Metabolic Processing of Selenium-Based Bioisosteres of -Diaminopimelic Acid in Live Bacteria

Overview

Journal Biochemistry

Specialty Biochemistry

Date 2022 Jun 10

PMID 35687722

Authors

Alexis J Apostolos

Karl L Ocius

Thameez M Koyasseril-Yehiya

Carolina Santamaria

Jose Rogerio A Silva

Jeronimo Lameira

Claudio N Alves

M Sloan Siegrist

Marcos M Pires

Affiliations

Soon will be listed here.

Abstract

A primary component of all known bacterial cell walls is the peptidoglycan (PG) layer, which is composed of repeating units of sugars connected to short and unusual peptides. The various steps within PG biosynthesis are targets of potent antibiotics as proper assembly of the PG is essential for cellular growth and survival. Synthetic mimics of PG have proven to be indispensable tools to study the bacterial cell structure, growth, and remodeling. Yet, a common component of PG, -diaminopimelic acid (-DAP) at the third position of the stem peptide, remains challenging to access synthetically and is not commercially available. Here, we describe the synthesis and metabolic processing of a selenium-based bioisostere of -DAP (selenolanthionine) and show that it is installed within the PG of live bacteria by the native cell wall crosslinking machinery in mycobacterial species. This PG probe has an orthogonal release mechanism that could be important for downstream proteomics studies. Finally, we describe a bead-based assay that is compatible with high-throughput screening of cell wall enzymes. We envision that this probe will supplement the current methods available for investigating PG crosslinking in -DAP-containing organisms.

Citing Articles

Study of Chalcogen Aspirin Derivatives with Carbonic Anhydrase Inhibitory Properties for Treating Inflammatory Pain.

Lucarini E, DAntogiovanni V, Antonioli L, Ghelardini C, Di Cesare Mannelli L, Ferraroni M ACS Med Chem Lett. 2024; 15(9):1559-1565.

PMID: 39291024 PMC: 11403731. DOI: 10.1021/acsmedchemlett.4c00284.

Measurement of Accumulation of Antibiotics to Staphylococcus aureus in Phagosomes of Live Macrophages.

Kelly J, Dalesandro B, Liu Z, Chordia M, Ongwae G, Pires M Angew Chem Int Ed Engl. 2023; 63(3):e202313870.

PMID: 38051128 PMC: 10799677. DOI: 10.1002/anie.202313870.

Chemical approaches to unraveling the biology of mycobacteria.

Finin P, Khan R, Oh S, Boshoff H, Barry 3rd C Cell Chem Biol. 2023; 30(5):420-435.

PMID: 37207631 PMC: 10201459. DOI: 10.1016/j.chembiol.2023.04.014.

A Metabolic-Tag-Based Method for Assessing the Permeation of Small Molecules Across the Mycomembrane in Live Mycobacteria.

Liu Z, Lepori I, Chordia M, Dalesandro B, Guo T, Dong J Angew Chem Int Ed Engl. 2023; 62(20):e202217777.

PMID: 36700874 PMC: 10159989. DOI: 10.1002/anie.202217777.

References

Bertsche U, Breukink E, Kast T, Vollmer W . In vitro murein peptidoglycan synthesis by dimers of the bifunctional transglycosylase-transpeptidase PBP1B from Escherichia coli. J Biol Chem. 2005; 280(45):38096-101. DOI: 10.1074/jbc.M508646200. View

PETIT J, Adam A, Lederer E, Ghuysen J . Chemical structure of the cell wall of Mycobacterium smegmatis. I. Isolation and partial characterization of the peptidoglycan. Biochem Biophys Res Commun. 1969; 35(4):478-85. DOI: 10.1016/0006-291x(69)90371-4. View

Morlot C, Straume D, Peters K, Hegnar O, Simon N, Villard A . Structure of the essential peptidoglycan amidotransferase MurT/GatD complex from Streptococcus pneumoniae. Nat Commun. 2018; 9(1):3180. PMC: 6085368. DOI: 10.1038/s41467-018-05602-w. View

Ito M, Kim Y, Tsuji H, Takahashi T, Kiwaki M, Nomoto K . Transposon mutagenesis of probiotic Lactobacillus casei identifies asnH, an asparagine synthetase gene involved in its immune-activating capacity. PLoS One. 2014; 9(1):e83876. PMC: 3885529. DOI: 10.1371/journal.pone.0083876. View

