Trapped translocation intermediates establish the route for export of capsular polysaccharides across Escherichia coli outer membranes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 22, 2014, Pages 8203-8208

  Nickerson, Nicholas N ^a   Mainprize, Iain L ^a   Hampton, Lauren ^a   Jones, Michelle L ^a   Naismith, James H ^b   Whitfield, Chris ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; LIPOPROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG; WZA LIPOROTEIN;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIOPHAGE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; IMMUNOBLOTTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; BACTERIAL CAPSULES; BACTERIAL OUTER MEMBRANE PROTEINS; CROSS-LINKING REAGENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES, BACTERIAL; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84901819258     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1400341111     Document Type: Article

References (37)

1. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67(4):593-656.
2. Taylor CM, Roberts IS (2005) Capsular polysaccharides and their role in virulence. Contrib Microbiol 12:55-66.
3. Becker A, Fraysse N, Sharypova L (2005) Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol Plant Microbe Interact 18(9):899-905. (Pubitemid 41170154)
4. Flemming HC,Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623-633.
5. Sutherland IW (1998) Novel and established applications of microbial polysaccharides. Trends Biotechnol 16(1):41-46.
6. Whitfield C (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75:39-68.
7. Cuthbertson L, Mainprize IL, Naismith JH, Whitfield C (2009) 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(1):155-177.
8. Drummelsmith J, Whitfield C (1999) Gene products required for surface expression of the capsular form of the group 1 K antigen in Escherichia coli (O9a:K30). Mol Microbiol 31(5):1321-1332. (Pubitemid 29110092)
9. Nesper J, et al. (2003) Translocation of group 1 capsular polysaccharide in Escherichia coli serotype K30. Structural and functional analysis of the outer membrane lipoprotein Wza. J Biol Chem 278(50):49763-49772. (Pubitemid 37548809)
10. Reid AN, Whitfield C (2005) Functional analysis of conserved gene products involved in assembly of Escherichia coli capsules and exopolysaccharides: Evidence for molecular recognition between Wza and Wzc for colanic acid biosynthesis. J Bacteriol 187(15):5470-5481. (Pubitemid 41022965)
11. Collins RF, et al. (2006) Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J Biol Chem 281(4):2144-2150. (Pubitemid 43845804)
12. Collins RF, et al. (2007) 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(7):2390-2395. (Pubitemid 46391407)
13. Dong C, et al. (2006) Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444(7116):226-229. (Pubitemid 44722064)
14. Ford RC, et al. (2009) Structure-function relationships of the outer membrane translocon Wza investigated by cryo-electronmicroscopy andmutagenesis. J Struct Biol 166(2):172-182.
15. Kong L, et al. (2013) Single-molecule interrogation of a bacterial sugar transporter allows the discovery of an extracellular inhibitor. Nat Chem 5(8):651-659.
16. Drummelsmith J, Whitfield C (2000) Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J 19(1):57-66. (Pubitemid 30009225)
17. Wugeditsch T, et al. (2001) Phosphorylation of Wzc, a tyrosine autokinase, is essential for assembly of group 1 capsular polysaccharides in Escherichia coli. J Biol Chem 276(4):2361-2371.
18. Kauer JC, Erickson-Viitanen S, Wolfe HR, Jr., DeGrado WF (1986) p-Benzoyl-L-phenylalanine, a new photoreactive amino acid. Photolabeling of calmodulin with a synthetic calmodulin-binding peptide. J Biol Chem 261(23):10695-10700. (Pubitemid 17194853)
19. Chin JW, Martin AB, King DS, Wang L, Schultz PG (2002) Addition of a photo-crosslinking amino acid to the genetic code of Escherichiacoli. Proc Natl Acad Sci USA 99(17):11020-11024. (Pubitemid 34920872)
20. Xie J, Schultz PG (2006) A chemical toolkit for proteins - An expanded genetic code. Nat Rev Mol Cell Biol 7(10):775-782. (Pubitemid 44450461)
21. Wang L, Brock A, Herberich B, Schultz PG (2001) Expanding the genetic code of Escherichia coli. Science 292(5516):498-500. (Pubitemid 32335951)
22. Liu CC, Schultz PG (2010) Adding new chemistries to the genetic code. Annu Rev Biochem 79:413-444.
23. Mori H, Ito K (2006) Different modes of SecY-SecA interactions revealed by site-directed in vivo photo-cross-linking. Proc Natl Acad Sci USA 103(44):16159-16164. (Pubitemid 44715167)
24. Okuda S, Freinkman E, Kahne D (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338(6111): 1214- 1217.
25. Schnaitman CA, Austin EA (1990) Efficient incorporation of galactose into lipopolysaccharide by Escherichia coli K-12 strains with polar galE mutations. J Bacteriol 172(9):5511-5513. (Pubitemid 20282014)
26. Kos V, Cuthbertson L, Whitfield C (2009) The Klebsiella pneumoniae O2a antigen defines a second mechanism for O antigen ATP-binding cassette transporters. J Biol Chem 284(5):2947-2956.
27. Beis K, Nesper J, Whitfield C, Naismith JH (2004) Crystallization and preliminary X-ray diffraction analysis of Wza outer-membrane lipoprotein from Escherichia coli serotype O9a:K30. Acta Crystallogr D Biol Crystallogr 60(Pt 3):558-560. (Pubitemid 41087596)
28. Okuda S, Tokuda H (2009) Model of mouth-to-mouth transfer of bacterial lipoproteins through inner membrane LolC, periplasmic LolA, and outer membrane LolB. Proc Natl Acad Sci USA 106(14):5877-5882.
29. Götze M, et al. (2012) StavroX - A software for analyzing crosslinked products in protein interaction studies. J Am Soc Mass Spectrom 23(1):76-87.
30. Dormán G, Prestwich GD (1994) Benzophenone photophores in biochemistry. Biochemistry 33(19):5661-5673. (Pubitemid 24184566)
31. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Plainview, NY), 2nd Ed, p A.3.
32. Young TS, Ahmad I, Yin JA, Schultz PG (2010) An enhanced system for unnatural amino acid mutagenesis in E. coli. J Mol Biol 395(2):361-374.
33. Farrell IS, Toroney R, Hazen JL, Mehl RA, Chin JW (2005) Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat Methods 2(5): 377-384. (Pubitemid 41130984)
34. Chin JW, Schultz PG (2002) In vivo photocrosslinking with unnatural amino acid mutagenesis. ChemBioChem 3(11):1135-1137. (Pubitemid 36008045)
35. Filip C, Fletcher G, Wulff JL, Earhart CF (1973) Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J Bacteriol 115(3):717-722.
36. Whitfield C, Lam M(1986) Characterisation of coliphage K30, a bacteriophage specific for Escherichia coli capsular serotype K30. FEMS Microbiol Lett 37:351-355. (Pubitemid 17204775)
37. Gfeller D, Michielin O, Zoete V (2013) SwissSidechain: A molecular and structural database of non-natural sidechains. Nucleic Acids Res 41(Database issue): D327-D332.