Macrocycle peptides delineate locked-open inhibition mechanism for microorganism phosphoglycerate mutases
Abstract
Glycolytic interconversion of phosphoglycerate isomers is catalysed in numerous pathogenic microorganisms by a cofactor-independent mutase (iPGM) structurally distinct from the mammalian cofactor-dependent (dPGM) isozyme. The iPGM active site dynamically assembles through substrate-triggered movement of phosphatase and transferase domains creating a solvent inaccessible cavity. Here we identify alternate ligand binding regions using nematode iPGM to select and enrich lariat-like ligands from an mRNA-display macrocyclic peptide library containing >1012 members. Functional analysis of the ligands, named ipglycermides, demonstrates sub-nanomolar inhibition of iPGM with complete selectivity over dPGM. The crystal structure of an iPGM macrocyclic peptide complex illuminated an allosteric, locked-open inhibition mechanism placing the cyclic peptide at the bi-domain interface. This binding mode aligns the pendant lariat cysteine thiolate for coordination with the iPGM transition metal ion cluster. The extended charged, hydrophilic binding surface interaction rationalizes the persistent challenges these enzymes have presented to small-molecule screening efforts highlighting the important roles of macrocyclic peptides in expanding chemical diversity for ligand discovery.
- Authors:
-
- Univ. of Tokyo (Japan)
- National Inst. of Health, Rockville, MD (United States)
- New England Biolabs, Ipswich, MA (United States)
- National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States)
- Univ. of Kansas, Lawrence, KS (United States)
- Univ. of the Sciences, Philadelphia, PA (United States); National Inst. of Health (NIH), Bethesda, MD (United States)
- Argonne National Lab. (ANL), Argonne, IL (United States)
- National Inst. of Health (NIH), Bethesda, MD (United States)
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of General Medical Sciences; National Inst. of Health
- OSTI Identifier:
- 1355041
- Grant/Contract Number:
- AC02-06CH11357; P30GM110761
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 8; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- ENGLISH
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Enzyme mechanisms; High-throughput screening; Isoenzymes; X-ray crystallography
Citation Formats
Yu, Hao, Dranchak, Patricia, Li, Zhiru, MacArthur, Ryan, Munson, Matthew S., Mehzabeen, Nurjahan, Baird, Nathan J., Battalie, Kevin P., Ross, David, Lovell, Scott, Carlow, Clotilde K. S., Suga, Hiroaki, and Inglese, James. Macrocycle peptides delineate locked-open inhibition mechanism for microorganism phosphoglycerate mutases. United States: N. p., 2017.
Web. doi:10.1038/ncomms14932.
Yu, Hao, Dranchak, Patricia, Li, Zhiru, MacArthur, Ryan, Munson, Matthew S., Mehzabeen, Nurjahan, Baird, Nathan J., Battalie, Kevin P., Ross, David, Lovell, Scott, Carlow, Clotilde K. S., Suga, Hiroaki, & Inglese, James. Macrocycle peptides delineate locked-open inhibition mechanism for microorganism phosphoglycerate mutases. United States. https://doi.org/10.1038/ncomms14932
Yu, Hao, Dranchak, Patricia, Li, Zhiru, MacArthur, Ryan, Munson, Matthew S., Mehzabeen, Nurjahan, Baird, Nathan J., Battalie, Kevin P., Ross, David, Lovell, Scott, Carlow, Clotilde K. S., Suga, Hiroaki, and Inglese, James. Mon .
"Macrocycle peptides delineate locked-open inhibition mechanism for microorganism phosphoglycerate mutases". United States. https://doi.org/10.1038/ncomms14932. https://www.osti.gov/servlets/purl/1355041.
@article{osti_1355041,
title = {Macrocycle peptides delineate locked-open inhibition mechanism for microorganism phosphoglycerate mutases},
author = {Yu, Hao and Dranchak, Patricia and Li, Zhiru and MacArthur, Ryan and Munson, Matthew S. and Mehzabeen, Nurjahan and Baird, Nathan J. and Battalie, Kevin P. and Ross, David and Lovell, Scott and Carlow, Clotilde K. S. and Suga, Hiroaki and Inglese, James},
abstractNote = {Glycolytic interconversion of phosphoglycerate isomers is catalysed in numerous pathogenic microorganisms by a cofactor-independent mutase (iPGM) structurally distinct from the mammalian cofactor-dependent (dPGM) isozyme. The iPGM active site dynamically assembles through substrate-triggered movement of phosphatase and transferase domains creating a solvent inaccessible cavity. Here we identify alternate ligand binding regions using nematode iPGM to select and enrich lariat-like ligands from an mRNA-display macrocyclic peptide library containing >1012 members. Functional analysis of the ligands, named ipglycermides, demonstrates sub-nanomolar inhibition of iPGM with complete selectivity over dPGM. The crystal structure of an iPGM macrocyclic peptide complex illuminated an allosteric, locked-open inhibition mechanism placing the cyclic peptide at the bi-domain interface. This binding mode aligns the pendant lariat cysteine thiolate for coordination with the iPGM transition metal ion cluster. The extended charged, hydrophilic binding surface interaction rationalizes the persistent challenges these enzymes have presented to small-molecule screening efforts highlighting the important roles of macrocyclic peptides in expanding chemical diversity for ligand discovery.},
doi = {10.1038/ncomms14932},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {Mon Apr 03 00:00:00 EDT 2017},
month = {Mon Apr 03 00:00:00 EDT 2017}
}
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journal, January 2019
- Katoh, Takayuki; Suga, Hiroaki
- International Journal of Molecular Sciences, Vol. 20, Issue 3