Pidgeon S, Apostolos A, Nelson J, Shaku M, Rimal B, Islam M . L,D-Transpeptidase Specific Probe Reveals Spatial Activity of Peptidoglycan Cross-Linking. ACS Chem Biol. 2019; 14(10):2185-2196. PMC: 6804245. DOI: 10.1021/acschembio.9b00427. View

Harris K, Flemer Jr S, Hondal R . Studies on deprotection of cysteine and selenocysteine side-chain protecting groups. J Pept Sci. 2006; 13(2):81-93. PMC: 3689433. DOI: 10.1002/psc.795. View

Levengood M, van der Donk W . Dehydroalanine-containing peptides: preparation from phenylselenocysteine and utility in convergent ligation strategies. Nat Protoc. 2007; 1(6):3001-10. DOI: 10.1038/nprot.2006.470. View

Apostolos A, Ferraro N, Dalesandro B, Pires M . SaccuFlow: A High-Throughput Analysis Platform to Investigate Bacterial Cell Wall Interactions. ACS Infect Dis. 2021; 7(8):2483-2491. PMC: 8434819. DOI: 10.1021/acsinfecdis.1c00255. View

Okeley N, Zhu Y, van der Donk W . Facile chemoselective synthesis of dehydroalanine-containing peptides. Org Lett. 2000; 2(23):3603-6. DOI: 10.1021/ol006485d. View

10.

Wolf A, Underhill D . Peptidoglycan recognition by the innate immune system. Nat Rev Immunol. 2018; 18(4):243-254. DOI: 10.1038/nri.2017.136. View

11.

Born P, Breukink E, Vollmer W . In vitro synthesis of cross-linked murein and its attachment to sacculi by PBP1A from Escherichia coli. J Biol Chem. 2006; 281(37):26985-93. DOI: 10.1074/jbc.M604083200. View

12.

Girardin S, Travassos L, Herve M, Blanot D, Boneca I, Philpott D . Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem. 2003; 278(43):41702-8. DOI: 10.1074/jbc.M307198200. View

13.

Baranowski C, Welsh M, Sham L, Eskandarian H, Lim H, Kieser K . Maturing peptidoglycan requires non-canonical crosslinks to maintain shape. Elife. 2018; 7. PMC: 6231781. DOI: 10.7554/eLife.37516. View

14.

Flores A, Parsons L, Pavelka M . Genetic analysis of the beta-lactamases of Mycobacterium tuberculosis and Mycobacterium smegmatis and susceptibility to beta-lactam antibiotics. Microbiology (Reading). 2005; 151(Pt 2):521-532. DOI: 10.1099/mic.0.27629-0. View

15.

Fura J, Kearns D, Pires M . D-Amino Acid Probes for Penicillin Binding Protein-based Bacterial Surface Labeling. J Biol Chem. 2015; 290(51):30540-50. PMC: 4683274. DOI: 10.1074/jbc.M115.683342. View

16.

Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, Saab L . An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol. 2003; 4(7):702-7. DOI: 10.1038/ni945. View

17.

Consaul S, Wright L, Mahapatra S, Crick D, Pavelka Jr M . An unusual mutation results in the replacement of diaminopimelate with lanthionine in the peptidoglycan of a mutant strain of Mycobacterium smegmatis. J Bacteriol. 2005; 187(5):1612-20. PMC: 1064014. DOI: 10.1128/JB.187.5.1612-1620.2005. View

18.

de Kruijff B, van Dam V, Breukink E . Lipid II: a central component in bacterial cell wall synthesis and a target for antibiotics. Prostaglandins Leukot Essent Fatty Acids. 2008; 79(3-5):117-21. DOI: 10.1016/j.plefa.2008.09.020. View

19.

Hsu Y, Hall E, Booher G, Murphy B, Radkov A, Yablonowski J . Fluorogenic D-amino acids enable real-time monitoring of peptidoglycan biosynthesis and high-throughput transpeptidation assays. Nat Chem. 2019; 11(4):335-341. PMC: 6444347. DOI: 10.1038/s41557-019-0217-x. View

20.

Denoel T, Zervosen A, Gerards T, Lemaire C, Joris B, Blanot D . Stereoselective synthesis of lanthionine derivatives in aqueous solution and their incorporation into the peptidoglycan of Escherichia coli. Bioorg Med Chem. 2014; 22(17):4621-8. DOI: 10.1016/j.bmc.2014.07.023. View