Structure and activity of PPX/GppA homologs from Escherichia coli and Helicobacter pylori

Song, He; Dharmasena, Madushini N.; Wang, Chao; Shaw, Gary X.; Cherry, Scott; Tropea, Joseph E.; Jin, Ding J.; Ji, Xinhua

doi:10.1111/febs.15120

Title: Structure and activity of PPX/GppA homologs from Escherichia coli and Helicobacter pylori

Journal Article · Sat Nov 23 00:00:00 EST 2019 · Federation of European Biochemical Societies (FEBS) Journal

DOI:https://doi.org/10.1111/febs.15120· OSTI ID:1575312

Song, He ^[1]; Dharmasena, Madushini N. ^[2]; Wang, Chao ^[1]; Shaw, Gary X. ^[1]; Cherry, Scott ^[1]; Tropea, Joseph E. ^[1]; Jin, Ding J. ^[2];

^[1]

Macromolecular Crystallography Laboratory National Cancer Institute Frederick MD USA
RNA Biology Laboratory National Cancer Institute Frederick MD USA

Rapid adaptation to environmental changes is crucial for bacterial survival. Almost all bacteria possess a conserved stringent response system to prompt transcriptional and metabolic responses toward stress. The adaptive process relies on alarmones, guanosine pentaphosphate (pppGpp), and tetraphosphate (ppGpp), to regulate global gene expression. The ppGpp is more potent than pppGpp in the regulatory activity, and pppGpp phosphohydrolase (GppA) plays a key role in (p)ppGpp homeostasis. Sharing a similar domain structure, GppA is indistinguishable from exopolyphosphatase (PPX), which mediates the metabolism of cellular inorganic polyphosphate. Here, our phylogenetic analysis of PPX/GppA homologs in bacteria shows a wide distribution with several distinct subfamilies, and our structural and functional analysis of Escherichia coli GppA and Helicobacter pylori PPX/GppA reveals unique properties of each homolog. These results explain how each homolog possesses its distinct functionality.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐AC02‐06CH11357

OSTI ID:: 1575312

Journal Information:: Federation of European Biochemical Societies (FEBS) Journal, Journal Name: Federation of European Biochemical Societies (FEBS) Journal Vol. 287 Journal Issue: 9; ISSN 1742-464X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

Citation Metrics:

Cited by: 13 works

Citation information provided by
Web of Science

References (48)

