Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study

Andrey Y. Kovalevsky; Leif Hanson; S. Zoe Fisher; Marat Mustyakimov; Sax A. Mason; V. Trevor Forsyth; Matthew P. Blakeley; David A. Keen; Trixie Wagner; H. L. Carrell; Amy K. Katz; Jenny P. Glusker; Paul Langan

doi:10.1016/j.str.2010.03.011

Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study

Andrey Y. Kovalevsky, Leif Hanson, S. Zoe Fisher, Marat Mustyakimov, Sax A. Mason, V. Trevor Forsyth, Matthew P. Blakeley, David A. Keen, Trixie Wagner, H. L. Carrell, Amy K. Katz, Jenny P. Glusker, Paul Langan

Research output: Contribution to journal › Article › peer-review

134 Scopus citations

Abstract

Conversion of aldo to keto sugars by the metalloenzyme D-xylose isomerase (XI) is a multistep reaction that involves hydrogen transfer. We have determined the structure of this enzyme by neutron diffraction in order to locate H atoms (or their isotope D). Two studies are presented, one of XI containing cadmium and cyclic D-glucose (before sugar ring opening has occurred), and the other containing nickel and linear D-glucose (after ring opening has occurred but before isomerization). Previously we reported the neutron structures of ligand-free enzyme and enzyme with bound product. The data show that His54 is doubly protonated on the ring N in all four structures. Lys289 is neutral before ring opening and gains a proton after this; the catalytic metal-bound water is deprotonated to hydroxyl during isomerization and O5 is deprotonated. These results lead to new suggestions as to how changes might take place over the course of the reaction.

Original language	English
Pages (from-to)	688-699
Number of pages	12
Journal	Structure
Volume	18
Issue number	6
DOIs	https://doi.org/10.1016/j.str.2010.03.011
State	Published - Jun 2010
Externally published	Yes

Funding

The PCS is funded by the Office of Biological and Environmental Research of the Department of Energy. The PCS is located at the Lujan Center at Los Alamos Neutron Science Center, funded by the DOE Office of Basic Energy Sciences. M.M. and P.L. were partly supported by an NIH-NIGMS funded consortium (1R01GM071939-01) between LANL and LNBL to develop computational tools for neutron protein crystallography. A.Y.K. was partly supported by LANL, LDRD grant (20080789PRD3). A.Y.K. and P.L. were partly supported by a LANL, LDRD grant (20070131ER), JPG CA10925 and Fox Chase CA06927, both from NIH. B.L.H. is supported by NSF 446218. V.T.F. and S.A.M. acknowledge support from EPSRC under grants GR/R47950/01, GR/R99393/01, EP/C015452/1. The new D19 diffractometer was built as part of a collaboration between Durham University, Keele University, Bath University, and ILL. We gratefully acknowledge the help of John Archer, John Allibon, and the efforts of the ILL detector group.

Funders	Funder number
DOE Office of Basic Energy Sciences
NIH-NIGMS	1R01GM071939-01
Office of Biological and Environmental Research of the Department of Energy
National Science Foundation	446218
National Institutes of Health
National Cancer Institute	P30CA006927
Laboratory Directed Research and Development	CA06927, JPG CA10925, 20080789PRD3, 20070131ER
Los Alamos National Laboratory
Engineering and Physical Sciences Research Council	EP/C015452/1, GR/R99393/01, GR/R47950/01

Keywords

Proteins

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.str.2010.03.011

Cite this

Kovalevsky, A. Y., Hanson, L., Fisher, S. Z., Mustyakimov, M., Mason, S. A., Trevor Forsyth, V., Blakeley, M. P., Keen, D. A., Wagner, T., Carrell, H. L., Katz, A. K., Glusker, J. P., & Langan, P. (2010). Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study. Structure, 18(6), 688-699. https://doi.org/10.1016/j.str.2010.03.011

