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Title: Conservation of the structure and function of bacterial tryptophan synthases

Abstract

Tryptophan biosynthesis is one of the most characterized processes in bacteria, in which the enzymes from Salmonella typhimuriumand Escherichia coliserve as model systems. Tryptophan synthase (TrpAB) catalyzes the final two steps of tryptophan biosynthesis in plants, fungi and bacteria. This pyridoxal 5'-phosphate (PLP)-dependent enzyme consists of two protein chains, α (TrpA) and β (TrpB), functioning as a linear αββα heterotetrameric complex containing two TrpAB units. The reaction has a complicated, multistep mechanism resulting in the β-replacement of the hydroxyl group of L-serine with an indole moiety. Recent studies have shown that functional TrpAB is required for the survival of pathogenic bacteria in macrophages and for evading host defense. Therefore, TrpAB is a promising target for drug discovery, as its orthologs include enzymes from the important human pathogens Streptococcus pneumoniae, Legionella pneumophilaand Francisella tularensis, the causative agents of pneumonia, legionnaires' disease and tularemia, respectively. However, specific biochemical and structural properties of the TrpABs from these organisms have not been investigated. To fill the important phylogenetic gaps in the understanding of TrpABs and to uncover unique features of TrpAB orthologs to spearhead future drug-discovery efforts, the TrpABs from L. pneumophila, F. tularensisand S. pneumoniaehave been characterized. In addition to kinetic properties andmore » inhibitor-sensitivity data, structural information gathered using X-ray crystallography is presented. The enzymes show remarkable structural conservation, but at the same time display local differences in both their catalytic and allosteric sites that may be responsible for the observed differences in catalysis and inhibitor binding. This functional dissimilarity may be exploited in the design of species-specific enzyme inhibitors.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [1];  [4];  [1];  [2];  [3];  [2];  [1]; ORCiD logo [2];  [2];  [2];  [2];  [3];  [5]
  1. Univ. of Chicago, IL (United States). Center for Structural Genomics of Infectious Diseases; Argonne National Lab. (ANL), Argonne, IL (United States). Bioscience Division
  2. Broad Institute of MIT and Harvard, Cambridge, MA (United States)
  3. Argonne National Lab. (ANL), Argonne, IL (United States). Bioscience Division
  4. Univ. of Chicago, IL (United States). Center for Structural Genomics of Infectious Diseases
  5. Univ. of Chicago, IL (United States). Center for Structural Genomics of Infectious Diseases, and Dept. of Biochemistry and Molecular Biology; Argonne National Lab. (ANL), Argonne, IL (United States). Bioscience Division
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1560154
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
IUCrJ
Additional Journal Information:
Journal Volume: 6; Journal Issue: 4; Journal ID: ISSN 2052-2525
Publisher:
International Union of Crystallography
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Francisella tularensis; Legionella pneumophila; Streptococcus pneumoniae; X-ray crystallography; allosteric regulation; catalysis; crystal structure; drug discovery; enzyme inhibitors; enzyme mechanisms; molecular recognition; protein structure; structure determination; tryptophan; tryptophan synthase

