Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic

Lewandowski, Eric M.; Skiba, Joanna; Torelli, Nicholas J.; Rajnisz, Aleksandra; Solecka, Jolanta; Kowalski, Konrad; Chen, Yu

doi:10.1039/C5CC00904A

Title: Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic

Abstract

We have determined a 1.18 Å resolution X-ray crystal structure of a novel ruthenocenyle-6-aminopenicillinic acid in complex with CTX-M β-lactamase, showing unprecedented details of interactions between ruthenocene and protein. As the first product complex with an intact catalytic serine, the structure also offers insights into β-lactamase catalysis and inhibitor design.

Authors:

Lewandowski, Eric M. ^[1]; Skiba, Joanna ^[2]; Torelli, Nicholas J. ^[1]; Rajnisz, Aleksandra ^[3]; Solecka, Jolanta ^[3]; Kowalski, Konrad ^[2]; Chen, Yu ^[1]

Univ. of South Florida, Tampa, FL (United States). Dept. of PMolecular Medicine
Univ. of Lodz (Poland). Dept. of Organic Chemistry
National Inst. of Public Health - National Inst. of Hygiene (NIPH-NIH), Warsaw (Poland)

Publication Date:: Mon Mar 02 00:00:00 EST 2015

Research Org.:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Org.:: National Institutes of Health (NIH); USDOE

OSTI Identifier:: 1178850

Grant/Contract Number:: W-31-109-Eng-38; DEC-2013/11/B/ST5/00997

Resource Type:: Accepted Manuscript

Journal Name:: ChemComm

Additional Journal Information:: Journal Volume: 51; Journal Issue: 28; Journal ID: ISSN 1359-7345

Publisher:: Royal Society of Chemistry

Country of Publication:: United States

Language:: ENGLISH

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats


                    Lewandowski, Eric M., Skiba, Joanna, Torelli, Nicholas J., Rajnisz, Aleksandra, Solecka, Jolanta, Kowalski, Konrad, and Chen, Yu. Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic.  United States: N. p., 2015. 
Web.  doi:10.1039/C5CC00904A.

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                    Lewandowski, Eric M., Skiba, Joanna, Torelli, Nicholas J., Rajnisz, Aleksandra, Solecka, Jolanta, Kowalski, Konrad, & Chen, Yu. Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic.  United States.  https://doi.org/10.1039/C5CC00904A

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                    Lewandowski, Eric M., Skiba, Joanna, Torelli, Nicholas J., Rajnisz, Aleksandra, Solecka, Jolanta, Kowalski, Konrad, and Chen, Yu. Mon .  
"Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic".  United States.  https://doi.org/10.1039/C5CC00904A.  https://www.osti.gov/servlets/purl/1178850.

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@article{osti_1178850,

  title        = {Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic},

  author       = {Lewandowski, Eric M. and Skiba, Joanna and Torelli, Nicholas J. and Rajnisz, Aleksandra and Solecka, Jolanta and Kowalski, Konrad and Chen, Yu},

  abstractNote = {We have determined a 1.18 Å resolution X-ray crystal structure of a novel ruthenocenyle-6-aminopenicillinic acid in complex with CTX-M β-lactamase, showing unprecedented details of interactions between ruthenocene and protein. As the first product complex with an intact catalytic serine, the structure also offers insights into β-lactamase catalysis and inhibitor design.},

  doi          = {10.1039/C5CC00904A},

  journal      = {ChemComm},

  number       = 28,

  volume       = 51,

  place        = {United States},

  year         = {Mon Mar 02 00:00:00 EST 2015},

  month        = {Mon Mar 02 00:00:00 EST 2015}

}

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Bio‐Organometallic Derivatives of Antibacterial Drugs
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Sierra, Miguel A.; Casarrubios, Luis; de la Torre, María C.
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Title: Antibacterial properties and atomic resolution X-ray complex crystal structure of a ruthenocene conjugated β-lactam antibiotic

Abstract

Citation Formats

The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis journal, March 2008

Penicillin Binding Proteins: key players in bacterial cell cycle and drug resistance processes journal, September 2006

