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Original Article

Electron spin-labelling of the EutC subunit in B12-dependent ethanolamine ammonia-lyase reveals dynamics and a two-state conformational equilibrium in the N-terminal, signal-sequence-associated domain

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Pages 307-318 | Received 23 Sep 2017, Accepted 29 Nov 2017, Published online: 18 Dec 2017

References

  • Toraya T. Radical catalysis in coenzyme B12-dependent isomerization (eliminating) reactions. Chem Rev 2003;103:2095–2127.
  • Roof DM, Roth JR. Ethanolamine utilization in salmonella typhimurium. J Bacteriol 1988;170:3855–3863.
  • Roof DM, Roth JR. Functions required for vitamin B12-dependent ethanolamine utilization in Salmonella typhimurium. J Bacteriol 1989;171:3316–3323.
  • Garsin DA. Ethanolamine utilization in bacterial pathogens: roles and regulation. Nat Rev Microbiol 2010;8:290–295.
  • Staib L, Fuchs TM. From food to cell: nutrient exploitation strategies of enteropathogens. Microbiology 2014;160:1020–1039.
  • Thiennimitr P, Winter SE, Winter MG, Xavier MN, Tolstikov V, Huseby DL, et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci USA 2011;108:17480–17485.
  • Faust LP, Babior BM. Overexpression, purification, and some properties of the AdoCbl-dependent ethanolamine ammonia-lyase from Salmonella typhimurium. Arch Biochem Biophys 1992;294:50–54.
  • Shibata N, Tamagaki H, Hieda N, Akita K, Komori H, Shomura Y, et al. Crystal structures of ethanolamine ammonia-lyase complexed with coenzyme B12 analogs and substrates. J Biol Chem 2010;285:26484–26493.
  • Bovell AM, Warncke K. The structural model of Salmonella typhimurium ethanolamine ammonia-lyase directs a rational approach to the assembly of the functional [(EutB-EutC)2]3 oligomer from isolated subunits. Biochemistry 2013;52:1419–1428.
  • Tanaka S, Sawaya MR, Yeates TO. Structure and mechanisms of a protein-based organelle in Escherichia coli. Science 2010;327:81–84.
  • Bobik TA, Lehman BP, Yeates TO. Bacterial microcompartments: widespread prokaryotic organelles for isolation and optimization of metabolic pathways. Mol Microbiol 2015;98:193–207.
  • Wang M, Zhu C, Kohne M, Warncke K. Resolution and characterization of chemical steps in enzyme catalytic sequences by using low-temperature and time-resolved, full-spectrum EPR spectroscopy in fluid cryosolvent and frozen solution systems. Meth Enzymol 2015;563:59–94.
  • Zhu C, Warncke K. Reaction of the Co(II)-substrate radical pair catalytic intermediate in coenzyme B12-dependent ethanolamine ammonia-lyase in frozen aqueous solution from 190 to 217 K. Biophys J 2008;95:5890–5900.
  • Kohne M, Zhu C, Warncke K. Two dynamical regimes of the substrate radical rearrangement reaction in B12-dependent ethanolamine ammonia-lyase resolve contributions of native protein configurations and collective configurational fluctuations to catalysis. Biochemistry 2017;56:3257–3264.
  • Fenimore PW, Frauenfelder H, McMahon BH, Young RD. Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci USA 2004;101:14408–14413.
  • Frauenfelder H, Chen G, Berendzen J, Fenimore PW, Jansson H, McMahon BH, et al. A unified model of protein dynamics. Proc Natl Acad Sci USA 2009;106:5129–5134.
  • Vitkup D, Ringe D, Petsko GA, Karplus M. Solvent mobility and the protein “glass” transition. Nat Struct Biol 2000;7:34–38.
  • Franks F. Freeze-drying of bioproducts: putting principles into practice. Eur J Pharm Biopharm 1998;45:221–229.
  • Goff HD, Verespej E, Jermann D. Glass transitions in frozen sucrose solutions are influenced by solute inclusions within ice crystals. Thermochim Acta 2003;399:43–55.
  • Franks F. Scientific and technological aspects of aqueous glasses. Biophys Chem 2003;105:251–261.
  • Douzou P Cryobiochemistry: an introduction. New York: Academic Press; 1977.
  • Rasmussen DH, Mackenzie AP. Phase diagram for the system water-dimethylsulphoxide. Nature 1968;220:1315–1317.
  • Murthy SSN. Phase behavior of the supercooled aqueous solutions of dimethyl sulfoxide, ethylene glycol, and methanol as seen by dielectric spectroscopy. J Phys Chem B 1997;101:6043–6049.
  • Bordignon E, Steinhoff H-J Membrane protein structure and dynamics studied by site-directed spin-labeling ESR. In ESR spectroscopy in membrane biophysics; biological magnetic resonance. Berlin: Springer; 2007.