Recent functional insights into the role of (p)ppGpp in bacterial physiology Hauryliuk, Vasili; Atkinson, Gemma C.; Murakami, Katsuhiko S. Nature Reviews Microbiology, Vol. 13, Issue 5 https://doi.org/10.1038/nrmicro3448	journal	April 2015
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
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences Huerta-Cepas, Jaime; Szklarczyk, Damian; Forslund, Kristoffer Nucleic Acids Research, Vol. 44, Issue D1 https://doi.org/10.1093/nar/gkv1248	journal	November 2015
Hit the right spots: cell cycle control by phosphorylated guanosines in alphaproteobacteria Hallez, Régis; Delaby, Marie; Sanselicio, Stefano Nature Reviews Microbiology, Vol. 15, Issue 3 https://doi.org/10.1038/nrmicro.2016.183	journal	January 2017
Novel Assay Reveals Multiple Pathways Regulating Stress-Induced Accumulations of Inorganic Polyphosphate in Escherichia coli Ault-Riché, Dana; Fraley, Cresson D.; Tzeng, Chi-Meng Journal of Bacteriology, Vol. 180, Issue 7 https://doi.org/10.1128/JB.180.7.1841-1847.1998	journal	April 1998
A Magic Spot in Genome Maintenance Rasouly, Aviram; Pani, Bibhusita; Nudler, Evgeny Trends in Genetics, Vol. 33, Issue 1 https://doi.org/10.1016/j.tig.2016.11.002	journal	January 2017
Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard Terwilliger, Thomas C.; Grosse-Kunstleve, Ralf W.; Afonine, Pavel V. Acta Crystallographica Section D Biological Crystallography, Vol. 64, Issue 1 https://doi.org/10.1107/S090744490705024X	journal	December 2007
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
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
ppGpp couples transcription to DNA repair in E. coli Kamarthapu, V.; Epshtein, V.; Benjamin, B. Science, Vol. 352, Issue 6288 https://doi.org/10.1126/science.aad6945	journal	May 2016
Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Keasling, J. D.; Bertsch, L.; Kornberg, A. Proceedings of the National Academy of Sciences, Vol. 90, Issue 15 https://doi.org/10.1073/pnas.90.15.7029	journal	August 1993
Functional characterization of exopolyphosphatase/guanosine pentaphosphate phosphohydrolase (PPX/GPPA) of Campylobacter jejuni Malde, Anandkumar; Gangaiah, Dharanesh; Chandrashekhar, Kshipra Virulence, Vol. 5, Issue 4 https://doi.org/10.4161/viru.28311	journal	February 2014
A polyphosphate kinase (PPK2) widely conserved in bacteria Zhang, H.; Ishige, K.; Kornberg, A. Proceedings of the National Academy of Sciences, Vol. 99, Issue 26 https://doi.org/10.1073/pnas.262655199	journal	December 2002
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
Bacterial nucleotide-based second messengers Pesavento, Christina; Hengge, Regine Current Opinion in Microbiology, Vol. 12, Issue 2 https://doi.org/10.1016/j.mib.2009.01.007	journal	April 2009
Two exopolyphosphatases with distinct molecular architectures and substrate specificities from the thermophilic green-sulfur bacterium Chlorobium tepidum TLS Albi, T.; Serrano, A. Microbiology, Vol. 160, Issue Pt_9 https://doi.org/10.1099/mic.0.080952-0	journal	June 2014
Inorganic Polyphosphate: A Molecule of Many Functions Kornberg, Arthur; Rao, Narayana N.; Ault-Riché, Dana Annual Review of Biochemistry, Vol. 68, Issue 1 https://doi.org/10.1146/annurev.biochem.68.1.89	journal	June 1999
Decision-making in structure solution using Bayesian estimates of map quality: the PHENIX AutoSol wizard Terwilliger, Thomas C.; Adams, Paul D.; Read, Randy J. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 6 https://doi.org/10.1107/S0907444909012098	journal	May 2009
The magic dance of the alarmones (p)ppGpp: The structural biology of the alarmones (p)ppGpp Steinchen, Wieland; Bange, Gert Molecular Microbiology, Vol. 101, Issue 4 https://doi.org/10.1111/mmi.13412	journal	June 2016
Inorganic Polyphosphate: Essential for Growth and Survival Rao, Narayana N.; Gómez-García, María R.; Kornberg, Arthur Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.77.083007.093039	journal	June 2009
Guanosine Tetra- and Pentaphosphate Promote Accumulation of Inorganic Polyphosphate in Escherichia coli Kuroda, Akio; Murphy, Helen; Cashel, Michael Journal of Biological Chemistry, Vol. 272, Issue 34 https://doi.org/10.1074/jbc.272.34.21240	journal	August 1997
Structural Characterization of the Stringent Response Related Exopolyphosphatase/Guanosine Pentaphosphate Phosphohydrolase Protein Family ^† ^, ^‡ Kristensen, Ole; Laurberg, Martin; Liljas, Anders Biochemistry, Vol. 43, Issue 28 https://doi.org/10.1021/bi049083c	journal	July 2004
ExPASy: the proteomics server for in-depth protein knowledge and analysis Gasteiger, E. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg563	journal	July 2003
The complete genome of the hyperthermophilic bacterium Aquifex aeolicus Deckert, Gerard; Warren, Patrick V.; Gaasterland, Terry Nature, Vol. 392, Issue 6674 https://doi.org/10.1038/32831	journal	March 1998
Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw290	journal	April 2016
