rajendran, Lawrence Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-0865-9	journal	March 2020
Marine amoebae with cytoplasmic and perinuclear symbionts deeply branching in the Gammaproteobacteria Schulz, Frederik; Tyml, Tomáš; Pizzetti, Ilaria Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep13381	journal	August 2015
Probable Person-to-Person Transmission of Legionnaires’ Disease Correia, Ana M.; Ferreira, Joana S.; Borges, Vítor New England Journal of Medicine, Vol. 374, Issue 5 https://doi.org/10.1056/NEJMc1505356	journal	February 2016
Estimating the timing of early eukaryotic diversification with multigene molecular clocks Parfrey, L. W.; Lahr, D. J. G.; Knoll, A. H. Proceedings of the National Academy of Sciences, Vol. 108, Issue 33 https://doi.org/10.1073/pnas.1110633108	journal	August 2011
Electrostatics of nanosystems: Application to microtubules and the ribosome Baker, N. A.; Sept, D.; Joseph, S. Proceedings of the National Academy of Sciences, Vol. 98, Issue 18, p. 10037-10041 https://doi.org/10.1073/pnas.181342398	journal	August 2001
Defining the Specificity Space of the Human Src Homology 2 Domain Huang, Haiming; Li, Lei; Wu, Chenggang Molecular & Cellular Proteomics, Vol. 7, Issue 4 https://doi.org/10.1074/mcp.M700312-MCP200	journal	October 2007
Two Dictyostelium tyrosine kinase–like kinases function in parallel, stress-induced STAT activation pathways Araki, Tsuyoshi; Vu, Linh Hai; Sasaki, Norimitsu Molecular Biology of the Cell, Vol. 25, Issue 20 https://doi.org/10.1091/mbc.e14-07-1182	journal	October 2014
STRAP: editor for STRuctural Alignments of Proteins Gille, C.; Frommel, C. Bioinformatics, Vol. 17, Issue 4 https://doi.org/10.1093/bioinformatics/17.4.377	journal	April 2001
Two Sample Logo: a graphical representation of the differences between two sets of sequence alignments Vacic, V.; Iakoucheva, L. M.; Radivojac, P. Bioinformatics, Vol. 22, Issue 12 https://doi.org/10.1093/bioinformatics/btl151	journal	April 2006
Jalview Version 2--a multiple sequence alignment editor and analysis workbench Waterhouse, A. M.; Procter, J. B.; Martin, D. M. A. Bioinformatics, Vol. 25, Issue 9 https://doi.org/10.1093/bioinformatics/btp033	journal	January 2009
Earliest Holozoan Expansion of Phosphotyrosine Signaling Suga, Hiroshi; Torruella, Guifré; Burger, Gertraud Molecular Biology and Evolution, Vol. 31, Issue 3 https://doi.org/10.1093/molbev/mst241	journal	December 2013
ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement Suhre, K.; Sanejouand, Y. -H. Nucleic Acids Research, Vol. 32, Issue Web Server https://doi.org/10.1093/nar/gkh368	journal	July 2004
Prediction of phosphotyrosine signaling networks using a scoring matrix-assisted ligand identification approach Li, Lei; Wu, Chenggang; Huang, Haiming Nucleic Acids Research, Vol. 36, Issue 10 https://doi.org/10.1093/nar/gkn161	journal	April 2008
Scalable web services for the PSIPRED Protein Analysis Workbench Buchan, Daniel W. A.; Minneci, Federico; Nugent, Tim C. O. Nucleic Acids Research, Vol. 41, Issue W1 https://doi.org/10.1093/nar/gkt381	journal	June 2013
The Pfam protein families database: towards a more sustainable future Finn, Robert D.; Coggill, Penelope; Eberhardt, Ruth Y. Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1344	journal	December 2015
Dali server update Holm, Liisa; Laakso, Laura M. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw357	journal	April 2016
20 years of the SMART protein domain annotation resource Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 46, Issue D1 https://doi.org/10.1093/nar/gkx922	journal	October 2017
Evolution of SH2 domains and phosphotyrosine signalling networks Liu, Bernard A.; Nash, Piers D. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1602 https://doi.org/10.1098/rstb.2012.0107	journal	September 2012
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
On the combination of molecular replacement and single-wavelength anomalous diffraction phasing for automated structure determination Panjikar, Santosh; Parthasarathy, Venkataraman; Lamzin, Victor S. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/S0907444909029643	journal	September 2009
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
iMOSFLM : a new graphical interface for diffraction-image processing with MOSFLM Battye, T. Geoff G.; Kontogiannis, Luke; Johnson, Owen Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910048675	journal	March 2011
