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Expression and Characterization of the Isolated Glycosyltransferase Module of Escherichia coli PBP1b
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    Expression and Characterization of the Isolated Glycosyltransferase Module of Escherichia coli PBP1b
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    Department of Chemistry, Princeton University, Princeton, New Jersey 08544
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    Biochemistry

    Cite this: Biochemistry 2004, 43, 38, 12375–12381
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    https://doi.org/10.1021/bi049142m
    Published September 3, 2004
    Copyright © 2004 American Chemical Society

    Abstract

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    The enzymes involved in the biosynthesis of peptidoglycan are targets for the development of new antibiotics. The bifunctional high molecular weight (HMW) penicillin-binding proteins (PBPs), which contain both glycosyltransferase (GTase) and transpeptidase (TPase) activities, are particularly attractive targets because of their extracellular location. However, there is limited mechanistic or structural information about the GTase modules of these enzymes. In this paper, we describe the overexpression and characterization of the GTase module of Escherichia coli PBP1b, a paradigm of the HMW PBPs. We define the C-terminal boundary of the GTase module and show that the isolated module can be overexpressed at significantly higher levels than the full-length protein. The catalytic efficiency and other characteristics of the isolated module are comparable in most respects to the full-length enzyme. This work lays the groundwork for mechanistic and structural analysis of GTase modules.

    Copyright © 2004 American Chemical Society

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     Financial support was provided by the National Institute of Health (NIH Grant R01AI50855).

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     To whom correspondence should be addressed. Phone:  (617) 432-5488. Fax:  (617) 496-0215. E-mail:  [email protected].

    Cited By

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    This article is cited by 31 publications.