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title = "Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study",

abstract = "Conversion of aldo to keto sugars by the metalloenzyme D-xylose isomerase (XI) is a multistep reaction that involves hydrogen transfer. We have determined the structure of this enzyme by neutron diffraction in order to locate H atoms (or their isotope D). Two studies are presented, one of XI containing cadmium and cyclic D-glucose (before sugar ring opening has occurred), and the other containing nickel and linear D-glucose (after ring opening has occurred but before isomerization). Previously we reported the neutron structures of ligand-free enzyme and enzyme with bound product. The data show that His54 is doubly protonated on the ring N in all four structures. Lys289 is neutral before ring opening and gains a proton after this; the catalytic metal-bound water is deprotonated to hydroxyl during isomerization and O5 is deprotonated. These results lead to new suggestions as to how changes might take place over the course of the reaction.",

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author = "Kovalevsky, {Andrey Y.} and Leif Hanson and Fisher, {S. Zoe} and Marat Mustyakimov and Mason, {Sax A.} and {Trevor Forsyth}, V. and Blakeley, {Matthew P.} and Keen, {David A.} and Trixie Wagner and Carrell, {H. L.} and Katz, {Amy K.} and Glusker, {Jenny P.} and Paul Langan",

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Kovalevsky, AY, Hanson, L, Fisher, SZ, Mustyakimov, M, Mason, SA, Trevor Forsyth, V, Blakeley, MP, Keen, DA, Wagner, T, Carrell, HL, Katz, AK, Glusker, JP & Langan, P 2010, 'Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study', Structure, vol. 18, no. 6, pp. 688-699. https://doi.org/10.1016/j.str.2010.03.011

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T1 - Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase

T2 - A Joint X-Ray and Neutron Diffraction Study

AU - Kovalevsky, Andrey Y.

AU - Hanson, Leif

AU - Fisher, S. Zoe

AU - Mustyakimov, Marat

AU - Mason, Sax A.

AU - Trevor Forsyth, V.

AU - Blakeley, Matthew P.

AU - Keen, David A.

AU - Wagner, Trixie

AU - Carrell, H. L.

AU - Katz, Amy K.

AU - Glusker, Jenny P.

AU - Langan, Paul

PY - 2010/6

Y1 - 2010/6

N2 - Conversion of aldo to keto sugars by the metalloenzyme D-xylose isomerase (XI) is a multistep reaction that involves hydrogen transfer. We have determined the structure of this enzyme by neutron diffraction in order to locate H atoms (or their isotope D). Two studies are presented, one of XI containing cadmium and cyclic D-glucose (before sugar ring opening has occurred), and the other containing nickel and linear D-glucose (after ring opening has occurred but before isomerization). Previously we reported the neutron structures of ligand-free enzyme and enzyme with bound product. The data show that His54 is doubly protonated on the ring N in all four structures. Lys289 is neutral before ring opening and gains a proton after this; the catalytic metal-bound water is deprotonated to hydroxyl during isomerization and O5 is deprotonated. These results lead to new suggestions as to how changes might take place over the course of the reaction.

AB - Conversion of aldo to keto sugars by the metalloenzyme D-xylose isomerase (XI) is a multistep reaction that involves hydrogen transfer. We have determined the structure of this enzyme by neutron diffraction in order to locate H atoms (or their isotope D). Two studies are presented, one of XI containing cadmium and cyclic D-glucose (before sugar ring opening has occurred), and the other containing nickel and linear D-glucose (after ring opening has occurred but before isomerization). Previously we reported the neutron structures of ligand-free enzyme and enzyme with bound product. The data show that His54 is doubly protonated on the ring N in all four structures. Lys289 is neutral before ring opening and gains a proton after this; the catalytic metal-bound water is deprotonated to hydroxyl during isomerization and O5 is deprotonated. These results lead to new suggestions as to how changes might take place over the course of the reaction.

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JF - Structure

IS - 6

ER -

Metal Ion Roles and the Movement of Hydrogen during Reaction Catalyzed by D-Xylose Isomerase: A Joint X-Ray and Neutron Diffraction Study

Abstract

Funding

Keywords

UN SDGs

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