Two substrate-targeting sites in the Yersinia protein tyrosine phosphatase co-operate to promote bacterial virulence: Mechanism of substrate targeting by Yersinia YopH Ivanov, Maya I.; Stuckey, Jeanne A.; Schubert, Heidi L. Molecular Microbiology, Vol. 55, Issue 5 https://doi.org/10.1111/j.1365-2958.2005.04477.x	journal	January 2005
Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways Heidtman, Matthew; Chen, Emy J.; Moy, Man-Yu Cellular Microbiology, Vol. 11, Issue 2 https://doi.org/10.1111/j.1462-5822.2008.01249.x	journal	February 2009
The E Block motif is associated with Legionella pneumophila translocated substrates: Legionella C-terminal Signal Huang, Li; Boyd, Dana; Amyot, Whitney M. Cellular Microbiology, Vol. 13, Issue 2 https://doi.org/10.1111/j.1462-5822.2010.01531.x	journal	November 2010
Small Molecule-Induced Allosteric Activation of the Vibrio cholerae RTX Cysteine Protease Domain Lupardus, P. J.; Shen, A.; Bogyo, M. Science, Vol. 322, Issue 5899 https://doi.org/10.1126/science.1162403	journal	October 2008
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
A Bacterial Tyrosine Phosphatase Inhibits Plant Pattern Recognition Receptor Activation Macho, A. P.; Schwessinger, B.; Ntoukakis, V. Science, Vol. 343, Issue 6178 https://doi.org/10.1126/science.1248849	journal	March 2014
Loops Govern SH2 Domain Specificity by Controlling Access to Binding Pockets Kaneko, T.; Huang, H.; Zhao, B. Science Signaling, Vol. 3, Issue 120 https://doi.org/10.1126/scisignal.2000796	journal	May 2010
Superbinder SH2 Domains Act as Antagonists of Cell Signaling Kaneko, T.; Huang, H.; Cao, X. Science Signaling, Vol. 5, Issue 243 https://doi.org/10.1126/scisignal.2003021	journal	September 2012
Heterogeneity in the Attachment and Uptake Mechanisms of the Legionnaires’ Disease Bacterium, Legionella pneumophila, by Protozoan Hosts Harb, Omar S.; Venkataraman, Chandrasekar; Haack, Bradley J. Applied and Environmental Microbiology, Vol. 64, Issue 1 https://doi.org/10.1128/AEM.64.1.126-132.1998	journal	January 1998
E3 Ubiquitin Ligase Activity and Targeting of BAT3 by Multiple Legionella pneumophila Translocated Substrates Ensminger, A. W.; Isberg, R. R. Infection and Immunity, Vol. 78, Issue 9 https://doi.org/10.1128/IAI.00344-10	journal	June 2010
Signal Transduction during Legionella pneumophila Entry into Human Monocytes Coxon, Patricia Y.; Summersgill, James T.; Ramirez, Julio A. Infection and Immunity, Vol. 66, Issue 6 https://doi.org/10.1128/IAI.66.6.2905-2913.1998	journal	June 1998
Legionella pneumophila Invasion of MRC-5 Cells Induces Tyrosine Protein Phosphorylation Susa, Milorad; Marre, Reinhard Infection and Immunity, Vol. 67, Issue 9 https://doi.org/10.1128/IAI.67.9.4490-4498.1999	journal	September 1999
DNA sequence of the viral and cellular src gene of chickens. II. Comparison of the src genes of two strains of avian sarcoma virus and of the cellular homolog. Takeya, T.; Hanafusa, H. Journal of Virology, Vol. 44, Issue 1 https://doi.org/10.1128/JVI.44.1.12-18.1982	journal	January 1982
Cell Regulation by Phosphotyrosine-Targeted Ubiquitin Ligases Cooper, Jonathan A.; Kaneko, Tomonori; Li, Shawn S. C. Molecular and Cellular Biology, Vol. 35, Issue 11 https://doi.org/10.1128/MCB.00098-15	journal	March 2015
A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps. Sadowski, I.; Stone, J. C.; Pawson, T. Molecular and Cellular Biology, Vol. 6, Issue 12 https://doi.org/10.1128/MCB.6.12.4396	journal	December 1986
DNA sequence of the viral and cellular src gene of chickens. II. Comparison of the src genes of two strains of avian sarcoma virus and of the cellular homolog. Takeya, T.; Hanafusa, H. Journal of Virology, Vol. 44, Issue 1 https://doi.org/10.1128/jvi.44.1.12-18.1982	journal	January 1982
A noncatalytic domain conserved among cytoplasmic protein-tyrosine kinases modifies the kinase function and transforming activity of Fujinami sarcoma virus P130gag-fps Sadowski, I.; Stone, J. C.; Pawson, T. Molecular and Cellular Biology, Vol. 6, Issue 12 https://doi.org/10.1128/mcb.6.12.4396-4408.1986	journal	December 1986
Modulation of Host Cell Function by Legionella pneumophila Type IV Effectors Hubber, Andree; Roy, Craig R. Annual Review of Cell and Developmental Biology, Vol. 26, Issue 1 https://doi.org/10.1146/annurev-cellbio-100109-104034	journal	November 2010
Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling Clarke, Michael; Lohan, Amanda J.; Liu, Bernard Genome Biology, Vol. 14, Issue 2 https://doi.org/10.1186/gb-2013-14-2-r11	journal	January 2013
Short linear motifs – ex nihilo evolution of protein regulation Davey, Norman E.; Cyert, Martha S.; Moses, Alan M. Cell Communication and Signaling, Vol. 13, Issue 1 https://doi.org/10.1186/s12964-015-0120-z	journal	November 2015
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Analysis of the Legionella longbeachae Genome and Transcriptome Uncovers Unique Strategies to Cause Legionnaires' Disease Cazalet, Christel; Gomez-Valero, Laura; Rusniok, Christophe PLoS Genetics, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pgen.1000851	journal	February 2010
Non-Opsonic Phagocytosis of Legionella pneumophila by Macrophages Is Mediated by Phosphatidylinositol 3-Kinase Tachado, Souvenir D.; Samrakandi, Mustapha M.; Cirillo, Jeffrey D. PLoS ONE, Vol. 3, Issue 10 https://doi.org/10.1371/journal.pone.0003324	journal	October 2008
Comprehensive Binary Interaction Mapping of SH2 Domains via Fluorescence Polarization Reveals Novel Functional Diversification of ErbB Receptors Hause, Ronald J.; Leung, Kin K.; Barkinge, John L. PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044471	journal	September 2012
RNA Interference Analysis of Legionella in Drosophila Cells: Exploitation of Early Secretory Apparatus Dynamics Dorer, Marion S.; Kirton, Donald; Bader, Joel S. PLoS Pathogens, Vol. 2, Issue 4 https://doi.org/10.1371/journal.ppat.0020034	journal	January 2006
The Legionella pneumophila IcmSW Complex Interacts with Multiple Dot/Icm Effectors to Facilitate Type IV Translocation Cambronne, Eric D.; Roy, Craig R. PLoS Pathogens, Vol. 3, Issue 12 https://doi.org/10.1371/journal.ppat.0030188	journal	January 2007
Chemical Genetics Reveals Bacterial and Host Cell Functions Critical for Type IV Effector Translocation by Legionella pneumophila Charpentier, Xavier; Gabay, Joëlle E.; Reyes, Moraima PLoS Pathogens, Vol. 5, Issue 7 https://doi.org/10.1371/journal.ppat.1000501	journal	July 2009
Legionella Metaeffector Exploits Host Proteasome to Temporally Regulate Cognate Effector Kubori, Tomoko; Shinzawa, Naoaki; Kanuka, Hirotaka PLoS Pathogens, Vol. 6, Issue 12 https://doi.org/10.1371/journal.ppat.1001216	journal	December 2010
Experimental Evolution of Legionella pneumophila in Mouse Macrophages Leads to Strains with Altered Determinants of Environmental Survival Ensminger, Alexander W.; Yassin, Yosuf; Miron, Alexander PLoS Pathogens, Vol. 8, Issue 5 https://doi.org/10.1371/journal.ppat.1002731	journal	May 2012
From Many Hosts, One Accidental Pathogen: The Diverse Protozoan Hosts of Legionella Boamah, David K.; Zhou, Guangqi; Ensminger, Alexander W. Frontiers in Cellular and Infection Microbiology, Vol. 7 https://doi.org/10.3389/fcimb.2017.00477	journal	November 2017
Interactions of Bacterial Proteins with Host Eukaryotic Ubiquitin Pathways Perrett, Charlotte Averil; Lin, David Yin-Wei; Zhou, Daoguo Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00143	journal	January 2011
Comparative and Functional Genomics of Legionella Identified Eukaryotic Like Proteins as Key Players in Host?Pathogen Interactions Gomez-Valero, Laura; Rusniok, Christophe; Cazalet, Christel Frontiers in Microbiology, Vol. 2 https://doi.org/10.3389/fmicb.2011.00208	journal	January 2011

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SH2 Domain Binding: Diverse FLVRs of Partnership Jaber Chehayeb, Rachel; Boggon, Titus J. Frontiers in Endocrinology, Vol. 11 https://doi.org/10.3389/fendo.2020.575220	journal	September 2020
Intracellular parasitism, the driving force of evolution of Legionella pneumophila and the genus Legionella Gomez-Valero, Laure; Buchrieser, Carmen Microbes and Infection, Vol. 21, Issue 5-6 https://doi.org/10.1016/j.micinf.2019.06.012	journal	June 2019
Intracellular parasitism, the driving force of evolution of Legionella pneumophila and the genus Legionella Gomez-Valero, Laura; Buchrieser, Carmen Genes & Immunity, Vol. 20, Issue 5 https://doi.org/10.1038/s41435-019-0074-z	journal	May 2019
Tyrosine Phosphorylation as a Widespread Regulatory Mechanism in Prokaryotes Getz, Landon J.; Runte, Cameron S.; Rainey, Jan K. Journal of Bacteriology, Vol. 201, Issue 19 https://doi.org/10.1128/jb.00205-19	journal	July 2019

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