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    5. Tsung-Shing Andrew Wang, Tania J. Lupoli, Yuto Sumida, Hirokazu Tsukamoto, Yihui Wu, Yuriy Rebets, Daniel E. Kahne, and Suzanne Walker . Primer Preactivation of Peptidoglycan Polymerases. Journal of the American Chemical Society 2011, 133 (22) , 8528-8530. https://doi.org/10.1021/ja2028712
    6. Peter Welzel. Syntheses around the Transglycosylation Step in Peptidoglycan Biosynthesis. Chemical Reviews 2005, 105 (12) , 4610-4660. https://doi.org/10.1021/cr040634e
    7. Suzanne Walker,, Lan Chen,, Yanan Hu,, Yosup Rew,, Dongwoo Shin, and, Dale L. Boger. Chemistry and Biology of Ramoplanin:  A Lipoglycodepsipeptide with Potent Antibiotic Activity. Chemical Reviews 2005, 105 (2) , 449-476. https://doi.org/10.1021/cr030106n
    8. Tse-Wei Hsu, Jim-Min Fang. Advances and prospects of analytic methods for bacterial transglycosylation and inhibitor discovery. The Analyst 2024, 149 (8) , 2204-2222. https://doi.org/10.1039/D3AN01968C
    9. Manuel Pazos, Katharina Peters. Peptidoglycan. 2019, 127-168. https://doi.org/10.1007/978-3-030-18768-2_5
    10. Nicola F. Galley, Amy M. O’Reilly, David I. Roper. Prospects for novel inhibitors of peptidoglycan transglycosylases. Bioorganic Chemistry 2014, 55 , 16-26. https://doi.org/10.1016/j.bioorg.2014.05.007
    11. Bart Blanchaert, Erwin Adams, Ann Van Schepdael. An overview of analytical methods for monitoring bacterial transglycosylation. Anal. Methods 2014, 6 (19) , 7590-7596. https://doi.org/10.1039/C4AY01299B
    12. Nordine Helassa, Waldemar Vollmer, Eefjan Breukink, Thierry Vernet, André Zapun. The membrane anchor of penicillin‐binding protein PBP2a from Streptococcus   pneumoniae influences peptidoglycan chain length. The FEBS Journal 2012, 279 (11) , 2071-2081. https://doi.org/10.1111/j.1742-4658.2012.08592.x
    13. Ankur Gautam, Rajan Vyas, Rupinder Tewari. Peptidoglycan biosynthesis machinery: A rich source of drug targets. Critical Reviews in Biotechnology 2011, 31 (4) , 295-336. https://doi.org/10.3109/07388551.2010.525498
    14. P. Macheboeuf, M. Piuzzi, S. Finet, F. Bontems, J. Pérez, A. Dessen, P. Vachette. Solution X-ray scattering study of a full-length class A penicillin-binding protein. Biochemical and Biophysical Research Communications 2011, 405 (1) , 107-111. https://doi.org/10.1016/j.bbrc.2011.01.003
    15. Julien Offant, Mohammed Terrak, Adeline Derouaux, Eefjan Breukink, Martine Nguyen‐Distèche, André Zapun, Thierry Vernet. Optimization of conditions for the glycosyltransferase activity of penicillin‐binding protein 1a from Thermotoga maritima. The FEBS Journal 2010, 277 (20) , 4290-4298. https://doi.org/10.1111/j.1742-4658.2010.07817.x
    16. Mohammed Terrak, Eric Sauvage, Adeline Derouaux, Dominique Dehareng, Ahmed Bouhss, Eefjan Breukink, Sylvie Jeanjean, Martine Nguyen-Distèche. Importance of the Conserved Residues in the Peptidoglycan Glycosyltransferase Module of the Class A Penicillin-binding Protein 1b of Escherichia coli. Journal of Biological Chemistry 2008, 283 (42) , 28464-28470. https://doi.org/10.1074/jbc.M803223200
    17. Waldemar Vollmer, Ute Bertsche. Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochimica et Biophysica Acta (BBA) - Biomembranes 2008, 1778 (9) , 1714-1734. https://doi.org/10.1016/j.bbamem.2007.06.007
    18. Eric Sauvage, Frédéric Kerff, Mohammed Terrak, Juan A. Ayala, Paulette Charlier. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiology Reviews 2008, 32 (2) , 234-258. https://doi.org/10.1111/j.1574-6976.2008.00105.x
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    20. Cynthia Ginsberg, Stephanie Brown, Suzanne Walker. Bacterial Cell Wall Components. 2008, 1535-1600. https://doi.org/10.1007/978-3-540-30429-6_38
    21. Jean van Heijenoort. Lipid Intermediates in the Biosynthesis of Bacterial Peptidoglycan. Microbiology and Molecular Biology Reviews 2007, 71 (4) , 620-635. https://doi.org/10.1128/MMBR.00016-07
    22. Andrew L. Lovering, Liza H. de Castro, Daniel Lim, Natalie C. J. Strynadka. Structural Insight into the Transglycosylation Step of Bacterial Cell-Wall Biosynthesis. Science 2007, 315 (5817) , 1402-1405. https://doi.org/10.1126/science.1136611
    23. Haitian Liu, Chi-Huey Wong. Characterization of a transglycosylase domain of Streptococcus pneumoniae PBP1b. Bioorganic & Medicinal Chemistry 2006, 14 (21) , 7187-7195. https://doi.org/10.1016/j.bmc.2006.06.058
    24. Petra Born, Eefjan Breukink, Waldemar Vollmer. In Vitro Synthesis of Cross-linked Murein and Its Attachment to Sacculi by PBP1A from Escherichia coli. Journal of Biological Chemistry 2006, 281 (37) , 26985-26993. https://doi.org/10.1074/jbc.M604083200
    25. Pauline Macheboeuf, Carlos Contreras-Martel, Viviana Job, Otto Dideberg, Andréa Dessen. Penicillin Binding Proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiology Reviews 2006, 30 (5) , 673-691. https://doi.org/10.1111/j.1574-6976.2006.00024.x
    26. Julien Offant, François Michoux, Annabelle Dermiaux, Jacques Biton, Yves Bourne. Functional characterization of the glycosyltransferase domain of penicillin-binding protein 1a from Thermotoga maritima. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2006, 1764 (6) , 1036-1042. https://doi.org/10.1016/j.bbapap.2006.03.012
    27. Wen Yi, Qingjia Yao, Yalong Zhang, Edwin Motari, Steven Lin, Peng George Wang. The wbnH gene of Escherichia coli O86:H2 encodes an α-1,3-N-acetylgalactosaminyl transferase involved in the O-repeating unit biosynthesis. Biochemical and Biophysical Research Communications 2006, 344 (2) , 631-639. https://doi.org/10.1016/j.bbrc.2006.03.181
    28. Mohammed Terrak, Martine Nguyen-Distèche. Kinetic Characterization of the Monofunctional Glycosyltransferase from Staphylococcus aureus. Journal of Bacteriology 2006, 188 (7) , 2528-2532. https://doi.org/10.1128/JB.188.7.2528-2532.2006
    29. Ute Bertsche, Eefjan Breukink, Thomas Kast, Waldemar Vollmer. In Vitro Murein (Peptidoglycan) Synthesis by Dimers of the Bifunctional Transglycosylase-Transpeptidase PBP1B from Escherichia coli. Journal of Biological Chemistry 2005, 280 (45) , 38096-38101. https://doi.org/10.1074/jbc.M508646200
    30. Bohdan Ostash, Suzanne Walker. Bacterial transglycosylase inhibitors. Current Opinion in Chemical Biology 2005, 9 (5) , 459-466. https://doi.org/10.1016/j.cbpa.2005.08.014
    31. Dianah Barrett, Catherine Leimkuhler, Lan Chen, Deborah Walker, Daniel Kahne, Suzanne Walker. Kinetic Characterization of the Glycosyltransferase Module of Staphylococcus aureus PBP2. Journal of Bacteriology 2005, 187 (6) , 2215-2217. https://doi.org/10.1128/JB.187.6.2215-2217.2005

    Biochemistry

    Cite this: Biochemistry 2004, 43, 38, 12375–12381
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bi049142m
    Published September 3, 2004
    Copyright © 2004 American Chemical Society

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