3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase

Abstract Advances in X-ray crystallography and cryogenic electron microscopy (cryo-EM) offer the promise of elucidating functionally relevant conformational changes that are not easily studied by other biophysical methods. Here we show that 3D variability analysis (3DVA) of the cryo-EM map for wild-...

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Main Authors: Adriana Coricello, Alanya J. Nardone, Antonio Lupia, Carmen Gratteri, Matthijn Vos, Vincent Chaptal, Stefano Alcaro, Wen Zhu, Yuichiro Takagi, Nigel G. J. Richards
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54912-9
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author Adriana Coricello
Alanya J. Nardone
Antonio Lupia
Carmen Gratteri
Matthijn Vos
Vincent Chaptal
Stefano Alcaro
Wen Zhu
Yuichiro Takagi
Nigel G. J. Richards
author_facet Adriana Coricello
Alanya J. Nardone
Antonio Lupia
Carmen Gratteri
Matthijn Vos
Vincent Chaptal
Stefano Alcaro
Wen Zhu
Yuichiro Takagi
Nigel G. J. Richards
author_sort Adriana Coricello
collection DOAJ
description Abstract Advances in X-ray crystallography and cryogenic electron microscopy (cryo-EM) offer the promise of elucidating functionally relevant conformational changes that are not easily studied by other biophysical methods. Here we show that 3D variability analysis (3DVA) of the cryo-EM map for wild-type (WT) human asparagine synthetase (ASNS) identifies a functional role for the Arg-142 side chain and test this hypothesis experimentally by characterizing the R142I variant in which Arg-142 is replaced by isoleucine. Support for Arg-142 playing a role in the intramolecular translocation of ammonia between the active site of the enzyme is provided by the glutamine-dependent synthetase activity of the R142 variant relative to WT ASNS, and MD simulations provide a possible molecular mechanism for these findings. Combining 3DVA with MD simulations is a generally applicable approach to generate testable hypotheses of how conformational changes in buried side chains might regulate function in enzymes.
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institution Kabale University
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publishDate 2024-12-01
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series Nature Communications
spelling doaj-art-22f449e680ca4a2fa2a7745c2d6980bc2024-12-08T12:37:05ZengNature PortfolioNature Communications2041-17232024-12-0115111510.1038/s41467-024-54912-93D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetaseAdriana Coricello0Alanya J. Nardone1Antonio Lupia2Carmen Gratteri3Matthijn Vos4Vincent Chaptal5Stefano Alcaro6Wen Zhu7Yuichiro Takagi8Nigel G. J. Richards9Dipartimento di Scienze della Salute, Università “Magna Græcia” di CatanzaroDepartment of Chemistry & Biochemistry, Florida State UniversityNet4Science Academic Spin-Off, Università “Magna Græcia” di CatanzaroDipartimento di Scienze della Salute, Università “Magna Græcia” di CatanzaroNanoImaging Core Facility, Centre de Resources et Recherches Technologiques, Institut PasteurMolecular Microbiology and Structural Biochemistry Laboratory, CNRS UMR 5086, University of LyonDipartimento di Scienze della Salute, Università “Magna Græcia” di CatanzaroDepartment of Chemistry & Biochemistry, Florida State UniversityDepartment of Biochemistry & Molecular Biology, Indiana University School of MedicineSchool of Chemistry, Cardiff UniversityAbstract Advances in X-ray crystallography and cryogenic electron microscopy (cryo-EM) offer the promise of elucidating functionally relevant conformational changes that are not easily studied by other biophysical methods. Here we show that 3D variability analysis (3DVA) of the cryo-EM map for wild-type (WT) human asparagine synthetase (ASNS) identifies a functional role for the Arg-142 side chain and test this hypothesis experimentally by characterizing the R142I variant in which Arg-142 is replaced by isoleucine. Support for Arg-142 playing a role in the intramolecular translocation of ammonia between the active site of the enzyme is provided by the glutamine-dependent synthetase activity of the R142 variant relative to WT ASNS, and MD simulations provide a possible molecular mechanism for these findings. Combining 3DVA with MD simulations is a generally applicable approach to generate testable hypotheses of how conformational changes in buried side chains might regulate function in enzymes.https://doi.org/10.1038/s41467-024-54912-9
spellingShingle Adriana Coricello
Alanya J. Nardone
Antonio Lupia
Carmen Gratteri
Matthijn Vos
Vincent Chaptal
Stefano Alcaro
Wen Zhu
Yuichiro Takagi
Nigel G. J. Richards
3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
Nature Communications
title 3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
title_full 3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
title_fullStr 3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
title_full_unstemmed 3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
title_short 3D variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
title_sort 3d variability analysis reveals a hidden conformational change controlling ammonia transport in human asparagine synthetase
url https://doi.org/10.1038/s41467-024-54912-9
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