The future of the β-lactams journal, October 2010

Distinct Single-Cell Morphological Dynamics under Beta-Lactam Antibiotics journal, December 2012

Structural Analysis of the Role of Pseudomonas aeruginosa Penicillin-Binding Protein 5 in β-Lactam Resistance journal, April 2013

Molecular basis of antibiotic resistance and β-lactamase inhibition by mechanism-based inactivators: perspectives and future directions journal, July 2000

Three Decades of -Lactamase Inhibitors journal, January 2010

Resistance to antibiotics targeted to the bacterial cell wall: The Bacterial Cell Wall as a Target for Antibiotics journal, January 2014

The Bacteria Fight Back journal, July 2008

Epidemiological Expansion, Structural Studies, and Clinical Challenges of New β-Lactamases from Gram-Negative Bacteria journal, October 2011

Three Decades of the Class A β-Lactamase Acyl-Enzyme journal, October 2009

Beta-lactamases and bacterial resistance to antibiotics journal, May 1995

A functional classification scheme for beta-lactamases and its correlation with molecular structure journal, June 1995

β-Secondary and Solvent Deuterium Kinetic Isotope Effects on β-Lactamase Catalysis † journal, January 1996

Organometallic Anticancer Compounds journal, January 2011

Ferrocenyl Quinone Methides as Strong Antiproliferative Agents: Formation by Metabolic and Chemical Oxidation of Ferrocenyl Phenols journal, October 2009

Application of ferrocene and its derivatives in cancer research journal, January 2011

Small organometallic compounds as antibacterial agents journal, January 2012

Protein crystal structures with ferrocene and ruthenocene-based enzyme inhibitors journal, January 2012

Bioorganometallic Chemistry of Ferrocene journal, December 2004

Synthesis and study of cytotoxic activity of 1,2,4-trioxane- and egonol-derived hybrid molecules against Plasmodium falciparum and multidrug-resistant human leukemia cells journal, March 2014

Ferrocenyl bioconjugates of ampicillin and 6-aminopenicillinic acid – Synthesis, electrochemistry and biological activity journal, November 2012

Analysis of the Mechanism of Action of Potent Antibacterial Hetero-tri-organometallic Compounds: A Structurally New Class of Antibiotics journal, April 2013

Getting to the route of Helicobacter pylori treatment journal, July 1998

Molecular Basis for the Catalytic Specificity of the CTX-M Extended-Spectrum β-Lactamases journal, December 2014

The Acylation Mechanism of CTX-M β-Lactamase at 0.88 Å Resolution journal, May 2007

Acyl-intermediate Structures of the Extended-spectrum Class A β-Lactamase, Toho-1, in Complex with Cefotaxime, Cephalothin, and Benzylpenicillin journal, September 2002

A series of penicillin-derived C2-symmetric inhibitors of HIV-1 proteinase: synthesis, mode of interaction, and structure-activity relationships journal, October 1993

Structure elucidation of degradation products of the antibiotic amoxicillin with ion trap MSn and accurate mass determination by ESI TOF journal, October 2005

The Molecular Structure of Penicillin journal, October 2004

Structural Insights into Substrate Recognition and Product Expulsion in CTX-M Enzymes journal, July 2010

Structural Milestones in the Reaction Pathway of an Amide Hydrolase journal, March 2002

Crucial role of Ru⋯H interactions in the crystal packing of ruthenocene and its derivatives journal, January 2008

Bio‐Organometallic Derivatives of Antibacterial Drugs journal, March 2019

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The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis
journal, March 2008

Penicillin Binding Proteins: key players in bacterial cell cycle and drug resistance processes
journal, September 2006

The future of the β-lactams
journal, October 2010

Distinct Single-Cell Morphological Dynamics under Beta-Lactam Antibiotics
journal, December 2012

Structural Analysis of the Role of Pseudomonas aeruginosa Penicillin-Binding Protein 5 in β-Lactam Resistance
journal, April 2013

