Acetylation by Eis and Deacetylation by Rv1151c of Mycobacterium tuberculosis HupB: Biochemical and Structural Insight

Green, Keith D.; Biswas, Tapan; Pang, Allan H.; Willby, Melisa J.; Reed, Matthew S.; Stuchlik, Olga; Pohl, Jan; Posey, James E.; Tsodikov, Oleg V.; Garneau-Tsodikova, Sylvie

doi:10.1021/acs.biochem.7b01089

Title: Acetylation by Eis and Deacetylation by Rv1151c of Mycobacterium tuberculosis HupB: Biochemical and Structural Insight

Journal Article · Thu Jan 18 00:00:00 EST 2018 · Biochemistry

DOI:https://doi.org/10.1021/acs.biochem.7b01089· OSTI ID:1424796

Green, Keith D. ^[1]; Biswas, Tapan ^[2]; Pang, Allan H. ^[1]; Willby, Melisa J. ^[3]; Reed, Matthew S. ^[3]; Stuchlik, Olga ^[3]; Pohl, Jan ^[3]; Posey, James E. ^[3]; Tsodikov, Oleg V. ^[1];

^[1]

Univ. of Kentucky, Lexington, KY (United States)
Univ. of California, San Diego, La Jolla, CA (United States)
Centers for Disease Control and Prevention, Atlanta, GA (United States)

Bacterial nucleoid-associated proteins (NAPs) are critical to genome integrity and chromosome maintenance. Post-translational modifications of bacterial NAPs appear to function similarly to their better studied mammalian counterparts. The histone-like NAP HupB from Mycobacterium tuberculosis (Mtb) was previously observed to be acetylated by the acetyltransferase Eis, leading to genome reorganization. We report biochemical and structural aspects of acetylation of HupB by Eis. We also found that the SirT-family NAD⁺-dependent deacetylase Rv1151c from Mtb deacetylated HupB in vitro and characterized the deacetylation kinetics. Here, we propose that activities of Eis and Rv1151c could regulate the acetylation status of HupB to remodel the mycobacterial chromosome in response to environmental changes.

View Accepted Manuscript (DOE)

Cite

Export

Save

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

Sponsoring Organization:: National Institutes of Health (NIH)

Grant/Contract Number:: AI090048

OSTI ID:: 1424796

Journal Information:: Biochemistry, Vol. 57, Issue 5; ISSN 0006-2960

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

Citation Metrics:

Cited by: 19 works

Citation information provided by
Web of Science

References (50)

