Studies of a Ring-Cleaving Dioxygenase Illuminate the Role of Cholesterol Metabolism in the Pathogenesis of Mycobacterium tuberculosis

Yam, Katherine C.; D'Angelo, Igor; Kalscheuer, Rainer; Zhu, Haizhong; Wang, Jian-Xin; Snieckus, Victor; Ly, Lan H.; Converse, Paul J.; Jacobs, William R.; Strynadka, Natalie; Eltis, Lindsay D.

doi:10.1371/journal.ppat.1000344

Title: Studies of a Ring-Cleaving Dioxygenase Illuminate the Role of Cholesterol Metabolism in the Pathogenesis of Mycobacterium tuberculosis

Journal Article · Fri Mar 20 00:00:00 UTC 2009 · PLoS Pathogens

DOI: https://doi.org/10.1371/journal.ppat.1000344 · OSTI ID:1627891

Yam, Katherine C. ^[1]; D'Angelo, Igor ^[2]; Kalscheuer, Rainer ^[3]; Zhu, Haizhong ^[2]; Wang, Jian-Xin ^[4]; Snieckus, Victor ^[4]; Ly, Lan H. ^[5]; Converse, Paul J. ^[6]; Jacobs, William R. ^[3]; Strynadka, Natalie ^[2]; Eltis, Lindsay D. ^[7]

Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology; DOE/OSTI
Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology
Albert Einstein College of Medicine, Bronx, NY (United States). Howard Hughes Medical Inst.
Queen's Univ., Kingston, ON (Canada). Dept. of Chemistry
Texas A & M Univ., College Station, TX (United States). Health Science Center. Dept. of Microbial and Molecular Pathogenesis
Johns Hopkins Univ., Baltimore, MD (United States). Dept. of Medicine. Center for Tuberculosis Research
Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Biochemistry and Molecular Biology; Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Microbiology and Immunology

Mycobacterium tuberculosis, the etiological agent of TB, possesses a cholesterol catabolic pathway implicated in pathogenesis. This pathway includes an iron-dependent extradiol dioxygenase, HsaC, that cleaves catechols. Immunocompromised mice infected with a DhsaC mutant of M. tuberculosis H37Rv survived 50% longer than mice infected with the wild-type strain. In guinea pigs, the mutant disseminated more slowly to the spleen, persisted less successfully in the lung, and caused little pathology. These data establish that, while cholesterol metabolism by M. tuberculosis appears to be most important during the chronic stage of infection, it begins much earlier and may contribute to the pathogen’s dissemination within the host. Purified HsaC efficiently cleaved the catecholic cholesterol metabolite, DHSA (3,4-dihydroxy-9,10- seconandrost-1,3,5(10)-triene-9,17-dione; kcat/Km = 14.460.5 mM^-1 s^-1), and was inactivated by a halogenated substrate analogue (partition coefficient,50). Remarkably, cholesterol caused loss of viability in the DhsaC mutant, consistent with catechol toxicity. Structures of HsaC:DHSA binary complexes at 2.1 A revealed two catechol-binding modes: bidentate binding to the active site iron, as has been reported in similar enzymes, and, unexpectedly, monodentate binding. The position of the bicyclo-alkanone moiety of DHSA was very similar in the two binding modes, suggesting that this interaction is a determinant in the initial substrate-binding event. These data provide insights into the binding of catechols by extradiol dioxygenases and facilitate inhibitor design.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1627891

Journal Information:: PLoS Pathogens, Journal Name: PLoS Pathogens Journal Issue: 3 Vol. 5; ISSN 1553-7374

