The structure of S . lividans acetoacetyl-CoA synthetase shows a novel interaction between the C-terminal extension and the N-terminal domain

Mitchell, Carter A.; Tucker, Alex C.; Escalante-Semerena, Jorge C.; Gulick, Andrew M.

doi:10.1002/prot.24738

The structure of S . lividans acetoacetyl-CoA synthetase shows a novel interaction between the C-terminal extension and the N-terminal domain

Journal Article · Tue Dec 09 00:00:00 EST 2014 · Proteins

DOI:https://doi.org/10.1002/prot.24738· OSTI ID:1343103

Mitchell, Carter A. ^[1]; Tucker, Alex C. ^[2]; Escalante-Semerena, Jorge C. ^[2]; Gulick, Andrew M. ^[3]

Hauptman-Woodward Institute, Buffalo New York 14203; Department of Structural Biology, University at Buffalo, Buffalo New York 14203; Office of Scientific and Technical Information (OSTI)
Department of Microbiology, University of Georgia, Athens Georgia 30602
Hauptman-Woodward Institute, Buffalo New York 14203; Department of Structural Biology, University at Buffalo, Buffalo New York 14203

The adenosine monoposphate-forming acyl-CoA synthetase enzymes catalyze a two-step reaction that involves the initial formation of an acyl adenylate that reacts in a second partial reaction to form a thioester between the acyl substrate and CoA. These enzymes utilize a Domain Alternation catalytic mechanism, whereby a ~110 residue C-terminal domain rotates by 140° to form distinct catalytic conformations for the two partial reactions. In this paper, the structure of an acetoacetyl-CoA synthetase (AacS) is presented that illustrates a novel aspect of this C-terminal domain. Specifically, several acetyl- and acetoacetyl-CoA synthetases contain a 30-residue extension on the C-terminus compared to other members of this family. Finally, whereas residues from this extension are disordered in prior structures, the AacS structure shows that residues from this extension may interact with key catalytic residues from the N-terminal domain.

View Accepted Manuscript (DOE)

Research Organization:: Hauptman-Woodward Inst., Buffalo, NY (United States); Univ. at Buffalo, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1343103

Journal Information:: Proteins, Journal Name: Proteins Journal Issue: 3 Vol. 83; ISSN 0887-3585

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (19)

[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Structural and Functional Investigation of the Intermolecular Interaction between NRPS Adenylation and Carrier Protein Domains Sundlov, Jesse A.; Shi, Ce; Wilson, Daniel J. Chemistry & Biology, Vol. 19, Issue 2 https://doi.org/10.1016/j.chembiol.2011.11.013	journal	February 2012
Characterization of the Propionyl-CoA Synthetase (PrpE) Enzyme of Salmonella enterica : Residue Lys592 Is Required for Propionyl-AMP Synthesis ^† Horswill, Alexander R.; Escalante-Semerena, Jorge C. Biochemistry, Vol. 41, Issue 7 https://doi.org/10.1021/bi015647q	journal	February 2002
The 1.75 Å Crystal Structure of Acetyl-CoA Synthetase Bound to Adenosine-5‘-propylphosphate and Coenzyme A ^† Gulick, Andrew M.; Starai, Vincent J.; Horswill, Alexander R. Biochemistry, Vol. 42, Issue 10, p. 2866-2873 https://doi.org/10.1021/bi0271603	journal	March 2003
Crystal Structure of Yeast Acetyl-Coenzyme A Synthetase in Complex with AMP Jogl, Gerwald; Tong, Liang Biochemistry, Vol. 43, Issue 6, p. 1425-1431 https://doi.org/10.1021/bi035911a	journal	February 2004
Mutagenesis Evidence that the Partial Reactions of Firefly Bioluminescence Are Catalyzed by Different Conformations of the Luciferase C-Terminal Domain ^† Branchini, Bruce R.; Southworth, Tara L.; Murtiashaw, Martha H. Biochemistry, Vol. 44, Issue 5 https://doi.org/10.1021/bi047903f	journal	February 2005
Crystal Structure of Firefly Luciferase in a Second Catalytic Conformation Supports a Domain Alternation Mechanism Sundlov, Jesse A.; Fontaine, Danielle M.; Southworth, Tara L. Biochemistry, Vol. 51, Issue 33 https://doi.org/10.1021/bi300934s	journal	August 2012
Biochemical and Crystallographic Analysis of Substrate Binding and Conformational Changes in Acetyl-CoA Synthetase ^† ^, ^‡ Reger, Albert S.; Carney, Jill M.; Gulick, Andrew M. Biochemistry, Vol. 46, Issue 22 https://doi.org/10.1021/bi6026506	journal	June 2007
Structural Characterization of a 140° Domain Movement in the Two-Step Reaction Catalyzed by 4-Chlorobenzoate:CoA Ligase ^† ^‡ Reger, Albert S.; Wu, Rui; Dunaway-Mariano, Debra Biochemistry, Vol. 47, Issue 31 https://doi.org/10.1021/bi800696y	journal	August 2008
Conformational Dynamics in the Acyl-CoA Synthetases, Adenylation Domains of Non-ribosomal Peptide Synthetases, and Firefly Luciferase Gulick, Andrew M. ACS Chemical Biology, Vol. 4, Issue 10, p. 811-827 https://doi.org/10.1021/cb900156h	journal	October 2009
Crystal Structure of DltA: IMPLICATIONS FOR THE REACTION MECHANISM OF NON-RIBOSOMAL PEPTIDE SYNTHETASE ADENYLATION DOMAINS Yonus, Huma; Neumann, Piotr; Zimmermann, Stephan Journal of Biological Chemistry, Vol. 283, Issue 47 https://doi.org/10.1074/jbc.M800557200	journal	September 2008
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
Blu-Ice and the Distributed Control System : software for data acquisition and instrument control at macromolecular crystallography beamlines McPhillips, Timothy M.; McPhillips, Scott E.; Chiu, Hsiu-Ju Journal of Synchrotron Radiation, Vol. 9, Issue 6 https://doi.org/10.1107/S0909049502015170	journal	November 2002
Acetoacetyl-CoA synthetase activity is controlled by a protein acetyltransferase with unique domain organization in Streptomyces lividans : Lysine acetylation control of AacS in Tucker, Alex C.; Escalante-Semerena, Jorge C. Molecular Microbiology, Vol. 87, Issue 1 https://doi.org/10.1111/mmi.12088	journal	November 2012
Sir2-Dependent Activation of Acetyl-CoA Synthetase by Deacetylation of Active Lysine Starai, V. J.; Celic, I.; Cole, R. N. Science, Vol. 298, Issue 5602, p. 2390-2392 https://doi.org/10.1126/science.1077650	journal	December 2002
Determinants within the C-Terminal Domain of Streptomyces lividans Acetyl-CoA Synthetase that Block Acetylation of Its Active Site Lysine In Vitro by the Protein Acetyltransferase (Pat) Enzyme Tucker, Alex C.; Escalante-Semerena, Jorge C. PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099817	journal	June 2014

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59 BASIC BIOLOGICAL SCIENCES
ANL superfamily
adenylate-forming enzymes
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The structure of S . lividans acetoacetyl-CoA synthetase shows a novel interaction between the C-terminal extension and the N-terminal domain

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References (19)

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