Citation Formats

Michalska, Karolina, Gale, Jennifer, Joachimiak, Grazyna, Chang, Changsoo, Hatzos-Skintges, Catherine, Nocek, Boguslaw, Johnston, Stephen E., Bigelow, Lance, Bajrami, Besnik, Jedrzejczak, Robert P., Wellington, Samantha, Hung, Deborah T., Nag, Partha P., Fisher, Stewart L., Endres, Michael, and Joachimiak, Andrzej. Conservation of the structure and function of bacterial tryptophan synthases. United States: N. p., 2019. Web. doi:10.1107/S2052252519005955.
Michalska, Karolina, Gale, Jennifer, Joachimiak, Grazyna, Chang, Changsoo, Hatzos-Skintges, Catherine, Nocek, Boguslaw, Johnston, Stephen E., Bigelow, Lance, Bajrami, Besnik, Jedrzejczak, Robert P., Wellington, Samantha, Hung, Deborah T., Nag, Partha P., Fisher, Stewart L., Endres, Michael, & Joachimiak, Andrzej. Conservation of the structure and function of bacterial tryptophan synthases. United States. doi:10.1107/S2052252519005955.
Michalska, Karolina, Gale, Jennifer, Joachimiak, Grazyna, Chang, Changsoo, Hatzos-Skintges, Catherine, Nocek, Boguslaw, Johnston, Stephen E., Bigelow, Lance, Bajrami, Besnik, Jedrzejczak, Robert P., Wellington, Samantha, Hung, Deborah T., Nag, Partha P., Fisher, Stewart L., Endres, Michael, and Joachimiak, Andrzej. Wed . "Conservation of the structure and function of bacterial tryptophan synthases". United States. doi:10.1107/S2052252519005955. https://www.osti.gov/servlets/purl/1560154.
@article{osti_1560154,
title = {Conservation of the structure and function of bacterial tryptophan synthases},
author = {Michalska, Karolina and Gale, Jennifer and Joachimiak, Grazyna and Chang, Changsoo and Hatzos-Skintges, Catherine and Nocek, Boguslaw and Johnston, Stephen E. and Bigelow, Lance and Bajrami, Besnik and Jedrzejczak, Robert P. and Wellington, Samantha and Hung, Deborah T. and Nag, Partha P. and Fisher, Stewart L. and Endres, Michael and Joachimiak, Andrzej},
abstractNote = {Tryptophan biosynthesis is one of the most characterized processes in bacteria, in which the enzymes fromSalmonella typhimuriumandEscherichia coliserve as model systems. Tryptophan synthase (TrpAB) catalyzes the final two steps of tryptophan biosynthesis in plants, fungi and bacteria. This pyridoxal 5'-phosphate (PLP)-dependent enzyme consists of two protein chains, α (TrpA) and β (TrpB), functioning as a linear αββα heterotetrameric complex containing two TrpAB units. The reaction has a complicated, multistep mechanism resulting in the β-replacement of the hydroxyl group of L-serine with an indole moiety. Recent studies have shown that functional TrpAB is required for the survival of pathogenic bacteria in macrophages and for evading host defense. Therefore, TrpAB is a promising target for drug discovery, as its orthologs include enzymes from the important human pathogensStreptococcus pneumoniae,Legionella pneumophilaandFrancisella tularensis, the causative agents of pneumonia, legionnaires' disease and tularemia, respectively. However, specific biochemical and structural properties of the TrpABs from these organisms have not been investigated. To fill the important phylogenetic gaps in the understanding of TrpABs and to uncover unique features of TrpAB orthologs to spearhead future drug-discovery efforts, the TrpABs fromL. pneumophila,F. tularensisandS. pneumoniaehave been characterized. In addition to kinetic properties and inhibitor-sensitivity data, structural information gathered using X-ray crystallography is presented. The enzymes show remarkable structural conservation, but at the same time display local differences in both their catalytic and allosteric sites that may be responsible for the observed differences in catalysis and inhibitor binding. This functional dissimilarity may be exploited in the design of species-specific enzyme inhibitors.},
doi = {10.1107/S2052252519005955},
journal = {IUCrJ},
number = 4,
volume = 6,
place = {United States},
year = {2019},
month = {5}
}

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    journal, June 2006

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    • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1764, Issue 6
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    • Rowlett, Roger; Yang, Li-Hong; Ahmed, S. Ashraf
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    • Niks, Dimitri; Hilario, Eduardo; Dierkers, Adam
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    • Cellular and Molecular Life Sciences, Vol. 66, Issue 14
    • DOI: 10.1007/s00018-009-0028-0

    Directed evolution of the tryptophan synthase β-subunit for stand-alone function recapitulates allosteric activation
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    The crystal structure of the tryptophan synthase β2 subunit from the hyperthermophile Pyrococcus furiosus: Investigation of stabilization factors
    journal, June 2004


    Beg, Borrow and Steal: Three Aspects of Horizontal Gene Transfer in the Protozoan Parasite, Cryptosporidium parvum
    journal, March 2016


    Allosteric regulation of substrate channeling and catalysis in the tryptophan synthase bienzyme complex
    journal, March 2012


    High-throughput protein purification and quality assessment for crystallization
    journal, September 2011


    βQ114N and βT110V Mutations Reveal a Critically Important Role of the Substrate α-Carboxylate Site in the Reaction Specificity of Tryptophan Synthase
    journal, December 2007

    • Blumenstein, Lars; Domratcheva, Tatiana; Niks, Dimitri
    • Biochemistry, Vol. 46, Issue 49
    • DOI: 10.1021/bi7008568

    Linking Crystallographic Model and Data Quality
    journal, May 2012


    Crystal Structure of Wild-Type Tryptophan Synthase Complexed with the Natural Substrate Indole-3-glycerol Phosphate
    journal, December 1999

    • Weyand, Michael; Schlichting, Ilme
    • Biochemistry, Vol. 38, Issue 50
    • DOI: 10.1021/bi9920533

    Crystallographic Studies of Phosphonate-Based α-Reaction Transition-State Analogues Complexed to Tryptophan Synthase ,
    journal, September 1999

    • Sachpatzidis, Aristidis; Dealwis, Chris; Lubetsky, Jodi B.
    • Biochemistry, Vol. 38, Issue 39
    • DOI: 10.1021/bi9907734

    Cleavable C-terminal His-tag vectors for structure determination
    journal, March 2010

    • Eschenfeldt, William H.; Maltseva, Natalia; Stols, Lucy
    • Journal of Structural and Functional Genomics, Vol. 11, Issue 1
    • DOI: 10.1007/s10969-010-9082-y

    Visualizing the tunnel in tryptophan synthase with crystallography: Insights into a selective filter for accommodating indole and rejecting water
    journal, March 2016

    • Hilario, Eduardo; Caulkins, Bethany G.; Huang, Yu-Ming M.
    • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1864, Issue 3
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