Chemical polyglycosylation and nanolitre detection enables single-molecule recapitulation of bacterial sugar export

Nature Chemistry

Volumn 8, Issue 5, 2016, Pages 461-469

  Kong, Lingbing ^a   Almond, Andrew ^b   Bayley, Hagan ^a   Davis, Benjamin G ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE;

CHEMISTRY; CONFORMATION; ESCHERICHIA COLI; GLYCOSYLATION; LIPID BILAYER; METABOLISM; MOLECULAR DYNAMICS; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CARBOHYDRATE CONFORMATION; ESCHERICHIA COLI; GLYCOSYLATION; LIPID BILAYERS; MOLECULAR DYNAMICS SIMULATION; POLYSACCHARIDES, BACTERIAL;

EID: 84964426740     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2487     Document Type: Article

References (42)

1. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nature Rev. Microbiol. 8, 171-184 (2010).
2. Bushell, S. R. et al. Crystallization and preliminary diffraction analysis of Wzi, a member of the capsule export and assembly pathway in Escherichia coli. Acta Crystallogr. F 66, 1621-1625 (2010).
3. Cuthbertson, L., Mainprize, I. L., Naismith, J. H. & Whitfield, C. Pivotal roles of the outer membrane polysaccharide export and polysaccharide copolymerase protein families in export of extracellular polysaccharides in Gram-negative bacteria. Microbiol. Mol. Biol. Rev. 73, 155-177 (2009).
4. Dong, C. et al. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444, 226-229 (2006).
5. Whitfield, C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75, 39-68 (2006).
6. Nickerson, N. N. et al. Trapped translocation intermediates establish the route for export of capsular polysaccharides across Escherichia coli outer membranes. Proc. Natl Acad. Sci. USA 111, 8203-8208 (2014).
7. Bushell, S. R. et al. Wzi is an outer membrane lectin that underpins group 1 capsule assembly in Escherichia coli. Structure 21, 844-853 (2013).
8. Willis, L. M. & Whitfield, C. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr. Res. 378, 35-44 (2013).
9. Micoli, F. et al. Development of a glycoconjugate vaccine to prevent meningitis in Africa caused by meningococcal serogroup X. Proc. Natl Acad. Sci. USA 110, 19077-19082 (2013).
10. Adamo, R. et al. Synthetically defined glycoprotein vaccines: current status and future directions. Chem. Sci. 4, 2995-3008 (2013).
11. Boltje, T. J., Buskas, T. & Boons, G.-J. Opportunities and challenges in synthetic oligosaccharide and glycoconjugate research. Nature Chem. 1, 611-622 (2009).
12. Wang, L.-X. & Davis, B. G. Realizing the promise of chemical glycobiology. Chem. Sci. 4, 3381-3394 (2013).
13. Hudak, J. E. & Bertozzi, C. R. Glycotherapy: new advances inspire a reemergence of glycans in medicine. Chem. Biol. 21, 16-37 (2014).
14. Hungerer, D., Jann, K., Jann, B., Orskov, F. & Orskov, I. Immunochemistry of K antigens of Escherichia coli. 4. The K antigen of E. coli O9:K30:H12. Eur. J. Biochem. 2, 115-126 (1967).
15. Schuster, H. J., Vijayakrishnan, B. & Davis, B. G. Chain-growth polyglycosylation: synthesis of linker-equipped mannosyl oligomers. Carbohydr. Res. 403, 135-141 (2015).
16. Kochetkov, N. K., Betaneh, V. I., Ovchmmkov, M. V. & Backmowsky, L. V. Synthesis of the O-antigenic polysaccharide of Salmonella newington and of its analogue differing in configuration at the only glycosidic centre. Tetrahedron 37, 149 (1981).
17. Kochetkov, N. K. Tetrahedron report number 218: synthesis of polysaccharides with a regular structure. Tetrahedron 43, 2389-2436 (1987).
18. Nifantiev, N. E., Backmowsky, L. V. & Kochetkov, N. K. Synthesis of the capsular polysaccharide of Streptococcus pneumoniae type 14. Bioorg Khzm (USSR) 13, 273 (1987).
19. Kong, L. et al. Single-molecule interrogation of a bacterial sugar transporter allows the discovery of an extracellular inhibitor. Nature Chem. 5, 651-659 (2013).