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Metagenomes Reveal Global Distribution of Bacterial Steroid Catabolism in Natural, Engineered, and Host Environments Holert, Johannes; Cardenas, Erick; Bergstrand, Lee H. mBio, Vol. 9, Issue 1 https://doi.org/10.1128/mbio.02345-17	journal	January 2018
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Characterization of Phosphofructokinase Activity in Mycobacterium tuberculosis Reveals That a Functional Glycolytic Carbon Flow Is Necessary to Limit the Accumulation of Toxic Metabolic Intermediates under Hypoxia Phong, Wai Yee; Lin, Wenwei; Rao, Srinivasa P. S. PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056037	journal	February 2013
Correction: A Novel Role of the PrpR as a Transcription Factor Involved in the Regulation of Methylcitrate Pathway in Mycobacterium tuberculosis Masiewicz, Paweł; Brzostek, Anna; Wolański, Marcin PLOS ONE, Vol. 13, Issue 12 https://doi.org/10.1371/journal.pone.0208565	journal	December 2018
An Anaerobic-Type α-Ketoglutarate Ferredoxin Oxidoreductase Completes the Oxidative Tricarboxylic Acid Cycle of Mycobacterium tuberculosis Baughn, Anthony D.; Garforth, Scott J.; Vilchèze, Catherine PLoS Pathogens, Vol. 5, Issue 11 https://doi.org/10.1371/journal.ppat.1000662	journal	November 2009
The Steroid Catabolic Pathway of the Intracellular Pathogen Rhodococcus equi Is Important for Pathogenesis and a Target for Vaccine Development van der Geize, R.; Grommen, A. W. F.; Hessels, G. I. PLoS Pathogens, Vol. 7, Issue 8 https://doi.org/10.1371/journal.ppat.1002181	journal	August 2011
High-Resolution Phenotypic Profiling Defines Genes Essential for Mycobacterial Growth and Cholesterol Catabolism Griffin, Jennifer E.; Gawronski, Jeffrey D.; DeJesus, Michael A. PLoS Pathogens, Vol. 7, Issue 9 https://doi.org/10.1371/journal.ppat.1002251	journal	September 2011
Linking the Transcriptional Profiles and the Physiological States of Mycobacterium tuberculosis during an Extended Intracellular Infection Rohde, Kyle H.; Veiga, Diogo F. T.; Caldwell, Shannon PLoS Pathogens, Vol. 8, Issue 6 https://doi.org/10.1371/journal.ppat.1002769	journal	June 2012
Steroids as Environmental Compounds Recalcitrant to Degradation: Genetic Mechanisms of Bacterial Biodegradation Pathways Olivera, Elías R.; Luengo, José M. Genes, Vol. 10, Issue 7 https://doi.org/10.3390/genes10070512	journal	July 2019
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Bacterial degradation of bile salts Philipp, Bodo Applied Microbiology and Biotechnology, Vol. 89, Issue 4 https://doi.org/10.1007/s00253-010-2998-0	journal	November 2010
Genome-wide bioinformatics analysis of steroid metabolism-associated genes in Nocardioides simplex VKM Ac-2033D Shtratnikova, Victoria Y.; Schelkunov, Mikhail I.; Fokina, Victoria V. Current Genetics, Vol. 62, Issue 3 https://doi.org/10.1007/s00294-016-0568-4	journal	February 2016
Cyclic di-GMP regulates Mycobacterium tuberculosis resistance to ethionamide Zhang, Hai-Nan; Xu, Zhao-Wei; Jiang, He-Wei Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-06289-7	journal	July 2017
Identification of Comamonas testosteroni as an androgen degrader in sewage Chen, Yi-Lung; Wang, Chia-Hsiang; Yang, Fu-Chun Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35386	journal	October 2016
Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis Kalscheuer, R.; Weinrick, B.; Veeraraghavan, U. Proceedings of the National Academy of Sciences, Vol. 107, Issue 50 https://doi.org/10.1073/pnas.1014642108	journal	November 2010
Cholesterol Ester Oxidation by Mycobacterial Cytochrome P450 Frank, Daniel J.; Madrona, Yarrow; Ortiz de Montellano, Paul R. Journal of Biological Chemistry, Vol. 289, Issue 44 https://doi.org/10.1074/jbc.M114.602771	journal	October 2014
Structural and Functional Characterization of a Ketosteroid Transcriptional Regulator of Mycobacterium tuberculosis Crowe, Adam M.; Stogios, Peter J.; Casabon, Israël Journal of Biological Chemistry, Vol. 290, Issue 2 https://doi.org/10.1074/jbc.M114.607481	journal	January 2015