Regulation of Cellular Metabolism by Protein Lysine Acetylation Zhao, S.; Xu, W.; Jiang, W. Science, Vol. 327, Issue 5968 https://doi.org/10.1126/science.1179689	journal	February 2010
Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions Choudhary, C.; Kumar, C.; Gnad, F. Science, Vol. 325, Issue 5942 https://doi.org/10.1126/science.1175371	journal	July 2009
Histone acetyltransferase complexes: one size doesn't fit all Lee, Kenneth K.; Workman, Jerry L. Nature Reviews Molecular Cell Biology, Vol. 8, Issue 4 https://doi.org/10.1038/nrm2145	journal	April 2007
Functions of Site-Specific Histone Acetylation and Deacetylation Shahbazian, Mona D.; Grunstein, Michael Annual Review of Biochemistry, Vol. 76, Issue 1 https://doi.org/10.1146/annurev.biochem.76.052705.162114	journal	June 2007
Isoform-selective histone deacetylase inhibitors Bieliauskas, Anton V.; Pflum, Mary Kay H. Chemical Society Reviews, Vol. 37, Issue 7 https://doi.org/10.1039/b703830p	journal	January 2008
HDAC inhibitors overcome first hurdle Garber, Ken Nature Biotechnology, Vol. 25, Issue 1 https://doi.org/10.1038/nbt0107-17	journal	January 2007
Therapeutic application of histone deacetylase inhibitors for central nervous system disorders Kazantsev, Aleksey G.; Thompson, Leslie M. Nature Reviews Drug Discovery, Vol. 7, Issue 10 https://doi.org/10.1038/nrd2681	journal	October 2008
Acetylation of Metabolic Enzymes Coordinates Carbon Source Utilization and Metabolic Flux Wang, Q.; Zhang, Y.; Yang, C. Science, Vol. 327, Issue 5968 https://doi.org/10.1126/science.1179687	journal	February 2010
Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv: Survival strategies of mycobacteria in host Meena, Laxman S.; Rajni, FEBS Journal, Vol. 277, Issue 11 https://doi.org/10.1111/j.1742-4658.2010.07666.x	journal	May 2010
Mycobacterial genes essential for the pathogen's survival in the host Ehrt, Sabine; Rhee, Kyu; Schnappinger, Dirk Immunological Reviews, Vol. 264, Issue 1 https://doi.org/10.1111/imr.12256	journal	February 2015
Unusual regioversatility of acetyltransferase Eis, a cause of drug resistance in XDR-TB Chen, Wenjing; Biswas, Tapan; Porter, Vanessa R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 24 https://doi.org/10.1073/pnas.1105379108	journal	May 2011
Overexpression of the chromosomally encoded aminoglycoside acetyltransferase eis confers kanamycin resistance in Mycobacterium tuberculosis Zaunbrecher, M. A.; Sikes, R. D.; Metchock, B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 47 https://doi.org/10.1073/pnas.0907925106	journal	November 2009
Mycobacterium tuberculosis EIS gene inhibits macrophage autophagy through up-regulation of IL-10 by increasing the acetylation of histone H3 Duan, Liang; Yi, Min; Chen, Juan Biochemical and Biophysical Research Communications, Vol. 473, Issue 4 https://doi.org/10.1016/j.bbrc.2016.04.045	journal	May 2016
Mycobacterium tuberculosis Eis protein initiates suppression of host immune responses by acetylation of DUSP16/MKP-7 Kim, K. H.; An, D. R.; Song, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 20 https://doi.org/10.1073/pnas.1120251109	journal	April 2012
Expression, production and release of the Eis protein by Mycobacterium tuberculosis during infection of macrophages and its effect on cytokine secretion Samuel, L. P.; Song, C. -H.; Wei, J. Microbiology, Vol. 153, Issue 2 https://doi.org/10.1099/mic.0.2006/002642-0	journal	February 2007
Eis (Enhanced Intracellular Survival) Protein of Mycobacterium tuberculosis Disturbs the Cross Regulation of T-cells Lella, Ravi K.; Sharma, Charu Journal of Biological Chemistry, Vol. 282, Issue 26 https://doi.org/10.1074/jbc.C600280200	journal	June 2007
Mycobacterium tuberculosis Eis Regulates Autophagy, Inflammation, and Cell Death through Redox-dependent Signaling Shin, Dong-Min; Jeon, Bo-Young; Lee, Hye-Mi PLoS Pathogens, Vol. 6, Issue 12 https://doi.org/10.1371/journal.ppat.1001230	journal	December 2010
Lysine acetylation of the Mycobacterium tuberculosis HU protein modulates its DNA binding and genome organization : Acetylation of MtHU by Eis Ghosh, Soumitra; Padmanabhan, Bhavna; Anand, Chinmay Molecular Microbiology, Vol. 100, Issue 4 https://doi.org/10.1111/mmi.13339	journal	February 2016
Identification of Mycobacterium tuberculosis genes preferentially expressed during human infection Kumar, Manoj; Khan, Farrah G.; Sharma, Sandeep Microbial Pathogenesis, Vol. 50, Issue 1 https://doi.org/10.1016/j.micpath.2010.10.003	journal	January 2011
Direct regulation of topoisomerase activity by a nucleoid-associated protein Ghosh, Soumitra; Mallick, Bratati; Nagaraja, Valakunja Nucleic Acids Research, Vol. 42, Issue 17 https://doi.org/10.1093/nar/gku804	journal	September 2014
Iron-Regulated Protein HupB of Mycobacterium tuberculosis Positively Regulates Siderophore Biosynthesis and Is Essential for Growth in Macrophages Pandey, Satya Deo; Choudhury, Mitali; Yousuf, Suhail Journal of Bacteriology, Vol. 196, Issue 10 https://doi.org/10.1128/JB.01483-13	journal	May 2014
Identification and Characterization of a Major Cell Wall-Associated Iron-Regulated Envelope Protein (Irep-28) in Mycobacterium tuberculosis Yeruva, Veena C.; Duggirala, Sridevi; Lakshmi, V. Clinical and Vaccine Immunology, Vol. 13, Issue 10 https://doi.org/10.1128/CVI.00125-06	journal	October 2006
Cloning and characterization of NAD-dependent protein deacetylase (Rv1151c) from Mycobacterium tuberculosis Gu, Jing; Deng, Jiao-Yu; Li, Ru Biochemistry (Moscow), Vol. 74, Issue 7 https://doi.org/10.1134/S0006297909070062	journal	July 2009
Reversible Acetylation and Inactivation of Mycobacterium tuberculosis Acetyl-CoA Synthetase Is Dependent on cAMP Xu, Hua; Hegde, Subray S.; Blanchard, John S. Biochemistry, Vol. 50, Issue 26 https://doi.org/10.1021/bi200156t	journal	July 2011
