Metabolic labelling of the carbohydrate core in bacterial peptidoglycan and its applications

Nature Communications

Volumn 8, Issue , 2017, Pages

  Liang, Hai ^a   DeMeester, Kristen E ^a   Hou, Ching Wen ^a   Parent, Michelle A ^a   Caplan, Jeffrey L ^a   Grimes, Catherine L ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MURAMIC ACID; N ACETYL MURAMIC ACID; PEPTIDOGLYCAN; UNCLASSIFIED DRUG; N-ACETYLMURAMIC ACID;

ANTIBIOTICS; BACTERIUM; CARBOHYDRATE; CELLS AND CELL COMPONENTS; IMMUNE SYSTEM; METABOLISM; OSMOSIS; POLYMER;

ARTICLE; BACTERIAL CELL WALL; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CHEMICAL LABELING; CLICK CHEMISTRY; CONTROLLED STUDY; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; IMMUNOCOMPETENT CELL; MICROSCOPY; NONHUMAN; WHOLE CELL; ANIMAL; BACTERIUM; CELL LINE; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENETICS; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE; PHYSIOLOGY; TIME LAPSE IMAGING;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

ANIMALS; BACTERIA; CARBOHYDRATE SEQUENCE; CELL LINE; CELL WALL; ESCHERICHIA COLI; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; MACROPHAGES; MICE; MICROSCOPY, FLUORESCENCE; MOLECULAR STRUCTURE; MURAMIC ACIDS; PEPTIDOGLYCAN; TIME-LAPSE IMAGING;

EID: 85018306593     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15015     Document Type: Article

References (70)

