Molecular interaction between human SUMO-I and histone like DNA binding protein of Helicobacter pylori (Hup) investigated by NMR and other biophysical tools

Nooren, 2003, Diversity of protein-protein interactions, EMBO J., 22, 3486, 10.1093/emboj/cdg359 Vaynberg, 2006, Weak protein-protein interactions as probed by NMR spectroscopy, Trends Biotechnol., 24, 22, 10.1016/j.tibtech.2005.09.006 Flotho, 2013, Sumoylation: a regulatory protein modification in health and disease, Annu. Rev. Biochem., 82, 357, 10.1146/annurev-biochem-061909-093311 Song, 2004, Identification of a SUMO-binding motif that recognizes SUMO-modified proteins, Proc. Natl. Acad. Sci. U. S. A., 101, 14373, 10.1073/pnas.0403498101 Johnson, 2004, Protein modification by SUMO, Annu. Rev. Biochem., 73, 355, 10.1146/annurev.biochem.73.011303.074118 Hannoun, 2010, Post-translational modification by SUMO, Toxicology, 278, 288, 10.1016/j.tox.2010.07.013 Burkle, 2001, 1533 Sarkar, 2018, Elucidating protein-protein interactions through computational approaches and designing small molecule inhibitors against them for various diseases, Curr. Top. Med. Chem., 10.2174/1568026618666181025114903 Paddibhatla, 2010, Role for sumoylation in systemic inflammation and immune homeostasis in Drosophila larvae, PLoS Pathog., 6, 10.1371/journal.ppat.1001234 Adorisio, 2017, SUMO proteins: guardians of immune system, J. Autoimmun., 10.1016/j.jaut.2017.09.001 Geiss-Friedlander, 2007, Concepts in sumoylation: a decade on, Nat. Rev. Mol. Cell Biol., 8, 10.1038/nrm2293 Verger, 2003, Modification with SUMO: a role in transcriptional regulation, EMBO Rep., 4, 137, 10.1038/sj.embor.embor738 Kerscher, 2006, Modification of proteins by ubiquitin and ubiquitin-like proteins, Annu. Rev. Cell Dev. Biol., 22, 159, 10.1146/annurev.cellbio.22.010605.093503 Kusters, 2006, Pathogenesis of helicobacter pylori infection, Clin. Microbiol. Rev., 19, 449, 10.1128/CMR.00054-05 Kao, 2016, Helicobacter pylori infection: an overview of bacterial virulence factors and pathogenesis, Biom. J., 39, 14 Dunn, 1997, Helicobacter pylori, Clin. Microbiol. Rev., 10, 720, 10.1128/CMR.10.4.720 Kusters, 2006, Pathogenesis of Helicobacter pylori infection, Clin. Microbiol. Rev., 19, 449, 10.1128/CMR.00054-05 Suerbaum, 2002, Helicobacter pylori infection, N. Engl. J. Med., 347, 1175, 10.1056/NEJMra020542 Uemura, 2001, Helicobacter pylori infection and the development of gastric cancer, N. Engl. J. Med., 345, 784, 10.1056/NEJMoa001999 Ferlay, 2010, Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008, Int. J. Cancer, 127, 2893, 10.1002/ijc.25516 Blaser, 1992, Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation, Gastroenterology, 102, 720, 10.1016/0016-5085(92)90126-J Blaser, 1994, Parasitism by the, J. Clin. Invest., 94, 4, 10.1172/JCI117336 Crabtree, 1991, Mucosal IgA recognition of Helicobacter pylori 120 kDa protein, peptic ulceration, and gastric pathology, Lancet, 338, 332, 10.1016/0140-6736(91)90477-7 Lee, 1993, Pathogenicity of Helicobacter pylori: a perspective, Infect. Immun., 61, 1601, 10.1128/iai.61.5.1601-1610.1993 Rodriguez, 2001, SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting, J. Biol. Chem., 276, 12654, 10.1074/jbc.M009476200 Covacci, 1999, Helicobacter pylori virulence and genetic geography, Science, 284, 1328, 10.1126/science.284.5418.1328 Kim, 2002, Proteins released by Helicobacter pylori in vitro, J. Bacteriol., 184, 6155, 10.1128/JB.184.22.6155-6162.2002 Oberto, 2009, The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction, PLoS One, 4, 