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Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase

Aerobic methane oxidation is catalyzed by particulate methane monooxygenase (pMMO), a copper-dependent, membrane metalloenzyme composed of subunits PmoA, PmoB, and PmoC. Characterization of the copper active site has been limited by challenges in spectroscopic analysis stemming from the presence of...

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Autores principales: Ro, Soo Y., Schachner, Luis F., Koo, Christopher W., Purohit, Rahul, Remis, Jonathan P., Kenney, Grace E., Liauw, Brandon W., Thomas, Paul M., Patrie, Steven M., Kelleher, Neil L., Rosenzweig, Amy C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6572826/
https://www.ncbi.nlm.nih.gov/pubmed/31209220
http://dx.doi.org/10.1038/s41467-019-10590-6
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author Ro, Soo Y.
Schachner, Luis F.
Koo, Christopher W.
Purohit, Rahul
Remis, Jonathan P.
Kenney, Grace E.
Liauw, Brandon W.
Thomas, Paul M.
Patrie, Steven M.
Kelleher, Neil L.
Rosenzweig, Amy C.
author_facet Ro, Soo Y.
Schachner, Luis F.
Koo, Christopher W.
Purohit, Rahul
Remis, Jonathan P.
Kenney, Grace E.
Liauw, Brandon W.
Thomas, Paul M.
Patrie, Steven M.
Kelleher, Neil L.
Rosenzweig, Amy C.
author_sort Ro, Soo Y.
collection PubMed
description Aerobic methane oxidation is catalyzed by particulate methane monooxygenase (pMMO), a copper-dependent, membrane metalloenzyme composed of subunits PmoA, PmoB, and PmoC. Characterization of the copper active site has been limited by challenges in spectroscopic analysis stemming from the presence of multiple copper binding sites, effects of detergent solubilization on activity and crystal structures, and the lack of a heterologous expression system. Here we utilize nanodiscs coupled with native top-down mass spectrometry (nTDMS) to determine the copper stoichiometry in each pMMO subunit and to detect post-translational modifications (PTMs). These results indicate the presence of a mononuclear copper center in both PmoB and PmoC. pMMO-nanodisc complexes with a higher stoichiometry of copper-bound PmoC exhibit increased activity, suggesting that the PmoC copper site plays a role in methane oxidation activity. These results provide key insights into the pMMO copper centers and demonstrate the ability of nTDMS to characterize complex membrane-bound metalloenzymes.
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spelling pubmed-65728262019-06-24 Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase Ro, Soo Y. Schachner, Luis F. Koo, Christopher W. Purohit, Rahul Remis, Jonathan P. Kenney, Grace E. Liauw, Brandon W. Thomas, Paul M. Patrie, Steven M. Kelleher, Neil L. Rosenzweig, Amy C. Nat Commun Article Aerobic methane oxidation is catalyzed by particulate methane monooxygenase (pMMO), a copper-dependent, membrane metalloenzyme composed of subunits PmoA, PmoB, and PmoC. Characterization of the copper active site has been limited by challenges in spectroscopic analysis stemming from the presence of multiple copper binding sites, effects of detergent solubilization on activity and crystal structures, and the lack of a heterologous expression system. Here we utilize nanodiscs coupled with native top-down mass spectrometry (nTDMS) to determine the copper stoichiometry in each pMMO subunit and to detect post-translational modifications (PTMs). These results indicate the presence of a mononuclear copper center in both PmoB and PmoC. pMMO-nanodisc complexes with a higher stoichiometry of copper-bound PmoC exhibit increased activity, suggesting that the PmoC copper site plays a role in methane oxidation activity. These results provide key insights into the pMMO copper centers and demonstrate the ability of nTDMS to characterize complex membrane-bound metalloenzymes. Nature Publishing Group UK 2019-06-17 /pmc/articles/PMC6572826/ /pubmed/31209220 http://dx.doi.org/10.1038/s41467-019-10590-6 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Ro, Soo Y.
Schachner, Luis F.
Koo, Christopher W.
Purohit, Rahul
Remis, Jonathan P.
Kenney, Grace E.
Liauw, Brandon W.
Thomas, Paul M.
Patrie, Steven M.
Kelleher, Neil L.
Rosenzweig, Amy C.
Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title_full Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title_fullStr Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title_full_unstemmed Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title_short Native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
title_sort native top-down mass spectrometry provides insights into the copper centers of membrane-bound methane monooxygenase
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6572826/
https://www.ncbi.nlm.nih.gov/pubmed/31209220
http://dx.doi.org/10.1038/s41467-019-10590-6
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