Crystal structures of KPC-2 β-lactamase in complex with 3-nitrophenyl boronic acid and the penam sulfone PSR-3-226

Antimicrob Agents Chemother. 2012 May;56(5):2713-8. doi: 10.1128/AAC.06099-11. Epub 2012 Feb 13.

Abstract

Class A carbapenemases are a major threat to the potency of carbapenem antibiotics. A widespread carbapenemase, KPC-2, is not easily inhibited by β-lactamase inhibitors (i.e., clavulanic acid, sulbactam, and tazobactam). To explore different mechanisms of inhibition of KPC-2, we determined the crystal structures of KPC-2 with two β-lactamase inhibitors that follow different inactivation pathways and kinetics. The first complex is that of a small boronic acid compound, 3-nitrophenyl boronic acid (3-NPBA), bound to KPC-2 with 1.62-Å resolution. 3-NPBA demonstrated a K(m) value of 1.0 ± 0.1 μM (mean ± standard error) for KPC-2 and blocks the active site by making a reversible covalent interaction with the catalytic S70 residue. The two boron hydroxyl atoms of 3-NPBA are positioned in the oxyanion hole and the deacylation water pocket, respectively. In addition, the aromatic ring of 3-NPBA provides an edge-to-face interaction with W105 in the active site. The structure of KPC-2 with the penam sulfone PSR-3-226 was determined at 1.26-Å resolution. PSR-3-226 displayed a K(m) value of 3.8 ± 0.4 μM for KPC-2, and the inactivation rate constant (k(inact)) was 0.034 ± 0.003 s(-1). When covalently bound to S70, PSR-3-226 forms a trans-enamine intermediate in the KPC-2 active site. The predominant active site interactions are generated via the carbonyl oxygen, which resides in the oxyanion hole, and the carboxyl moiety of PSR-3-226, which interacts with N132, N170, and E166. 3-NPBA and PSR-3-226 are the first β-lactamase inhibitors to be trapped as an acyl-enzyme complex with KPC-2. The structural and inhibitory insights gained here could aid in the design of potent KPC-2 inhibitors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / chemistry*
  • Anti-Bacterial Agents / metabolism
  • Boronic Acids / chemistry*
  • Carbapenems / chemistry*
  • Carbapenems / metabolism
  • Catalytic Domain
  • Crystallography, X-Ray
  • Heterocyclic Compounds, 2-Ring / chemistry*
  • Heterocyclic Compounds, 2-Ring / metabolism
  • Kinetics
  • Klebsiella pneumoniae / enzymology*
  • Models, Molecular
  • Sulfones / chemistry*
  • Thiazolidines / chemistry*
  • Thiazolidines / metabolism
  • beta-Lactam Resistance / physiology
  • beta-Lactamase Inhibitors
  • beta-Lactamases / chemistry*
  • beta-Lactamases / metabolism

Substances

  • Anti-Bacterial Agents
  • Boronic Acids
  • Carbapenems
  • Heterocyclic Compounds, 2-Ring
  • PSR-3-226
  • Sulfones
  • Thiazolidines
  • beta-Lactamase Inhibitors
  • 3-nitrobenzeneboronic acid
  • beta-lactamase KPC-2
  • beta-Lactamases