1. Holtje, J. V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62, 181-203 (1998).
2. Schleifer, K. H. & Kandler, O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36, 407-477 (1972).
3. Rogers, H. J. Peptidoglycans (mucopeptides): structure, function, and variations. Ann. N. Y. Acad. Sci. 235, 29-51 (1974).
4. Walsh, C. Molecular mechanisms that confer antibacterial drug resistance. Nature 406, 775-781 (2000).
5. Strominger, J. L. Bacterial cell walls, innate immunity and immunoadjuvants. Nat. Immunol. 8, 1269-1271 (2007).
6. Janeway, Jr. C. A. & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
7. Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14 e1002533 1-21 (2016).
8. Mackey, D. & McFall, A. J. MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol. Microbiol. 61, 1365-1371 (2006).
9. Brubaker, S. W., Bonham, K. S., Zanoni, I. & Kagan, J. C. Innate immune pattern recognition: a cell biological perspective. Annu. Rev. Immunol. 33, 257-290 (2015).
10. Ting, J. P., Duncan, J. A. & Lei, Y. How the noninflammasome NLRs function in the innate immune system. Science 327, 286-290 (2010).
11. Chen, G., Shaw, M. H., Kim, Y. G. & Nunez, G. NOD-like receptors: role in innate immunity and inflammatory disease. Annu. Rev. Pathol. 4, 365-398 (2009).
12. Ellouz, F., Adam, A., Ciorbaru, R. & Lederer, E. Minimal structural requirements for adjuvant activity of bacterial peptidoglycan derivatives. Biochem. Biophys. Res. Commun. 59, 1317-1325 (1974).
13. Girardin, S. E. et al. Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278, 41702-41708 (2003).
14. Inohara, N. et al. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278, 5509-5512 (2003).
15. Geddes, K., Magalhaes, J. G. & Girardin, S. E. Unleashing the therapeutic potential of NOD-like receptors. Nat. Rev. Drug Discov. 8, 465-479 (2009).
16. Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65-74 (2016).
17. Hasegawa, M. et al. Differential release and distribution of Nod1 and Nod2 immunostimulatory molecules among bacterial species and environments J. Biol. Chem. 281, 29054-29063 (2006).
18. Humann, J. & Lenz, L. L. Bacterial peptidoglycan degrading enzymes and their impact on host muropeptide detection. J. Innate Immun. 1, 88-97 (2009).
19. Dziarski, R. Recognition of bacterial peptidoglycan by the innate immune system. Cell Mol. Life Sci. 60, 1793-1804 (2003).
20. Shimada, T. et al. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7, 38-49 (2010).
21. Herskovits, A. A., Auerbuch, V. & Portnoy, D. A. Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog. 3 e51 431-443 (2007).
22. Wyckoff, T. J., Taylor, J. A. & Salama, N. R. Beyond growth: novel functions for bacterial cell wall hydrolases. Trends Microbiol. 20, 540-547 (2012).
23. Strominger, J. L., Park, J. T. & Thompson, R. E. Composition of the cell wall of Staphylococcus aureus: its relation to the mechanism of action of penicillin J. Biol. Chem. 234, 3263-3268 (1959).
24. Bertozzi, C. R. & Kiessling, L. L. Chemical glycobiology. Science 291, 2357-2364 (2001).
25. Sadamoto, R. et al. Cell-wall engineering of living bacteria. J. Am. Chem. Soc. 124, 9018-9019 (2002).
26. Liechti, G. W. et al. A new metabolic cell-wall labelling method reveals peptidoglycan in Chlamydia trachomatis. Nature 506, 507-510 (2014).
27. Kuru, E. et al. In Situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent D-amino acids. Angew. Chem. Int. Ed. Engl. 51, 12519-12523 (2012).
28. Lebar, M. D. et al. Reconstitution of peptidoglycan cross-linking leads to improved fluorescent probes of cell wall synthesis. J. Am. Chem. Soc. 136, 10874-10877 (2014).
29. Gale, R. T. & Brown, E. D. New chemical tools to probe cell wall biosynthesis in bacteria. Curr. Opin. Microbiol. 27, 69-77 (2015).
30. Siegrist, M. S. et al. (D)-Amino acid chemical reporters reveal peptidoglycan dynamics of an intracellular pathogen. ACS Chem. Biol. 8, 500-505 (2013).
31. Shieh, P., Siegrist, M. S., Cullen, A. J. & Bertozzi, C. R. Imaging bacterial peptidoglycan with near-infrared fluorogenic azide probes. Proc. Natl Acad. Sci. USA 111, 5456-5461 (2014).
32. Tiyanont, K. et al. Imaging peptidoglycan biosynthesis in Bacillus subtilis with fluorescent antibiotics. Proc. Natl Acad. Sci. USA 103, 11033-11038 (2006).
33. Kocaoglu, O. et al. Selective penicillin-binding protein imaging probes reveal substructure in bacterial cell division. ACS Chem. Biol. 7, 1746-1753 (2012).
34. Daniel, R. A. & Errington, J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113, 767-776 (2003).
35. Nelson, J.W. et al. A biosynthetic strategy for re-engineering the Staphylococcus aureus cell wall with non-native small molecules. ACS Chem. Biol. 5, 1147-1155 (2010).
36. Garner, E. C. et al. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333, 222-225 (2011).
37. Sadamoto, R. et al. Bacterial surface engineering utilizing glucosamine phosphate derivatives as cell wall precursor surrogates. Chemistry 14, 10192-10195 (2008).
38. Raymond, J. B., Mahapatra, S., Crick, D. C. & Pavelka, Jr. M. S. Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J. Biol. Chem. 280, 326-333 (2005).
39. Hansen, J. M. et al. N-glycolylated peptidoglycan contributes to the immunogenicity but not pathogenicity of Mycobacterium tuberculosis. J. Infect. Dis. 209, 1045-1054 (2014).
