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Direct determination of protonation states and visualization of hydrogen bonding in a glycoside hydrolase with neutron crystallography.

Wan Q, Parks JM, Hanson BL, Fisher SZ, Ostermann A, Schrader TE, Graham DE, Coates L, Langan P, Kovalevsky A
Proc Natl Acad Sci U S A 112 12384-9 (2015)
Related entries: 4hk8, 4hk9, 4hkl, 4hko, 4hkw, 4s2d, 4s2f, 4s2g, 4s2h, 4xq4, 4xqd, 4xqw, 6k9x

Cited: 19 times
EuropePMC logo PMID: 26392527

Abstract

Glycoside hydrolase (GH) enzymes apply acid/base chemistry to catalyze the decomposition of complex carbohydrates. These ubiquitous enzymes accept protons from solvent and donate them to substrates at close to neutral pH by modulating the pKa values of key side chains during catalysis. However, it is not known how the catalytic acid residue acquires a proton and transfers it efficiently to the substrate. To better understand GH chemistry, we used macromolecular neutron crystallography to directly determine protonation and ionization states of the active site residues of a family 11 GH at multiple pD (pD=pH+0.4) values. The general acid glutamate (Glu) cycles between two conformations, upward and downward, but is protonated only in the downward orientation. We performed continuum electrostatics calculations to estimate the pKa values of the catalytic Glu residues in both the apo- and substrate-bound states of the enzyme. The calculated pKa of the Glu increases substantially when the side chain moves down. The energy barrier required to rotate the catalytic Glu residue back to the upward conformation, where it can protonate the glycosidic oxygen of the substrate, is 4.3 kcal/mol according to free energy simulations. These findings shed light on the initial stage of the glycoside hydrolysis reaction in which molecular motion enables the general acid catalyst to obtain a proton from the bulk solvent and deliver it to the glycosidic oxygen.

Reviews - 4xpv mentioned but not cited (2)

  1. Fifteen years of the Protein Crystallography Station: the coming of age of macromolecular neutron crystallography. Chen JC, Unkefer CJ. IUCrJ 4 72-86 (2017)
  2. Evaluation of models determined by neutron diffraction and proposed improvements to their validation and deposition. Liebschner D, Afonine PV, Moriarty NW, Langan P, Adams PD. Acta Crystallogr D Struct Biol 74 800-813 (2018)

Articles - 4xpv mentioned but not cited (2)

  1. Direct determination of protonation states and visualization of hydrogen bonding in a glycoside hydrolase with neutron crystallography. Wan Q, Parks JM, Hanson BL, Fisher SZ, Ostermann A, Schrader TE, Graham DE, Coates L, Langan P, Kovalevsky A. Proc Natl Acad Sci U S A 112 12384-12389 (2015)
  2. Neutron crystallographic refinement with REFMAC5 from the CCP4 suite. Catapano L, Long F, Yamashita K, Nicholls RA, Steiner RA, Murshudov GN. Acta Crystallogr D Struct Biol 79 1056-1070 (2023)


Reviews citing this publication (1)

  1. The use of neutron scattering to determine the functional structure of glycoside hydrolase. Nakamura A, Ishida T, Samejima M, Igarashi K. Curr Opin Struct Biol 40 54-61 (2016)

Articles citing this publication (14)

