Structural insight into substrate and product binding in an archaeal mevalonate kinase

Miller, Bradley R.; Kung, Yan; Kobe, Bostjan

doi:10.1371/journal.pone.0208419

Title: Structural insight into substrate and product binding in an archaeal mevalonate kinase

Journal Article · 06 December 2018 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0208419 · OSTI ID:1485678

Miller, Bradley R. ^[1];

^[2]; Kobe, Bostjan ^[3]

The Wistar Inst., Philadelphia, PA (United States); Bryn Mawr College, Bryn Mawr, PA (United States)
Bryn Mawr College, Bryn Mawr, PA (United States)
Univ. of Queensland, Brisbane, QLD (Australia)

Mevalonate kinase (MK) is a key enzyme of the mevalonate pathway, which produces the biosynthetic precursors for steroids, including cholesterol, and isoprenoids, the largest class of natural products. Currently available crystal structures of MK from different organisms depict the enzyme in its unbound, substrate-bound, and inhibitor-bound forms; however, until now no structure has yet been determined of MK bound to its product, 5-phosphomevalonate. Here, we present crystal structures of mevalonate-bound and 5-phosphomevalonate-bound MK from Methanosarcina mazei (MmMK), a methanogenic archaeon. In contrast to the prior structure of a eukaryotic MK bound with mevalonate, we find a striking lack of direct interactions between this archaeal MK and its substrate. Further, these two MmMK structures join the prior structure of the apoenzyme to complete the first suite of structural snapshots that depict unbound, substrate-bound, and product-bound forms of the same MK. With this collection of structures, we now provide additional insight into the catalytic mechanism of this biologically essential enzyme.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: National Inst. of Health; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1485678

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 12 Vol. 13; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (43)