Characterization of a Carbon-Carbon Hydrolase from Mycobacterium tuberculosis Involved in Cholesterol Metabolism Lack, Nathan A.; Yam, Katherine C.; Lowe, Edward D. Journal of Biological Chemistry, Vol. 285, Issue 1 https://doi.org/10.1074/jbc.m109.058081	journal	January 2010
Mycobacterial Cytochrome P450 125 (Cyp125) Catalyzes the Terminal Hydroxylation of C27 Steroids Capyk, Jenna K.; Kalscheuer, Rainer; Stewart, Gordon R. Journal of Biological Chemistry, Vol. 284, Issue 51 https://doi.org/10.1074/jbc.m109.072132	journal	December 2009
A Flavin-dependent Monooxygenase from Mycobacterium tuberculosis Involved in Cholesterol Catabolism Dresen, Carola; Lin, Leo Y. -C.; D'Angelo, Igor Journal of Biological Chemistry, Vol. 285, Issue 29 https://doi.org/10.1074/jbc.m109.099028	journal	July 2010
Activity of 3-Ketosteroid 9α-Hydroxylase (KshAB) Indicates Cholesterol Side Chain and Ring Degradation Occur Simultaneously in Mycobacterium tuberculosis Capyk, Jenna K.; Casabon, Israël; Gruninger, Robert Journal of Biological Chemistry, Vol. 286, Issue 47 https://doi.org/10.1074/jbc.m111.289975	journal	November 2011
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Deciphering the Transcriptional Regulation of Cholesterol Catabolic Pathway in Mycobacteria García-Fernández, Esther; Medrano, Francisco Javier; Galán, Beatriz Journal of Biological Chemistry, Vol. 289, Issue 25 https://doi.org/10.1074/jbc.m113.545715	journal	June 2014
Central Role of Pyruvate Kinase in Carbon Co-catabolism of Mycobacterium tuberculosis Noy, Tahel; Vergnolle, Olivia; Hartman, Travis E. Journal of Biological Chemistry, Vol. 291, Issue 13 https://doi.org/10.1074/jbc.m115.707430	journal	March 2016
The Structure of the Transcriptional Repressor KstR in Complex with CoA Thioester Cholesterol Metabolites Sheds Light on the Regulation of Cholesterol Catabolism in Mycobacterium tuberculosis Ho, Ngoc Anh Thu; Dawes, Stephanie S.; Crowe, Adam M. Journal of Biological Chemistry, Vol. 291, Issue 14 https://doi.org/10.1074/jbc.m115.707760	journal	April 2016
From Lipid Transport to Oxygenation of Aromatic Compounds: Evolution within the Bet v1-like Superfamily Chakraborty, Joydeep; Dutta, Tapan K. Journal of Biomolecular Structure and Dynamics, Vol. 29, Issue 1 https://doi.org/10.1080/07391102.2011.10507375	journal	August 2011
Cholesterol utilization in mycobacteria is controlled by two TetR-type transcriptional regulators: kstR and kstR2 Kendall, Sharon L.; Burgess, Philippa; Balhana, Ricardo Microbiology, Vol. 156, Issue 5 https://doi.org/10.1099/mic.0.034538-0	journal	May 2010
Characterization of the KstR-dependent promoter of the gene for the first step of the cholesterol degradative pathway in Mycobacterium smegmatis Uhía, Iria; Galán, Beatriz; Medrano, Francisco Javier Microbiology, Vol. 157, Issue 9 https://doi.org/10.1099/mic.0.049213-0	journal	September 2011
Rv3723/LucA coordinates fatty acid and cholesterol uptake in Mycobacterium tuberculosis Nazarova, Evgeniya V.; Montague, Christine R.; La, Thuy eLife https://doi.org/10.1101/121780	posted_content	March 2017
Unravelling a new catabolic pathway of C-19 steroids in Mycobacterium smegmatis: C-19 steroids in M. smegmatis Fernández-Cabezón, Lorena; Galán, Beatriz; García, José L. Environmental Microbiology, Vol. 20, Issue 5 https://doi.org/10.1111/1462-2920.14114	journal	April 2018
Microbial degradation of steroid sex hormones: implications for environmental and ecological studies Chiang, Yin‐Ru; Wei, Sean Ting‐Shyang; Wang, Po‐Hsiang Microbial Biotechnology, Vol. 13, Issue 4 https://doi.org/10.1111/1751-7915.13504	journal	October 2019
Arylamine N‐acetyltransferases: from drug metabolism and pharmacogenetics to drug discovery Sim, E.; Abuhammad, A.; Ryan, A. British Journal of Pharmacology, Vol. 171, Issue 11 https://doi.org/10.1111/bph.12598	journal	May 2014