  1. Direct visualization of critical hydrogen atoms in a pyridoxal 5'-phosphate enzyme. Dajnowicz S, Johnston RC, Parks JM, Blakeley MP, Keen DA, Weiss KL, Gerlits O, Kovalevsky A, Mueser TC. Nat Commun 8 955 (2017)
  2. The human gut symbiont Ruminococcus gnavus shows specificity to blood group A antigen during mucin glycan foraging: Implication for niche colonisation in the gastrointestinal tract. Wu H, Crost EH, Owen CD, van Bakel W, Martínez Gascueña A, Latousakis D, Hicks T, Walpole S, Urbanowicz PA, Ndeh D, Monaco S, Sánchez Salom L, Griffiths R, Reynolds RS, Colvile A, Spencer DIR, Walsh M, Angulo J, Juge N. PLoS Biol 19 e3001498 (2021)
  3. Configurational Entropy of Folded Proteins and Its Importance for Intrinsically Disordered Proteins. Liu M, Das AK, Lincoff J, Sasmal S, Cheng SY, Vernon RM, Forman-Kay JD, Head-Gordon T. Int J Mol Sci 22 3420 (2021)
  4. Structural and functional characterization of a highly stable endo-β-1,4-xylanase from Fusarium oxysporum and its development as an efficient immobilized biocatalyst. Gómez S, Payne AM, Savko M, Fox GC, Shepard WE, Fernandez FJ, Cristina Vega M. Biotechnol Biofuels 9 191 (2016)
  5. Neutron structure of the T26H mutant of T4 phage lysozyme provides insight into the catalytic activity of the mutant enzyme and how it differs from that of wild type. Hiromoto T, Meilleur F, Shimizu R, Shibazaki C, Adachi M, Tamada T, Kuroki R. Protein Sci 26 1953-1963 (2017)
  6. Maize WI5 encodes an endo-1,4-β-xylanase required for secondary cell wall synthesis and water transport in xylem. Hu X, Cui Y, Lu X, Song W, Lei L, Zhu J, Lai J, E L, Zhao H. J Integr Plant Biol 62 1607-1624 (2020)
  7. Protonation State of an Important Histidine from High Resolution Structures of Lytic Polysaccharide Monooxygenases. Banerjee S, Muderspach SJ, Tandrup T, Frandsen KEH, Singh RK, Ipsen JØ, Hernández-Rollán C, Nørholm MHH, Bjerrum MJ, Johansen KS, Lo Leggio L. Biomolecules 12 194 (2022)
  8. Capturing the Catalytic Proton of Dihydrofolate Reductase: Implications for General Acid-Base Catalysis. Wan Q, Bennett BC, Wymore T, Li Z, Wilson MA, Brooks CL, Langan P, Kovalevsky A, Dealwis CG. ACS Catal 11 5873-5884 (2021)
  9. Capture of activated dioxygen intermediates at the copper-active site of a lytic polysaccharide monooxygenase. Schröder GC, O'Dell WB, Webb SP, Agarwal PK, Meilleur F. Chem Sci 13 13303-13320 (2022)
  10. Titration of ionizable groups in proteins using multiple neutron data sets from a single crystal: application to the small GTPase Ras. Knihtila R, Volmar AY, Meilleur F, Mattos C. Acta Crystallogr F Struct Biol Commun 75 111-115 (2019)
  11. Description of peptide bond planarity from high-resolution neutron crystallography. Hanazono Y, Hirano Y, Tamada T, Miki K. Biophys Physicobiol 20 e200035 (2023)
  12. Investigating the effect of substrate binding on the catalytic activity of xylanase. Ma L, Li G, Liu Y, Li Z, Miao Y, Wan Q, Liu D, Zhang R. Appl Microbiol Biotechnol 107 6873-6886 (2023)
  13. Neutron and X-ray crystal structures of Lactobacillus brevis alcohol dehydrogenase reveal new insights into hydrogen-bonding pathways. Hermann J, Nowotny P, Schrader TE, Biggel P, Hekmat D, Weuster-Botz D. Acta Crystallogr F Struct Biol Commun 74 754-764 (2018)
  14. Structural and biophysical characterization of the multidomain xylanase Xyl. Anye V, Kruger RF, Schubert WD. PLoS One 17 e0269188 (2022)


Related citations provided by authors (3)

  1. Preliminary joint X-ray and neutron protein crystallographic studies of endoxylanase II from the fungus Trichoderma longibrachiatum.. Kovalevsky AY, Hanson BL, Seaver S, Fisher SZ, Mustyakimov M, Langan P Acta Crystallogr Sect F Struct Biol Cryst Commun 67 283-6 (2011)
  2. X-ray crystallographic studies of family 11 xylanase Michaelis and product complexes: implications for the catalytic mechanism.. Wan Q, Zhang Q, Hamilton-Brehm S, Weiss K, Mustyakimov M, Coates L, Langan P, Graham D, Kovalevsky A Acta Crystallogr D Biol Crystallogr 70 11-23 (2014)
  3. Heterologous expression, purification, crystallization and preliminary X-ray analysis of Trichoderma reesei xylanase II and four variants.. Wan Q, Kovalevsky A, Zhang Q, Hamilton-Brehm S, Upton R, Weiss KL, Mustyakimov M, Graham D, Coates L, Langan P Acta Crystallogr Sect F Struct Biol Cryst Commun 69 320-3 (2013)

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