Structural analysis of a set of proteins resulting from a bacterial genomics project Badger, J.; Sauder, J. M.; Adams, J. M. Proteins: Structure, Function, and Bioinformatics, Vol. 60, Issue 4 https://doi.org/10.1002/prot.20541	journal	July 2005
Purification and Characterization of Mevalonate Kinase from Suspension-Cultured Cells of Catharanthus roseus (L.) G. Don Schulte, Anna E.; van der Heijden, Robert; Verpoorte, Robert Archives of Biochemistry and Biophysics, Vol. 378, Issue 2 https://doi.org/10.1006/abbi.2000.1779	journal	June 2000
The Scottish Structural Proteomics Facility: targets, methods and outputs Oke, Muse; Carter, Lester G.; Johnson, Kenneth A. Journal of Structural and Functional Genomics, Vol. 11, Issue 2 https://doi.org/10.1007/s10969-010-9090-y	journal	April 2010
Enzymes of the mevalonate pathway of isoprenoid biosynthesis Miziorko, Henry M. Archives of Biochemistry and Biophysics, Vol. 505, Issue 2 https://doi.org/10.1016/j.abb.2010.09.028	journal	January 2011
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
The mevalonate pathway in neurons: It's not just about cholesterol Moutinho, Miguel; Nunes, Maria João; Rodrigues, Elsa Experimental Cell Research, Vol. 360, Issue 1 https://doi.org/10.1016/j.yexcr.2017.02.034	journal	November 2017
Biochemical and Structural Basis for Feedback Inhibition of Mevalonate Kinase and Isoprenoid Metabolism ^† ^, ^‡ Fu, Zhuji; Voynova, Natalia E.; Herdendorf, Timothy J. Biochemistry, Vol. 47, Issue 12 https://doi.org/10.1021/bi7024386	journal	March 2008
Engineering a mevalonate pathway in Escherichia coli for production of terpenoids Martin, Vincent J. J.; Pitera, Douglas J.; Withers, Sydnor T. Nature Biotechnology, Vol. 21, Issue 7 https://doi.org/10.1038/nbt833	journal	June 2003
The interplay between cell signalling and the mevalonate pathway in cancer Mullen, Peter J.; Yu, Rosemary; Longo, Joseph Nature Reviews Cancer, Vol. 16, Issue 11 https://doi.org/10.1038/nrc.2016.76	journal	August 2016
Identification of Catalytic Residues in Human Mevalonate Kinase Potter, David; Miziorko, Henry M. Journal of Biological Chemistry, Vol. 272, Issue 41 https://doi.org/10.1074/jbc.272.41.25449	journal	October 1997
Identification and Functional Characterization of an Active-site Lysine in Mevalonate Kinase Potter, David; Wojnar, Jean M.; Narasimhan, Chakravarthy Journal of Biological Chemistry, Vol. 272, Issue 9 https://doi.org/10.1074/jbc.272.9.5741	journal	February 1997
Structure of the Methanococcus jannaschii Mevalonate Kinase, a Member of the GHMP Kinase Superfamily Yang, Dong; Shipman, Lance W.; Roessner, Charles A. Journal of Biological Chemistry, Vol. 277, Issue 11 https://doi.org/10.1074/jbc.m110787200	journal	December 2001
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/s0021889807021206	journal	July 2007
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/s0907444912001308	journal	March 2012
Crystal structure of the Streptococcus pneumoniae mevalonate kinase in complex with diphosphomevalonate Andreassi, John L.; Bilder, Patrick W.; Vetting, Matthew W. Protein Science, Vol. 16, Issue 5 https://doi.org/10.1110/ps.072755707	journal	May 2007
Structure, substrate recognition and reactivity of Leishmania major mevalonate kinase Sgraja, Tanja; Smith, Terry K.; Hunter, William N. BMC Structural Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1472-6807-7-20	journal	January 2007
Improvements to the APBS biomolecular solvation software suite: Improvements to the APBS Software Suite Jurrus, Elizabeth; Engel, Dave; Star, Keith Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3280	journal	October 2017
Convergent evolution of similar enzymatic function on different protein folds: The hexokinase, ribokinase, and galactokinase families of sugar kinases Bork, Peer; Sander, Chris; Valencia, Alfonso Protein Science, Vol. 2, Issue 1 https://doi.org/10.1002/pro.5560020104	journal	January 1993
Structural analysis of a set of proteins resulting from a bacterial genomics project Badger, J.; Sauder, J. M.; Adams, J. M. Proteins: Structure, Function, and Bioinformatics, Vol. 60, Issue 4 https://doi.org/10.1002/prot.20541	journal	July 2005
Purification and Characterization of Mevalonate Kinase from Suspension-Cultured Cells of Catharanthus roseus (L.) G. Don Schulte, Anna E.; van der Heijden, Robert; Verpoorte, Robert Archives of Biochemistry and Biophysics, Vol. 378, Issue 2 https://doi.org/10.1006/abbi.2000.1779	journal	June 2000
The Scottish Structural Proteomics Facility: targets, methods and outputs Oke, Muse; Carter, Lester G.; Johnson, Kenneth A. Journal of Structural and Functional Genomics, Vol. 11, Issue 2 https://doi.org/10.1007/s10969-010-9090-y	journal	April 2010
Purification and Mechanism of Action of Hog Liver Mevalonic Kinase Beytia, Enrique; Dorsey, J. Kevin; Marr, Jane Journal of Biological Chemistry, Vol. 245, Issue 20 https://doi.org/10.1016/S0021-9258(18)62775-9	journal	October 1970