10.1371/journal.pone.0004367 Bhowmick, 2014, Targeting Mycobacterium tuberculosis nucleoid-associated protein HU with structure-based inhibitors, Nat. Commun., 5, 4124, 10.1038/ncomms5124 Wang, 2012, A histone-like protein of Helicobacter pylori protects DNA from stress damage and aids host colonization, DNA Repair, 11, 733, 10.1016/j.dnarep.2012.06.006 Wang, 2015, A novel DNA-binding protein plays an important role in Helicobacter pylori stress tolerance and survival in the host, J. Bacteriol., 197, 973, 10.1128/JB.02489-14 Amundsen, 2008, Helicobacter pylori AddAB helicase-nuclease and RecA promote recombination-related DNA repair and survival during stomach colonization, Mol. Microbiol., 69, 994, 10.1111/j.1365-2958.2008.06336.x Fischer, 2014, A comprehensive analysis of Helicobacter pylori plasticity zones reveals that they are integrating conjugative elements with intermediate integration specificity, BMC Genomics, 15, 310, 10.1186/1471-2164-15-310 Yamaoka, 2010, Mechanisms of disease: Helicobacter pylori virulence factors, Nat. Rev. Gastroenterol. Hepatol., 7, 629, 10.1038/nrgastro.2010.154 Gill, 2004, SUMO and ubiquitin in the nucleus: different functions, similar mechanisms?, Genes Dev., 18, 2046, 10.1101/gad.1214604 Hannoun, 2016, The implication of SUMO in intrinsic and innate immunity, Cytokine Growth Factor Rev., 29, 3, 10.1016/j.cytogfr.2016.04.003 Hecker, 2006, Specification of SUMO1-and SUMO2-interacting motifs, J. Biol. Chem., 281, 16117, 10.1074/jbc.M512757200 Hannich, 2005, Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae, J. Biol. Chem., 280, 4102, 10.1074/jbc.M413209200 Dohmen, 2004, SUMO protein modification, Biochim. Biophys. Acta (BBA) - Mol. Cell Res., 1695, 113, 10.1016/j.bbamcr.2004.09.021 Jaiswal, 2018, NMR elucidation of monomer–dimer transition and conformational heterogeneity in histone-like DNA binding protein of Helicobacter pylori, Magn. Reson. Chem., 56, 285, 10.1002/mrc.4701 Jin, 2001, Heteronuclear nuclear magnetic resonance assignments, structure and dynamics of SUMO-1, a human ubiquitin-like protein, Int. J. Biol. Macromol., 28, 227, 10.1016/S0141-8130(00)00169-0 Schanda, 2005, SOFAST-HMQC experiments for recording two-dimensional deteronuclear correlation spectra of proteins within a few seconds, J. Biomol. NMR, 33, 199, 10.1007/s10858-005-4425-x Peng, 1992, Mapping of the spectral densities of nitrogen-hydrogen bond motions in Eglin c using heteronuclear relaxation experiments, Biochemistry, 31, 8571, 10.1021/bi00151a027 Peng, 1995, Frequency spectrum of NH bonds in eglin c from spectral density mapping at multiple fields, Biochemistry, 34, 16733, 10.1021/bi00051a023 Farrow, 1994, Backbone dynamics of a free and a phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation, Biochemistry, 33, 5984, 10.1021/bi00185a040 Spyracopoulos, 2006, A suite of Mathematica notebooks for the analysis of protein main chain 15 N NMR relaxation data, J. Biomol. NMR, 36, 215, 10.1007/s10858-006-9083-0 Schwede, 2003, SWISS-MODEL: an automated protein homology-modeling server, Nucleic Acids Res., 31, 3381, 10.1093/nar/gkg520 Chen, 2006, (PS)2: protein structure prediction server, Nucleic Acids Res., 34, W152, 10.1093/nar/gkl187 Chen, 2009, (PS)2-v2: template-based protein structure prediction server, BMC Bioinf., 10, 1, 10.1186/1471-2105-10-366 Pierce, 2014, ZDOCK server: interactive docking prediction of protein–protein complexes and symmetric multimers, Bioinformatics, 30, 1771, 10.1093/bioinformatics/btu097 Keskin, 2016, Predicting protein-protein interactions