Investigation of the mycobacterial enzyme HsaD as a potential novel target for anti-tubercular agents using a fragment-based drug design approach: HsaD: a potential target for antitubercular agents Ryan, Ali; Polycarpou, Elena; Lack, Nathan A. British Journal of Pharmacology, Vol. 174, Issue 14 https://doi.org/10.1111/bph.13810	journal	May 2017
3-Ketosteroid 9Î±-hydroxylase is an essential factor in the pathogenesis of Mycobacterium tuberculosis Hu, Yanmin; van der Geize, Robert; Besra, Gurdyal S. Molecular Microbiology, Vol. 75, Issue 1 https://doi.org/10.1111/j.1365-2958.2009.06957.x	journal	January 2010
Mycobacterium tuberculosis CYP125A1, a steroid C27 monooxygenase that detoxifies intracellularly generated cholest-4-en-3-one: CYP125A1 in cholesterol metabolism Ouellet, Hugues; Guan, Shenheng; Johnston, Jonathan B. Molecular Microbiology, Vol. 77, Issue 3 https://doi.org/10.1111/j.1365-2958.2010.07243.x	journal	June 2010
Cholesterol oxidase: physiological functions: Cholesterol oxidase and membranes Kreit, Joseph; Sampson, Nicole S. FEBS Journal, Vol. 276, Issue 23 https://doi.org/10.1111/j.1742-4658.2009.07378.x	journal	October 2009
Catabolism and biotechnological applications of cholesterol degrading bacteria: Cholesterol degradation García, J. L.; Uhía, I.; Galán, B. Microbial Biotechnology, Vol. 5, Issue 6 https://doi.org/10.1111/j.1751-7915.2012.00331.x	journal	February 2012
FadD3 is an acyl-CoA synthetase that initiates catabolism of cholesterol rings C and D in actinobacteria: Role of FadD3 in cholesterol catabolism Casabon, Israël; Crowe, Adam M.; Liu, Jie Molecular Microbiology, Vol. 87, Issue 2 https://doi.org/10.1111/mmi.12095	journal	December 2012
Regulation of the KstR2 regulon of Mycobacterium tuberculosis by a cholesterol catabolite: KstR2 regulation in Mycobacterium tuberculosis Casabon, Israël; Zhu, Song-Hua; Otani, Hiroshi Molecular Microbiology, Vol. 89, Issue 6 https://doi.org/10.1111/mmi.12340	journal	August 2013
Acyldepsipeptide antibiotics kill mycobacteria by preventing the physiological functions of the ClpP1P2 protease: ADEPs target ClpP1P2 of M. tuberculosis Famulla, Kirsten; Sass, Peter; Malik, Imran Molecular Microbiology, Vol. 101, Issue 2 https://doi.org/10.1111/mmi.13362	journal	April 2016
The Nitrogen Regulator GlnR Directly Controls Transcription of the prpDBC Operon Involved in Methylcitrate Cycle in Mycobacterium smegmatis Liu, Wei-Bing; Liu, Xin-Xin; Shen, Meng-Jia Journal of Bacteriology, Vol. 201, Issue 8 https://doi.org/10.1128/jb.00099-19	journal	April 2019
Mycobacterium tuberculosis Cholesterol Catabolism Requires a New Class of Acyl Coenzyme A Dehydrogenase Voskuil, Martin I. Journal of Bacteriology, Vol. 195, Issue 19 https://doi.org/10.1128/jb.00867-13	journal	October 2013
Actinobacterial Acyl Coenzyme A Synthetases Involved in Steroid Side-Chain Catabolism Casabon, Israël; Swain, Kendra; Crowe, Adam M. Journal of Bacteriology, Vol. 196, Issue 3 https://doi.org/10.1128/jb.01012-13	journal	February 2014
Cholesterol Is Not an Essential Source of Nutrition for Mycobacterium tuberculosis during Infection Yang, Xinxin; Gao, Jin; Smith, Issar Journal of Bacteriology, Vol. 193, Issue 6 https://doi.org/10.1128/jb.01210-10	journal	March 2011
Metagenomes Reveal Global Distribution of Bacterial Steroid Catabolism in Natural, Engineered, and Host Environments Holert, Johannes; Cardenas, Erick; Bergstrand, Lee H. mBio, Vol. 9, Issue 1 https://doi.org/10.1128/mbio.02345-17	journal	January 2018
Microbial Functional Responses to Cholesterol Catabolism in Denitrifying Sludge Wei, Sean Ting-Shyang; Wu, Yu-Wei; Lee, Tzong-Huei mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/msystems.00113-18	journal	October 2018
Adventures in Rhodococcus — from steroids to explosivesThis article is based on a presentation by Dr. Lindsay Eltis at the 60th Annual Meeting of the Canadian Society of Microbiologists in Hamilton, Ontario, 14 June 2010. Dr. Eltis was the recipient of the 2010 Norgen Biotek Corporation / CSM Award, an annual award sponsored by Norgen Biotek and the Canadian Society of Microbiologists intended to recognize outstanding scientific work in microbiology by a Canadian researcher. Yam, Katherine C.; Okamoto, Sachi; Roberts, Joseph N. Canadian Journal of Microbiology, Vol. 57, Issue 3 https://doi.org/10.1139/w10-115	journal	March 2011