20. Fischer, A., Holden, M. A., Pentelute, B. L. & Collier, R. J. Ultrasensitive detection of protein translocated through toxin pores in droplet-interface bilayers. Proc. Natl Acad. Sci. USA 108, 16577-16581.
21. Holden, M. A., Needham, D. & Bayley, H. Functional bionetworks from nanoliter water droplets. J. Am. Chem. Soc. 129, 8650-8655 (2007).
22. Hwang, W. L., Chen, M., Cronin, B., Holden, M. A. & Bayley, H. Asymmetric droplet interface bilayers. J. Am. Chem. Soc. 130, 5878-5879 (2008).
23. Hwang, W. L., Holden, M. A., White, S. & Bayley, H. Electrical behavior of droplet interface bilayer networks: experimental analysis and modeling. J. Am. Chem. Soc. 129, 11854-11864 (2007).
24. Syeda, R., Holden, M. A., Hwang, W. L. & Bayley, H. Screening blockers against a potassium channel with a droplet interface bilayer array. J. Am. Chem. Soc. 130, 15543-15548 (2008).
25. Lein, M., Huang, J. & Holden, M. A. Robust reagent addition and perfusion strategy for droplet-interface bilayers. Lab Chip 13, 2749-2753 (2013).
26. Li, Z. & Gildersleeve, J. C. Mechanistic studies and methods to prevent aglycon transfer of thioglycosides. J. Am. Chem. Soc. 128, 11612-11619 (2006).
27. Kato, M., Hirai, G. & Sodeoka, M. Studies on the selectivity between glycosylation and intermolecular aglycone transfer of thioglucoside in synthesis of lactose derivatives. Chem. Lett. 40, 877-879 (2011).
28. Cheng, L., Chen, Q., Liu, J. & Du, Y. Synthesis of a fluorescence-labeled K30 antigen repeating unit using click chemistry. Carbohydr. Res. 342, 975-981 (2007).
29. Bazin, H. G., Wolff, M. W. & Linhardt, R. J. Regio- and stereoselective synthesis of β-D-gluco-, α-L-ido-, and α-L-altropyranosiduronic acids from Δ(4)-uronates. J. Org. Chem. 64, 144-152 (1999).
30. Matsuo, I., Isomura, M., Miyazaki, T., Sakakibara, T. & Ajisaka, K. Chemoenzymatic synthesis of the branched oligosaccharides which correspond to the core structures of N-linked sugar chains. Carbohydr. Res. 305, 401-413 (1997).
31. de Kort, M. et al. Synthesis of potent agonists of the D-myo-inositol 1,4,5-trisphosphate receptor based on clustered disaccharide polyphosphate analogues of adenophostin A. J. Med. Chem. 43, 3295-3303 (2000).
32. Kullman, L., Winterhalter, M. & Bezrukov, S. M. Transport of maltodextrins through maltoporin: a single-channel study. Biophys. J. 82, 803-812 (2002).
33. Dumas, F., Koebnik, R., Winterhalter, M. & Van Gelder, P. Sugar transport through maltoporin of Escherichia coli: role of polar tracks. J. Biol. Chem. 275, 19747-19751 (2000).
34. Sanchez-Quesada, J., Ghadiri, M. R., Bayley, H. & Braha, O. Cyclic peptides as molecular adapters for a pore-forming protein. J. Am. Chem. Soc. 122, 11758-11766 (2000).
35. Gu, L.-Q., Cheley, S. & Bayley, H. Capture of a single molecule in a nanocavity. Science 291, 636-640 (2001).
36. Sattelle, B. M. & Almond, A. Shaping up for structural glycomics: a predictive protocol for oligosaccharide conformational analysis applied to N-linked glycans. Carbohydr. Res. 383, 34-42 (2014).
37. Harvey, M. J., Giupponi, G. & Fabritiis, G. D. ACEMD: accelerating biomolecular dynamics in the microsecond time-scale. J. Chem. Theory Comput. 5, 1632-1639 (2009).
38. Schirmer, T., Keller, T. A., Wang, Y. F. & Rosenbusch, J. P. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science 267, 512-514 (1995).
39. Nikaido, H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67, 593-656 (2003).
40. Collins, R. F. et al. The 3D structure of a periplasm-spanning platform required for assembly of group 1 capsular polysaccharides in Escherichia coli. Proc. Natl Acad. Sci. USA 104, 2390-2395 (2007).
41. Bohne, A., Lang, E. & von der Lieth, C.W. W3-SWEET: carbohydrate modeling by internet. J. Mol. Model. 4, 33-43 (1998).
42. Bohne, A., Lang, E. & von der Lieth, C. W. SWEET-WWW-based rapid 3D construction of oligo- and polysaccharides. Bioinformatics 15, 767-768 (1999).