from the molecular to the proteome level, Chem. Rev., 116, 4884, 10.1021/acs.chemrev.5b00683 Zhao, 2014, GPS-SUMO: a tool for the prediction of sumoylation sites and SUMO-interaction motifs, Nucleic Acids Res., 42, W325, 10.1093/nar/gku383 Minty, 2000, Covalent modification of p73α by SUMO-1 two-hybrid screening with p73 identifies novel SUMO-1-interacting proteins and a SUMO-1 interaction motif, J. Biol. Chem., 275, 36316, 10.1074/jbc.M004293200 Song, 2005, Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif a reversal of the bound orientation, J. Biol. Chem., 280, 40122, 10.1074/jbc.M507059200 Grove, 2011, Functional evolution of bacterial histone-like HU proteins, Curr. Issues Mol. Biol., 13, 1 Nathan, 2006, Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications, Genes Dev., 20, 966, 10.1101/gad.1404206 Nathan, 2003, Histone modifications: now summoning sumoylation, Proc. Natl. Acad. Sci., 100, 13118, 10.1073/pnas.2436173100 Wyss, 1997, The counterreceptor binding site of human CD2 exhibits an extended surface patch with multiple conformations fluctuating with millisecond to microsecond motions, Protein Sci., 6, 534, 10.1002/pro.5560060303 Pellecchia, 2000, Structural insights into substrate binding by the molecular chaperone DnaK, Nat. Struct. Mol. Biol., 7, 298, 10.1038/74062 Kleckner, 2011, An introduction to NMR-based approaches for measuring protein dynamics, Biochim. Biophys. Acta Proteom., 1814, 942, 10.1016/j.bbapap.2010.10.012 Palmer, 2004, NMR characterization of the dynamics of biomacromolecules, Chem. Rev., 104, 3623, 10.1021/cr030413t Cavanagh, 1995 Kay, 1989, Backbone dynamics of proteins as studied by nitrogen-15 inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease, Biochemistry, 28, 8972, 10.1021/bi00449a003 Palmer, 2001, Nuclear magnetic resonance methods for quantifying microsecond-to-millisecond motions in biological macromolecules, Methods Enzymol., 339, 204, 10.1016/S0076-6879(01)39315-1 Wallis, 1995, Protein-protein interactions in colicin E9 DNase-immunity protein complexes. 1. Diffusion-controlled association and femtomolar binding for the cognate complex, Biochemistry, 34, 13743, 10.1021/bi00042a004 Iakoucheva, 2002, Intrinsic disorder in cell-signaling and cancer-associated proteins, J. Mol. Biol., 323, 573, 10.1016/S0022-2836(02)00969-5 Krause, 2006, Detection and analysis of protein–protein interactions in organellar and prokaryotic proteomes by native gel electrophoresis: (membrane) protein complexes and supercomplexes, Electrophoresis, 27, 2759, 10.1002/elps.200600049 Darie, 2013, Investigation of protein-protein interactions by blue native-PAGE & mass spectrometry, Mod. Chem. Appl., 1, 111 Ramarao, 2000, Helicobacter pylori induces but survives the extracellular release of oxygen radicals from professional phagocytes using its catalase activity, Mol. Microbiol., 38, 103, 10.1046/j.1365-2958.2000.02114.x O'Rourke, 2003, Pathogen DNA as target for host-generated oxidative stress: role for repair of bacterial DNA damage in Helicobacter pylori colonization, Proc. Natl. Acad. Sci., 100, 2789, 10.1073/pnas.0337641100 Baik, 1996, Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa, Cancer Res., 56, 1279 Bagchi, 1996, Production of reactive oxygen species by gastric cells in association with Helicobacter pylori, Free Radic. Res., 24, 439, 10.3109/10715769609088043 Flint, 2016, Oxidative and nitrosative stress defences of Helicobacter and Campylobacter species that counteract mammalian immunity, FEMS Microbiol. Rev., 40, 938, 10.1093/femsre/fuw025