Acetylation of acetyl-CoA synthetase from Mycobacterium tuberculosis leads to specific inactivation of the adenylation reaction Noy, Tahel; Xu, Hua; Blanchard, John S. Archives of Biochemistry and Biophysics, Vol. 550-551 https://doi.org/10.1016/j.abb.2014.04.004	journal	May 2014
Mechanism and Regulation of Mycobactin Fatty Acyl-AMP Ligase FadD33 Vergnolle, Olivia; Xu, Hua; Blanchard, John S. Journal of Biological Chemistry, Vol. 288, Issue 39 https://doi.org/10.1074/jbc.M113.495549	journal	August 2013
The Interaction of Alba, a Conserved Archaeal Chromatin Protein, with Sir2 and Its Regulation by Acetylation Bell, S. D. Science, Vol. 296, Issue 5565 https://doi.org/10.1126/science.1070506	journal	April 2002
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
Effects of Altering Aminoglycoside Structures on Bacterial Resistance Enzyme Activities Green, Keith D.; Chen, Wenjing; Garneau-Tsodikova, Sylvie Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 7 https://doi.org/10.1128/AAC.00312-11	journal	May 2011
Domain dissection and characterization of the aminoglycoside resistance enzyme ANT(3″)-Ii/AAC(6′)-IId from Serratia marcescens Green, Keith D.; Garneau-Tsodikova, Sylvie Biochimie, Vol. 95, Issue 6 https://doi.org/10.1016/j.biochi.2013.02.011	journal	June 2013
Potent Inhibitors of Acetyltransferase Eis Overcome Kanamycin Resistance in Mycobacterium tuberculosis Willby, Melisa J.; Green, Keith D.; Gajadeera, Chathurada S. ACS Chemical Biology, Vol. 11, Issue 6 https://doi.org/10.1021/acschembio.6b00110	journal	April 2016
Identification and Characterization of Inhibitors of the Aminoglycoside Resistance Acetyltransferase Eis from Mycobacterium tuberculosis Green, Keith D.; Chen, Wenjing; Garneau-Tsodikova, Sylvie ChemMedChem, Vol. 7, Issue 1 https://doi.org/10.1002/cmdc.201100332	journal	September 2011
Discovery and Optimization of Two Eis Inhibitor Families as Kanamycin Adjuvants against Drug-Resistant M. tuberculosis Garzan, Atefeh; Willby, Melisa J.; Green, Keith D. ACS Medicinal Chemistry Letters, Vol. 7, Issue 12 https://doi.org/10.1021/acsmedchemlett.6b00261	journal	September 2016
Combating Enhanced Intracellular Survival (Eis)-Mediated Kanamycin Resistance of Mycobacterium tuberculosis by Novel Pyrrolo[1,5- a ]pyrazine-Based Eis Inhibitors Garzan, Atefeh; Willby, Melisa J.; Ngo, Huy X. ACS Infectious Diseases, Vol. 3, Issue 4 https://doi.org/10.1021/acsinfecdis.6b00193	journal	October 2016
Chemical and Structural Insights into the Regioversatility of the Aminoglycoside Acetyltransferase Eis Houghton, Jacob L.; Biswas, Tapan; Chen, Wenjing ChemBioChem, Vol. 14, Issue 16 https://doi.org/10.1002/cbic.201300359	journal	September 2013
[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
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
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Polder maps: improving OMIT maps by excluding bulk solvent Liebschner, Dorothee; Afonine, Pavel V.; Moriarty, Nigel W. Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 2, p. 148-157 https://doi.org/10.1107/S2059798316018210	journal	February 2017
Sulfonamide-Based Inhibitors of Aminoglycoside Acetyltransferase Eis Abolish Resistance to Kanamycin in Mycobacterium tuberculosis Garzan, Atefeh; Willby, Melisa J.; Green, Keith D. Journal of Medicinal Chemistry, Vol. 59, Issue 23 https://doi.org/10.1021/acs.jmedchem.6b01161	journal	November 2016
Aminoglycoside Multiacetylating Activity of the Enhanced Intracellular Survival Protein from Mycobacterium smegmatis and Its Inhibition Chen, Wenjing; Green, Keith D.; Tsodikov, Oleg V. Biochemistry, Vol. 51, Issue 24 https://doi.org/10.1021/bi3004473	journal	June 2012
Biochemical and structural analysis of aminoglycoside acetyltransferase Eis from Anabaena variabilis Pricer, Rachel E.; Houghton, Jacob L.; Green, Keith D. Molecular BioSystems, Vol. 8, Issue 12 https://doi.org/10.1039/c2mb25341k	journal	January 2012
Biochemical and Structural Analysis of an Eis Family Aminoglycoside Acetyltransferase from Bacillus anthracis Green, Keith D.; Biswas, Tapan; Chang, Changsoo Biochemistry, Vol. 54, Issue 20 https://doi.org/10.1021/acs.biochem.5b00244	journal	May 2015
Comparative Study of Eis-like Enzymes from Pathogenic and Nonpathogenic Bacteria Green, Keith D.; Pricer, Rachel E.; Stewart, Megan N. ACS Infectious Diseases, Vol. 1, Issue 6 https://doi.org/10.1021/acsinfecdis.5b00036	journal	May 2015
Unexpected N-acetylation of capreomycin by mycobacterial Eis enzymes Houghton, J. L.; Green, K. D.; Pricer, R. E. Journal of Antimicrobial Chemotherapy, Vol. 68, Issue 4 https://doi.org/10.1093/jac/dks497	journal	December 2012
Aminoglycoside-modifying enzymes Wright, Gerard D. Current Opinion in Microbiology, Vol. 2, Issue 5 https://doi.org/10.1016/S1369-5274(99)00007-7	journal	October 1999
A Bacterial Acetyltransferase Capable of Regioselective N-Acetylation of Antibiotics and Histones Vetting, Matthew W.; Magnet, Sophie; Nieves, Edward Chemistry & Biology, Vol. 11, Issue 4 https://doi.org/10.1016/j.chembiol.2004.03.017	journal	April 2004
Structure of Tetrahymena GCN5 bound to coenzyme A and a histone H3 peptide Rojas, Jeannie R.; Trievel, Raymond C.; Zhou, Jianxin Nature, Vol. 401, Issue 6748 https://doi.org/10.1038/43487	journal	September 1999
Structural Basis for Histone and Phosphohistone Binding by the GCN5 Histone Acetyltransferase Clements, Adrienne; Poux, Arienne N.; Lo, Wan-Sheng Molecular Cell, Vol. 12, Issue 2 https://doi.org/10.1016/S1097-2765(03)00288-0	journal	August 2003
Molecular Basis for Gcn5/PCAF Histone Acetyltransferase Selectivity for Histone and Nonhistone Substrates ^† ^, ^‡ Poux, Arienne N.; Marmorstein, Ronen Biochemistry, Vol. 42, Issue 49 https://doi.org/10.1021/bi035632n	journal	December 2003