40. Melnyk, J. E., Mohanan, V., Schaefer, A. K., Hou, C. W. & Grimes, C. L. Peptidoglycan modifications tune the stability and function of the innate immune receptor Nod2. J. Am. Chem. Soc. 137, 6987-6990 (2015).
41. Gisin, J., Schneider, A., Nagele, B., Borisova, M. & Mayer, C. A cell wall recycling shortcut that bypasses peptidoglycan de novo biosynthesis. Nat. Chem. Biol. 9, 491-493 (2013).
42. Ye, H. et al. A safe and facile route to imidazole-1-sulfonyl azide as a diazotransfer reagent. Org. Lett. 15, 18-21 (2013).
43. Dahl, U., Jaeger, T., Nguyen, B. T., Sattler, J. M. & Mayer, C. Identification of a phosphotransferase system of Escherichia coli required for growth on N-acetylmuramic acid. J. Bacteriol. 186, 2385-2392 (2004).
44. Uehara, T., Suefuji, K., Jaeger, T., Mayer, C. & Park, J. T. MurQ Etherase is required by Escherichia coli in order to metabolize anhydro-N-acetylmuramic acid obtained either from the environment or from its own cell wall. J. Bacteriol. 188, 1660-1662 (2006).
45. Kahan, F. M., Kahan, J. S., Cassidy, P. J. & Kropp, H. The mechanism of action of fosfomycin (phosphonomycin). Ann. N. Y. Acad. Sci. 235, 364-386 (1974).
46. Kolb, H. C., Finn, M. G. & Sharpless, K. B. Click chemistry: diverse chemical function from a few good reactions. Angew. Chem. Int. Ed. Engl. 40, 2004-2021 (2001).
47. Gustafsson, M. G. et al. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957-4970 (2008).
48. Adams, D. W. & Errington, J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7, 642-653 (2009).
49. Rust, M. J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793-795 (2006).
50. Buss, J. et al. In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol. Microbiol. 89, 1099-1120 (2013).
51. Turner, R. D., Hurd, A. F., Cadby, A., Hobbs, J. K. & Foster, S. J. Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture. Nat. Commun. 4, 1496 (2013).
52. Osawa, T. & Jeanloz, R. W. An improved, stereoselective synthesis of 2-amino- 3-O-(D-1-carboxyethyl)-2-deoxy-D-glucose (muramic acid). J. Org. Chem. 30, 448-450 (1965).
53. Matsushima, Y. & Park, J. T. Stereospecific synthesis of 2-amino-3-O-(D-10- carboxyethyl)-2-deoxy-D-glucose (muramic acid) and related compounds1, 2. J. Org. Chem. 27, 3581-3583 (1962).
54. Ragoussis, V., Leondiadis, L., Livaniou, E. & Evangelatos, G. P. A simple approach to the synthesis of muramic acid and isomuramic acid: 1H and 13C NMR characterisation. Carbohydrate Res. 297, 289-295 (1997).
55. Borisova, M. et al. Peptidoglycan recycling in Gram-positive bacteria is crucial for survival in stationary phase. mBio 7, e00923-e01016 (2016).
56. Tsui, H. C. et al. Pbp2x localizes separately from Pbp2b and other peptidoglycan synthesis proteins during later stages of cell division of Streptococcus pneumoniae D39. Mol. Microbiol. 94, 21-40 (2014).
57. de Pedro, M. A. & Cava, F. Structural constraints and dynamics of bacterial cell wall architecture. Front. Microbiol. 6, 449 (2015).
58. Hayhurst, E. J., Kailas, L., Hobbs, J. K. & Foster, S. J. Cell wall peptidoglycan architecture in Bacillus subtilis. Proc. Natl Acad. Sci. USA 105, 14603-14608 (2008).
59. Wang, S., Furchtgott, L., Huang, K. C. & Shaevitz, J. W. Helical insertion of peptidoglycan produces chiral ordering of the bacterial cell wall. Proc. Natl Acad. Sci. USA 109, 595-604 (2012).
60. Scheffers, D. J. & Pinho, M. G. Bacterial cell wall synthesis: new insights from localization studies. Microbiol. Mol. Biol. Rev. 69, 585-607 (2005).
61. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 1-11 (2006).
62. Konkol, M. A., Blair, K. M. & Kearns, D. B. Plasmid-encoded ComI inhibits competence in the ancestral 3610 strain of Bacillus subtilis. J. Bacteriol. 195, 4085-4093 (2013).
63. Yasbin, R. E., Wilson, G. A. & Young, F. E. Transformation and transfection in lysogenic strains of Bacillus subtilis: evidence for selective induction of prophage in competent cells. J. Bacteriol. 121, 296-304 (1975).
64. Falk, P. J., Ervin, K. M., Volk, K. S. & Ho, H. T. Biochemical evidence for the formation of a covalent acyl-phosphate linkage between UDP-Nacetylmuramate and ATP in the Escherichia coli UDP-N-acetylmuramate: L-alanine ligase-catalyzed reaction. Biochemistry 35, 1417-1422 (1996).
65. Auger, G. et al. Large-scale preparation, purification, and crystallization of UDP-N-acetylmuramoyl-L-alanine: D-glutamate ligase from Escherichia coli. Protein Expr. Purif. 13, 23-29 (1998).
66. Zeng, B., Wong, K. K., Pompliano, D. L., Reddy, S. & Tanner, M. E. A phosphinate inhibitor of the meso-diaminopimelic acid-adding enzyme (MurE) of peptidoglycan biosynthesis. J. Org. Chem. 63, 10081-10085 (1998).
67. Anderson, M. S., Eveland, S. S., Onishi, H. R. & Pompliano, D. L. Kinetic mechanism of the Escherichia coli UDPMurNAc-tripeptide D-alanyl-D-alanineadding enzyme: use of a glutathione S-transferase fusion. Biochemistry 35, 16264-16269 (1996).
68. Dempsey, G. T., Vaughan, J. C., Chen, K. H., Bates, M. & Zhuang, X. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat. Methods 8, 1027-1036 (2011).
69. Klein, T. et al. Live-cell dSTORM with SNAP-tag fusion proteins. Nat. Methods 8, 7-9 (2011).
70. van de Linde, S. et al. Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat. Protoc. 6, 991-1009 (2011).