Enzymes of the mevalonate pathway of isoprenoid biosynthesis Miziorko, Henry M. Archives of Biochemistry and Biophysics, Vol. 505, Issue 2 https://doi.org/10.1016/j.abb.2010.09.028	journal	January 2011
Mevalonate pathway: A review of clinical and therapeutical implications Buhaescu, Irina; Izzedine, Hassane Clinical Biochemistry, Vol. 40, Issue 9-10 https://doi.org/10.1016/j.clinbiochem.2007.03.016	journal	June 2007
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
The mevalonate pathway in neurons: It's not just about cholesterol Moutinho, Miguel; Nunes, Maria João; Rodrigues, Elsa Experimental Cell Research, Vol. 360, Issue 1 https://doi.org/10.1016/j.yexcr.2017.02.034	journal	November 2017
Structural Basis for the Catalysis and Substrate Specificity of Homoserine Kinase ^† Krishna, S. Sri; Zhou, Tianjun; Daugherty, Matthew Biochemistry, Vol. 40, Issue 36 https://doi.org/10.1021/bi010851z	journal	September 2001
Role of Arg228 in the Phosphorylation of Galactokinase: The Mechanism of GHMP Kinases by Quantum Mechanics/Molecular Mechanics Studies Huang, Meilan; Li, Xiaozhou; Zou, Jian-Wei Biochemistry, Vol. 52, Issue 28 https://doi.org/10.1021/bi400228e	journal	July 2013
Biochemical and Structural Basis for Feedback Inhibition of Mevalonate Kinase and Isoprenoid Metabolism ^† ^, ^‡ Fu, Zhuji; Voynova, Natalia E.; Herdendorf, Timothy J. Biochemistry, Vol. 47, Issue 12 https://doi.org/10.1021/bi7024386	journal	March 2008
From Fields to Fuels: Recent Advances in the Microbial Production of Biofuels Kung, Yan; Runguphan, Weerawat; Keasling, Jay D. ACS Synthetic Biology, Vol. 1, Issue 11 https://doi.org/10.1021/sb300074k	journal	November 2012
Production of the antimalarial drug precursor artemisinic acid in engineered yeast Ro, Dae-Kyun; Paradise, Eric M.; Ouellet, Mario Nature, Vol. 440, Issue 7086, p. 940-943 https://doi.org/10.1038/nature04640	journal	April 2006
Engineering a mevalonate pathway in Escherichia coli for production of terpenoids Martin, Vincent J. J.; Pitera, Douglas J.; Withers, Sydnor T. Nature Biotechnology, Vol. 21, Issue 7 https://doi.org/10.1038/nbt833	journal	June 2003
Production of isoprenoid pharmaceuticals by engineered microbes Chang, Michelle C. Y.; Keasling, Jay D. Nature Chemical Biology, Vol. 2, Issue 12 https://doi.org/10.1038/nchembio836	journal	November 2006
The interplay between cell signalling and the mevalonate pathway in cancer Mullen, Peter J.; Yu, Rosemary; Longo, Joseph Nature Reviews Cancer, Vol. 16, Issue 11 https://doi.org/10.1038/nrc.2016.76	journal	August 2016
Identification of Catalytic Residues in Human Mevalonate Kinase Potter, David; Miziorko, Henry M. Journal of Biological Chemistry, Vol. 272, Issue 41 https://doi.org/10.1074/jbc.272.41.25449	journal	October 1997
Identification and Functional Characterization of an Active-site Lysine in Mevalonate Kinase Potter, David; Wojnar, Jean M.; Narasimhan, Chakravarthy Journal of Biological Chemistry, Vol. 272, Issue 9 https://doi.org/10.1074/jbc.272.9.5741	journal	February 1997
Structure of the Methanococcus jannaschii Mevalonate Kinase, a Member of the GHMP Kinase Superfamily Yang, Dong; Shipman, Lance W.; Roessner, Charles A. Journal of Biological Chemistry, Vol. 277, Issue 11 https://doi.org/10.1074/jbc.M110787200	journal	December 2001
The Structure of a Binary Complex between a Mammalian Mevalonate Kinase and ATP: INSIGHTS INTO THE REACTION MECHANISM AND HUMAN INHERITED DISEASE Fu, Zhuji; Wang, Ming; Potter, David Journal of Biological Chemistry, Vol. 277, Issue 20 https://doi.org/10.1074/jbc.M200912200	journal	February 2002
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Crystal structure of the Streptococcus pneumoniae mevalonate kinase in complex with diphosphomevalonate Andreassi, John L.; Bilder, Patrick W.; Vetting, Matthew W. Protein Science, Vol. 16, Issue 5 https://doi.org/10.1110/ps.072755707	journal	May 2007
Characterization of a Feedback-Resistant Mevalonate Kinase from the Archaeon Methanosarcina mazei Primak, Yuliya A.; Du, Mai; Miller, Michael C. Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.05761-11	journal	September 2011
Structure, substrate recognition and reactivity of Leishmania major mevalonate kinase Sgraja, Tanja; Smith, Terry K.; Hunter, William N. BMC Structural Biology, Vol. 7, Issue 1 https://doi.org/10.1186/1472-6807-7-20	journal	January 2007
Improvements to the APBS biomolecular solvation software suite Jurrus, Elizabeth; Engel, Dave; Star, Keith arXiv https://doi.org/10.48550/arxiv.1707.00027	text	January 2017

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Title: Structural insight into substrate and product binding in an archaeal mevalonate kinase

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