Abstract
Serine hydrolases are one of the largest and most diverse enzyme classes in Nature. Most serine hydrolases lack selective inhibitors, which are valuable probes for assigning functions to these enzymes. We recently discovered a set of aza-β-lactams (ABLs) that act as potent and selective inhibitors of the mammalian serine hydrolase protein-phosphatase methylesterase-1 (PME-1). The ABLs inactivate PME-1 by covalent acylation of the enzyme's serine nucleophile, suggesting that they could offer a general scaffold for serine hydrolase inhibitor discovery. Here, we have tested this hypothesis by screening ABLs more broadly against cell and tissue proteomes by competitive activity-based protein profiling (ABPP), leading to the discovery of lead inhibitors for several serine hydrolases, including the uncharacterized enzyme α,β-hydrolase domain-containing 10 (ABHD10). ABPP-guided medicinal chemistry yielded a compound ABL303 that potently (IC(50) ≈ 30 nM) and selectively inactivated ABHD10 in vitro and in living cells. A comparison of optimized inhibitors for PME-1 and ABHD10 indicates that modest structural changes that alter steric bulk can tailor the ABL to selectively react with distinct, distantly related serine hydrolases. Our findings, taken together, designate the ABL as a versatile reactive group for creating first-in-class serine hydrolase inhibitors.
MeSH Terms
Binding, Competitive/drug effects
Molecular Structure
Serine Endopeptidases/metabolism
Serine Proteinase Inhibitors/chemical synthesis,chemistry,pharmacology
Stereoisomerism
Structure-Activity Relationship
beta-Lactams/chemistry,pharmacology
Chemicals
Serine Proteinase Inhibitors
beta-Lactams
Serine Endopeptidases
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Zuhl Andrea M
Department of Chemical Physiology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037, United States.
Mohr Justin T
Bachovchin Daniel A
Niessen Sherry
Hsu Ku-Lung
Berlin Jacob M
Dochnahl Maximilian
López-Alberca María P
Fu Gregory C
Cravatt Benjamin F
References (21)
21 references, click to expand
-
A potent and selective inhibitor of KIAA1363/AADACL1 that impairs prostate cancer pathogenesis.
Chem Biol. 2011 Apr 22;18(4):476-84
PMID: 21513884
-
Activity-based protein profiling: from enzyme chemistry to proteomic chemistry.
Annu Rev Biochem. 2008;77:383-414
PMID: 18366325
-
Discovering potent and selective reversible inhibitors of enzymes in complex proteomes.
Nat Biotechnol. 2003 Jun;21(6):687-91
PMID: 12740587
-
Activity-based protein profiling: applications to biomarker discovery, in vivo imaging and drug discovery.
Am J Pharmacogenomics. 2004;4(6):371-81
PMID: 15651898
-
Catalytic asymmetric cycloaddition of ketenes and nitroso compounds: enantioselective synthesis of alpha-hydroxycarboxylic acid derivatives.
Angew Chem Int Ed Engl. 2009;48(13):2391-3
PMID: 19226588
-
ALS-linked mutant superoxide dismutase 1 (SOD1) alters mitochondrial protein composition and decreases protein import.
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21146-51
PMID: 21078990
-
Direct visualization of serine hydrolase activities in complex proteomes using fluorescent active site-directed probes.
Proteomics. 2001 Sep;1(9):1067-71
PMID: 11990500
-
Academic cross-fertilization by public screening yields a remarkable class of protein phosphatase methylesterase-1 inhibitors.
Proc Natl Acad Sci U S A. 2011 Apr 26;108(17):6811-6
PMID: 21398589
-
Beta-lactones as privileged structures for the active-site labeling of versatile bacterial enzyme classes.
Angew Chem Int Ed Engl. 2008;47(24):4600-3
PMID: 18383487
-
A functional proteomic strategy to discover inhibitors for uncharacterized hydrolases.
J Am Chem Soc. 2007 Aug 8;129(31):9594-5
PMID: 17629278
-
The metabolic serine hydrolases and their functions in mammalian physiology and disease.
Chem Rev. 2011 Oct 12;111(10):6022-63
PMID: 21696217
-
A streamlined platform for high-content functional proteomics of primary human specimens.
Nat Methods. 2005 Sep;2(9):691-7
PMID: 16118640
-
Click-generated triazole ureas as ultrapotent in vivo-active serine hydrolase inhibitors.
Nat Chem Biol. 2011 May 15;7(7):469-78
PMID: 21572424
-
Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects.
Nat Chem Biol. 2009 Jan;5(1):37-44
PMID: 19029917
-
Discovery and characterization of a highly selective FAAH inhibitor that reduces inflammatory pain.
Chem Biol. 2009 Apr 24;16(4):411-20
PMID: 19389627
-
Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening.
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):20941-6
PMID: 21084632
-
Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes.
Nat Biotechnol. 2009 Apr;27(4):387-94
PMID: 19329999
-
A review of HCV protease inhibitors.
Curr Opin Investig Drugs. 2009 Aug;10(8):821-37
PMID: 19649927
-
The pharmacological landscape and therapeutic potential of serine hydrolases.
Nat Rev Drug Discov. 2012 Jan 03;11(1):52-68
PMID: 22212679
-
Enantioselective nucleophilic catalysis: the synthesis of aza-beta-lactams through [2+2] cycloadditions of ketenes with azo compounds.
Angew Chem Int Ed Engl. 2008;47(37):7048-50
PMID: 18668500
-
Acylating drugs: redesigning natural covalent inhibitors.
Curr Opin Chem Biol. 2010 Jun;14(3):421-7
PMID: 20457000