  • Jeschke G. Conformational dynamics and distribution of nitroxide spin labels. Prog Nucl Magn Reson Spectrosc 2013;72:42–60.
  • Altenbach C, López CJ, Hideg K, Hubbell WL. Exploring structure, dynamics, and topology of nitroxide spin-labeled proteins using continuous-wave electron paramagnetic resonance spectroscopy. Meth Enzymol 2015;564:59–100.
  • Todd AP, Cong J, Levinthal F, Levinthal C, Hubbell WL. Site-directed mutagenesis of colicin E1 provides specific attachment sites for spin labels whose spectra are sensitive to local conformation. Proteins 1989;6:294–305.
  • Mchaourab HS, Lietzow MA, Hideg K, Hubbell WL. Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 1996;35:7692–7704.
  • Ahmad S, Gromiha M, Fawareh H, Sarai A. ASAView: database and tool for solvent accessibility representation in proteins. BMC Bioinformatics 2004;5:51.
  • Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983;22:2577–2637.
  • Fan C, Cheng S, Liu Y, Escobar CM, Crowley CS, Jefferson RE, et al. Short N-terminal sequences package proteins into bacterial microcompartments. Proc Natl Acad Sci USA 2010;107:7509–7514.
  • Choudhary S, Quin MB, Sanders MA, Escobar CM, Crowley CS, Jefferson RE, et al. Engineered protein nano-compartments for targeted enzyme localization. PLoS One 2012;7:e33342.
  • Faust LRP, Connor JA, Roof DM, Hoch JA, Babior BM. Cloning, sequencing, and expression of the genes encoding the adenosylcobalamin-dependent ethanolamine ammonia-lyase of Salmonella typhimurium. J Biol Chem 1990;265:12462–12466.
  • Kaplan BH, Stadtman ER. Ethanolamine deaminase a cobamide coenzyme-dependent enzyme. I. Purification assay and properties of enzyme. J Biol Chem Rev 1968;243:1787–1793.
  • Morrison KL, Weiss GA. Combinatorial alanine-scanning. Curr Opin Chem Biol 2001;5:302–307.
  • Stoll S, Schweiger A. EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J Magn Reson 2006;178:42–55.
  • Chen H, Sun L, Warncke K. Heterogeneous ordered-disordered structure of the mesodomain in frozen sucrose-water solutions revealed by multiple electron paramagnetic resonance spectroscopies. Langmuir 2013;29:4357–4365.
  • Wertz JE, Bolton JR Electron spin resonance. Chapman & Hall; 1986.
  • Banerjee D, Bhat SN, Bhat SV, Leporini D. ESR evidence for 2 coexisting liquid phases in deeply supercooled bulk water. Proc Natl Acad Sci USA 2009;106:11448–11453.
  • Carugo O. Predicting residue solvent accessibility from protein sequence by considering the sequence environment. Protein Eng 2000;13:607–609.
  • Chen H, Zhou HX. Prediction of solvent accessibility and sites of deleterious mutations from protein sequence. Nucleic Acids Res 2005;33:3193–3199.
  • Zhang H, Zhang T, Chen K, Shen S, Ruan J, Kurgan L. On the relation between residue flexibility and local solvent accessibility in proteins. Proteins 2009;76:617–636.
  • Wu W, Wang Z, Cong P, Li T. Accurate prediction of protein relative solvent accessibility using a balanced model. BioData Min 2017;10:1.
  • Akita K, Hieda N, Baba N, Kawaguchi S, Sakamoto H, Nakanishi Y, et al. Purification and some properties of wild-type and N-terminal-truncated ethanolamine ammonia-lyase of Escherichia coli. J Biochem 2010;147:83–93.
  • Guruprasad K, Reddy BV, Pandit MW. Correlation between stability of a protein and its dipeptide composition – a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng 1990;4:155–161.
  • Canfield JM, Warncke K. Geometry of reactant centers in the Co II substrate radical pair state of coenzyme B 12-dependent ethanolamine deaminase determined by using orientation-selection-ESEEM spectroscopy. J Phys Chem B 2002;106:8831–8841.
  • Polyhach Y, Bordignon E, Jeschke G. Rotamer libraries of spin labelled cysteines for protein studies. Phys Chem Chem Phys 2011;13:2356–2366.
  • Hatmal MM, Li Y, Hegde BG, Hegde PB, Jao CC. Computer modeling of nitroxide spin labels on proteins. Biopolymers 2012;97:35–44.
  • Hagelueken G, Ward R, Naismith JH, Schiemann O. MtsslWizard: in silico spin-labelling and generation of distance distributions in PyMOL. Appl Magn Reson 2012;42:377–391.
  • Cornish-Bowden A. Fundamentals of enzyme kinetics. London: Butterworths and Company, Ltd; 1981.

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