Cited By (3)

Mechanisms, Detection, and Relevance of Protein Acetylation in Prokaryotes Christensen, D. G.; Baumgartner, J. T.; Xie, X. mBio, Vol. 10, Issue 2 https://doi.org/10.1128/mbio.02708-18	journal	April 2019
Mycobacterial Aminoglycoside Acetyltransferases: A Little of Drug Resistance, and a Lot of Other Roles Sanz-García, Fernando; Anoz-Carbonell, Ernesto; Pérez-Herrán, Esther Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00046	journal	January 2019
Post-translational Protein Acetylation: An Elegant Mechanism for Bacteria to Dynamically Regulate Metabolic Functions Christensen, David G.; Xie, Xueshu; Basisty, Nathan Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01604	journal	July 2019

Similar Records

Potent Inhibitors of Acetyltransferase Eis Overcome Kanamycin Resistance in Mycobacterium tuberculosis

Journal Article · Thu Mar 24 00:00:00 EDT 2016 · ACS Chemical Biology · OSTI ID:1424796

Willby, Melisa J.; Green, Keith D.; Gajadeera, Chathurada S.; +4 more

Potent 1,2,4-Triazino[5,6 b ]indole-3-thioether Inhibitors of the Kanamycin Resistance Enzyme Eis from Mycobacterium tuberculosis

Journal Article · Fri Mar 30 00:00:00 EDT 2018 · ACS Infectious Diseases · OSTI ID:1424796

Ngo, Huy X.; Green, Keith D.; Gajadeera, Chathurada S.; +8 more

Probing the Robustness of Inhibitors of Tuberculosis Aminoglycoside Resistance Enzyme Eis by Mutagenesis

Journal Article · Wed Aug 21 00:00:00 EDT 2019 · ACS Infectious Diseases · OSTI ID:1424796

Green, Keith D.; Punetha, Ankita; Hou, Caixia; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Title: Acetylation by Eis and Deacetylation by Rv1151c of Mycobacterium tuberculosis HupB: Biochemical and Structural Insight

Citation Formats

References (50)

Cited By (3)

Similar Records

Related Subjects