The mechanism of RNA duplex recognition and unwinding by DEAD-box helicase DDX3X Song, He; Ji, Xinhua Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11083-2	journal	July 2019
Direct binding targets of the stringent response alarmone (p)ppGpp Kanjee, Usheer; Ogata, Koji; Houry, Walid A. Molecular Microbiology, Vol. 85, Issue 6, p. 1029-1043 https://doi.org/10.1111/j.1365-2958.2012.08177.x	journal	August 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
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Structure of the PPX/GPPA Phosphatase from Aquifex aeolicus in Complex with the Alarmone ppGpp Kristensen, Ole; Ross, Birthe; Gajhede, Michael Journal of Molecular Biology, Vol. 375, Issue 5 https://doi.org/10.1016/j.jmb.2007.11.073	journal	February 2008
Restoring Low Resolution Structure of Biological Macromolecules from Solution Scattering Using Simulated Annealing Svergun, D. I. Biophysical Journal, Vol. 76, Issue 6, p. 2879-2886 https://doi.org/10.1016/S0006-3495(99)77443-6	journal	June 1999
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
Living dangerously: how Helicobacter pylori survives in the human stomach Montecucco, Cesare; Rappuoli, Rino Nature Reviews Molecular Cell Biology, Vol. 2, Issue 6 https://doi.org/10.1038/35073084	journal	June 2001
Helicobacter pylori Initiates the Stringent Response upon Nutrient and pH Downshift Wells, D. H.; Gaynor, E. C. Journal of Bacteriology, Vol. 188, Issue 10 https://doi.org/10.1128/JB.188.10.3726-3729.2006	journal	May 2006
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
The Functional Cycle of Rnt1p: Five Consecutive Steps of Double-Stranded RNA Processing by a Eukaryotic RNase III Song, He; Fang, Xianyang; Jin, Lan Structure, Vol. 25, Issue 2 https://doi.org/10.1016/j.str.2016.12.013	journal	February 2017
Automated matching of high- and low-resolution structural models Kozin, M. B.; Svergun, D. I. Journal of Applied Crystallography, Vol. 34, Issue 1, p. 33-41 https://doi.org/10.1107/S0021889800014126	journal	February 2001
The Structure of the Exopolyphosphatase (PPX) from Escherichia coli O157:H7 Suggests a Binding Mode for Long Polyphosphate Chains Rangarajan, Erumbi S.; Nadeau, Guy; Li, Yunge Journal of Molecular Biology, Vol. 359, Issue 5 https://doi.org/10.1016/j.jmb.2006.04.031	journal	June 2006
An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. Akiyama, M.; Crooke, E.; Kornberg, A. Journal of Biological Chemistry, Vol. 268, Issue 1 https://doi.org/10.1016/S0021-9258(18)54198-3	journal	January 1993
Determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale Fischer, H.; de Oliveira Neto, M.; Napolitano, H. B. Journal of Applied Crystallography, Vol. 43, Issue 1 https://doi.org/10.1107/S0021889809043076	journal	December 2009
(p)ppGpp: Still Magical? Potrykus, Katarzyna; Cashel, Michael Annual Review of Microbiology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev.micro.62.081307.162903	journal	October 2008
Preparation of selenomethionyl proteins for phase determination Doublié, Sylvie Methods in Enzymology https://doi.org/10.1016/S0076-6879(97)76075-0 p. 523-530	book	January 1997
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Differential regulation by ppGpp versus pppGpp in Escherichia coli Mechold, Undine; Potrykus, Katarzyna; Murphy, Helen Nucleic Acids Research, Vol. 41, Issue 12 https://doi.org/10.1093/nar/gkt302	journal	April 2013
Origin of Exopolyphosphatase Processivity: Fusion of an ASKHA Phosphotransferase and a Cyclic Nucleotide Phosphodiesterase Homolog Alvarado, Johnjeff; Ghosh, Anita; Janovitz, Tyler Structure, Vol. 14, Issue 8 https://doi.org/10.1016/j.str.2006.06.009	journal	August 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
The RelA/SpoT Homolog (RSH) Superfamily: Distribution and Functional Evolution of ppGpp Synthetases and Hydrolases across the Tree of Life Atkinson, Gemma C.; Tenson, Tanel; Hauryliuk, Vasili PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023479	journal	August 2011
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

Similar Records

Survival Strategies in the Aquatic and Terrestrial World: The Impact of Second Messengers on Cyanobacterial Processes

Journal Article · Tue Nov 18 00:00:00 EST 2014 · Life · OSTI ID:1575312

Agostoni, Marco; Montgomery, Beronda

(5'-/sup 32/P)-8-azidoguanosine-3',5'-monophosphate. I. Synthesis and properties. II. Interaction with E. coli proteins

Thesis/Dissertation · Sat Jan 01 00:00:00 EST 1983 · OSTI ID:1575312

Owens, J R

The structure of the exopolyphsophatase (PPX) from Escherchia coli O157:H7 suggests a binding mode for long polyphosphate chains

Journal Article · Sun Jan 01 00:00:00 EST 2006 · J. Mol. Biol. · OSTI ID:1575312

Rangarajan, E; Nadeau, G; Li, Y; +5 more

Title: Structure and activity of PPX/GppA homologs from Escherichia coli and Helicobacter pylori

Citation Formats

References (48)

Similar Records

Related Subjects