Mycobacterium tuberculosis Requires Cholesterol Oxidase to Disrupt TLR2 Signalling in Human Macrophages Szulc-Kielbik, Izabela; Kielbik, Michal; Przygodzka, Patrycja Mediators of Inflammation, Vol. 2019 https://doi.org/10.1155/2019/2373791	journal	December 2019
Comprehensive insights into transcriptional adaptation of intracellular mycobacteria by microbe-enriched dual RNA sequencing Rienksma, Rienk A.; Suarez-Diez, Maria; Mollenkopf, Hans-Joachim BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-014-1197-2	journal	January 2015
Transposon libraries identify novel Mycobacterium bovis BCG genes involved in the dynamic interactions required for BCG to persist during in vivo passage in cattle Mendum, Tom A.; Chandran, Aneesh; Williams, Kerstin BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5791-1	journal	May 2019
Piperidinols That Show Anti-Tubercular Activity as Inhibitors of Arylamine N-Acetyltransferase: An Essential Enzyme for Mycobacterial Survival Inside Macrophages Abuhammad, Areej; Fullam, Elizabeth; Lowe, Edward D. PLoS ONE, Vol. 7, Issue 12 https://doi.org/10.1371/journal.pone.0052790	journal	December 2012
Characterization of Phosphofructokinase Activity in Mycobacterium tuberculosis Reveals That a Functional Glycolytic Carbon Flow Is Necessary to Limit the Accumulation of Toxic Metabolic Intermediates under Hypoxia Phong, Wai Yee; Lin, Wenwei; Rao, Srinivasa P. S. PLoS ONE, Vol. 8, Issue 2 https://doi.org/10.1371/journal.pone.0056037	journal	February 2013
An Anaerobic-Type α-Ketoglutarate Ferredoxin Oxidoreductase Completes the Oxidative Tricarboxylic Acid Cycle of Mycobacterium tuberculosis Baughn, Anthony D.; Garforth, Scott J.; Vilchèze, Catherine PLoS Pathogens, Vol. 5, Issue 11 https://doi.org/10.1371/journal.ppat.1000662	journal	November 2009
High-Resolution Phenotypic Profiling Defines Genes Essential for Mycobacterial Growth and Cholesterol Catabolism Griffin, Jennifer E.; Gawronski, Jeffrey D.; DeJesus, Michael A. PLoS Pathogens, Vol. 7, Issue 9 https://doi.org/10.1371/journal.ppat.1002251	journal	September 2011
Linking the Transcriptional Profiles and the Physiological States of Mycobacterium tuberculosis during an Extended Intracellular Infection Rohde, Kyle H.; Veiga, Diogo F. T.; Caldwell, Shannon PLoS Pathogens, Vol. 8, Issue 6 https://doi.org/10.1371/journal.ppat.1002769	journal	June 2012
Novel Inhibitors of Cholesterol Degradation in Mycobacterium tuberculosis Reveal How the Bacterium’s Metabolism Is Constrained by the Intracellular Environment VanderVen, Brian C.; Fahey, Ruth J.; Lee, Wonsik PLOS Pathogens, Vol. 11, Issue 2 https://doi.org/10.1371/journal.ppat.1004679	journal	February 2015
Pathogen roid rage: Cholesterol utilization by Mycobacterium tuberculosis Wipperman, Matthew F.; Sampson, Nicole S.; Thomas, Suzanne T. Critical Reviews in Biochemistry and Molecular Biology, Vol. 49, Issue 4 https://doi.org/10.3109/10409238.2014.895700	journal	March 2014
Steroids as Environmental Compounds Recalcitrant to Degradation: Genetic Mechanisms of Bacterial Biodegradation Pathways Olivera, Elías R.; Luengo, José M. Genes, Vol. 10, Issue 7 https://doi.org/10.3390/genes10070512	journal	July 2019
Exploration of Piperidinols as Potential Antitubercular Agents Abuhammad, Areej; Fullam, Elizabeth; Bhakta, Sanjib Molecules, Vol. 19, Issue 10 https://doi.org/10.3390/molecules191016274	journal	October 2014
Virulence factors of the Mycobacterium tuberculosis complex Forrellad, Marina A.; Klepp, Laura I.; Gioffré, Andrea Virulence, Vol. 4, Issue 1 https://doi.org/10.4161/viru.22329	journal	January 2013
Rv3723/LucA coordinates fatty acid and cholesterol uptake in Mycobacterium tuberculosis Nazarova, Evgeniya V.; Montague, Christine R.; La, Thuy eLife, Vol. 6 https://doi.org/10.7554/elife.26969	journal	June 2017

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