Molecular basis of antibiotic resistance and β-lactamase inhibition by mechanism-based inactivators: perspectives and future directions
journal, July 2000

Three Decades of -Lactamase Inhibitors
journal, January 2010

Resistance to antibiotics targeted to the bacterial cell wall: The Bacterial Cell Wall as a Target for Antibiotics
journal, January 2014

The Bacteria Fight Back
journal, July 2008

Epidemiological Expansion, Structural Studies, and Clinical Challenges of New β-Lactamases from Gram-Negative Bacteria
journal, October 2011

Three Decades of the Class A β-Lactamase Acyl-Enzyme
journal, October 2009

Beta-lactamases and bacterial resistance to antibiotics
journal, May 1995

A functional classification scheme for beta-lactamases and its correlation with molecular structure
journal, June 1995

β-Secondary and Solvent Deuterium Kinetic Isotope Effects on β-Lactamase Catalysis ^†
journal, January 1996

Organometallic Anticancer Compounds
journal, January 2011

Ferrocenyl Quinone Methides as Strong Antiproliferative Agents: Formation by Metabolic and Chemical Oxidation of Ferrocenyl Phenols
journal, October 2009

Application of ferrocene and its derivatives in cancer research
journal, January 2011

Small organometallic compounds as antibacterial agents
journal, January 2012

Protein crystal structures with ferrocene and ruthenocene-based enzyme inhibitors
journal, January 2012

Bioorganometallic Chemistry of Ferrocene
journal, December 2004

Synthesis and study of cytotoxic activity of 1,2,4-trioxane- and egonol-derived hybrid molecules against Plasmodium falciparum and multidrug-resistant human leukemia cells
journal, March 2014

Ferrocenyl bioconjugates of ampicillin and 6-aminopenicillinic acid – Synthesis, electrochemistry and biological activity
journal, November 2012

Analysis of the Mechanism of Action of Potent Antibacterial Hetero-tri-organometallic Compounds: A Structurally New Class of Antibiotics
journal, April 2013

Getting to the route of Helicobacter pylori treatment
journal, July 1998

Molecular Basis for the Catalytic Specificity of the CTX-M Extended-Spectrum β-Lactamases
journal, December 2014

The Acylation Mechanism of CTX-M β-Lactamase at 0.88 Å Resolution
journal, May 2007

Acyl-intermediate Structures of the Extended-spectrum Class A β-Lactamase, Toho-1, in Complex with Cefotaxime, Cephalothin, and Benzylpenicillin
journal, September 2002

A series of penicillin-derived C2-symmetric inhibitors of HIV-1 proteinase: synthesis, mode of interaction, and structure-activity relationships
journal, October 1993

Structure elucidation of degradation products of the antibiotic amoxicillin with ion trap MSn and accurate mass determination by ESI TOF
journal, October 2005

The Molecular Structure of Penicillin
journal, October 2004

Structural Insights into Substrate Recognition and Product Expulsion in CTX-M Enzymes
journal, July 2010

Structural Milestones in the Reaction Pathway of an Amide Hydrolase
journal, March 2002

Crucial role of Ru⋯H interactions in the crystal packing of ruthenocene and its derivatives
journal, January 2008

Bio‐Organometallic Derivatives of Antibacterial Drugs
journal, March 2019

Novel π-Extended Quinazoline-Ferrocene Conjugates: Synthesis, Structure, and Redox Behavior: Novel π-Extended Quinazoline-Ferrocene Conjugates: Synthesis, Structure, and Redox Behavior
journal, May 2020

Anticancer and Antibacterial Activity of Transition Metal Complexes
journal, February 2019

Combatting AMR: photoactivatable ruthenium( ii )-isoniazid complex exhibits rapid selective antimycobacterial activity
journal, January 2017

Mechanisms of proton relay and product release by Class A β‐lactamase at ultrahigh resolution
journal, November 2017

Influence of substrates and inhibitors on the structure of Klebsiella pneumoniae carbapenemase-2
journal, June 2019

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journal, April 2017

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