TY - JOUR
T1 - Inhibiting Mycobacterium abscessus Cell Wall Synthesis
T2 - Using a Novel Diazabicyclooctane b-Lactamase Inhibitor To Augment b-Lactam Action
AU - Dousa, Khalid M.
AU - Nguyen, David C.
AU - Kurz, Sebastian G.
AU - Taracila, Magdalena A.
AU - Bethel, Christopher R.
AU - Schinabeck, William
AU - Kreiswirth, Barry N.
AU - Brown, Sheldon T.
AU - Henry Boom, W.
AU - Hotchkiss, Richard S.
AU - Remy, Kenneth E.
AU - Jacono, Frank J.
AU - Daley, Charles L.
AU - Holland, Steven M.
AU - Miller, Alita A.
AU - Bonomo, Robert A.
N1 - Publisher Copyright:
© 2022 American Society for Microbiology. All rights reserved.
PY - 2022/2/1
Y1 - 2022/2/1
N2 - Mycobacterium abscessus (Mab) infections are a growing menace to the health of many patients, especially those suffering from structural lung disease and cystic fibrosis. With multidrug resistance a common feature and a growing understanding of peptidoglycan synthesis in Mab, it is advantageous to identify potent b-lactam and b-lactamase inhibitor combinations that can effectively disrupt cell wall synthesis. To improve existing therapeutic regimens to address serious Mab infections, we evaluated the ability of durlobactam (DUR), a novel diazobicyclooctane b-lactamase inhibitor to restore in vitro susceptibilities in combination with b-lactams and provide a biochemical rationale for the activity of this compound. In cell-based assays, susceptibility of Mab subsp. abscessus isolates to amoxicillin (AMOX), imipenem (IMI), and cefuroxime (CXM) was significantly enhanced with the addition of DUR. The triple drug combinations of CXM-DUR-AMOX and IMI-DUR-AMOX were most potent, with MIC ranges of #0.06 to 1 mg/mL and an MIC50/MIC90 of #0.06/ 0.25 mg/mL, respectively. We propose a model by which this enhancement may occur, DUR potently inhibited the b-lactamase BlaMab with a relative Michaelis constant (Ki app) of 4 x 1023 6 0.8 x 1023 mM and acylation rate (k2/K) of 1 x 107 M21 s21. Timed mass spectrometry captured stable formation of carbamoyl-enzyme complexes between DUR and LdtMab2-4 and Mab D,D-carboxypeptidase, potentially contributing to the intrinsic activity of DUR. Molecular modeling showed unique and favorable interactions of DUR as a BlaMab inhibitor. Similarly, modeling showed how DUR might form stable Michaelis-Menten complexes with LdtMab2-4 and Mab D,D-carboxypeptidase. The ability of DUR combined with amoxicillin or cefuroxime and imipenem to inactivate multiple targets such as D,D-carboxypeptidase and LdtMab2,4 supports new therapeutic approaches using b-lactams in eradicating Mab. IMPORTANCE Durlobactam (DUR) is a potent inhibitor of BlaMab and provides protection of amoxicillin and imipenem against hydrolysis. DUR has intrinsic activity and forms stable acyl-enzyme complexes with LdtMab2 and LdtMab4. The ability of DUR to protect amoxicillin and imipenem against BlaMab and its intrinsic activity along with the dual b-lactam target redundancy can explain the rationale behind the potent activity of this combination.
AB - Mycobacterium abscessus (Mab) infections are a growing menace to the health of many patients, especially those suffering from structural lung disease and cystic fibrosis. With multidrug resistance a common feature and a growing understanding of peptidoglycan synthesis in Mab, it is advantageous to identify potent b-lactam and b-lactamase inhibitor combinations that can effectively disrupt cell wall synthesis. To improve existing therapeutic regimens to address serious Mab infections, we evaluated the ability of durlobactam (DUR), a novel diazobicyclooctane b-lactamase inhibitor to restore in vitro susceptibilities in combination with b-lactams and provide a biochemical rationale for the activity of this compound. In cell-based assays, susceptibility of Mab subsp. abscessus isolates to amoxicillin (AMOX), imipenem (IMI), and cefuroxime (CXM) was significantly enhanced with the addition of DUR. The triple drug combinations of CXM-DUR-AMOX and IMI-DUR-AMOX were most potent, with MIC ranges of #0.06 to 1 mg/mL and an MIC50/MIC90 of #0.06/ 0.25 mg/mL, respectively. We propose a model by which this enhancement may occur, DUR potently inhibited the b-lactamase BlaMab with a relative Michaelis constant (Ki app) of 4 x 1023 6 0.8 x 1023 mM and acylation rate (k2/K) of 1 x 107 M21 s21. Timed mass spectrometry captured stable formation of carbamoyl-enzyme complexes between DUR and LdtMab2-4 and Mab D,D-carboxypeptidase, potentially contributing to the intrinsic activity of DUR. Molecular modeling showed unique and favorable interactions of DUR as a BlaMab inhibitor. Similarly, modeling showed how DUR might form stable Michaelis-Menten complexes with LdtMab2-4 and Mab D,D-carboxypeptidase. The ability of DUR combined with amoxicillin or cefuroxime and imipenem to inactivate multiple targets such as D,D-carboxypeptidase and LdtMab2,4 supports new therapeutic approaches using b-lactams in eradicating Mab. IMPORTANCE Durlobactam (DUR) is a potent inhibitor of BlaMab and provides protection of amoxicillin and imipenem against hydrolysis. DUR has intrinsic activity and forms stable acyl-enzyme complexes with LdtMab2 and LdtMab4. The ability of DUR to protect amoxicillin and imipenem against BlaMab and its intrinsic activity along with the dual b-lactam target redundancy can explain the rationale behind the potent activity of this combination.
KW - Antibiotic resistance
KW - Antibiotics
KW - B-lactamase inhibitor
KW - B-lactams
KW - Bacteria
KW - Diazabicyclooctane
KW - Durlobactam
KW - Inhibitor
KW - Mycobacterium
KW - Mycobacterium abscessus
UR - http://www.scopus.com/inward/record.url?scp=85125840621&partnerID=8YFLogxK
U2 - 10.1128/MBIO.03529-21
DO - 10.1128/MBIO.03529-21
M3 - Article
C2 - 35073757
AN - SCOPUS:85125840621
SN - 2161-2129
VL - 13
JO - mBio
JF - mBio
IS - 1
M1 - e03529
ER -