MacA, a periplasmic membrane fusion protein of the macrolide transporter MacAB-TolC, binds lipopolysaccharide core specifically and with high affinity

Journal of Bacteriology

Volumn 195, Issue 21, 2013, Pages 4865-4872

  Lu, Shuo ^a   Zgurskaya, Helen I ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; LIPOPOLYSACCHARIDE; MACA PROTEIN; MACROLIDE; MEMBRANE FUSION PROTEIN; POLYMYXIN B; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CYTOPLASM; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; SUBSTITUTION REACTION;

ATP-BINDING CASSETTE TRANSPORTERS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPOLYSACCHARIDES; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 84886032478     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00756-13     Document Type: Article

References (31)

1. Nikaido H. 2009. Multidrug resistance in bacteria. Annu. Rev. Biochem. 78:119-146.
2. Nikaido H, Zgurskaya HI. 2001. Acrab and related multidrug efflux pumps of Escherichia coli. J. Mol. Microbiol. Biotechnol. 3:215-218.
3. Nishino K, Nikaido E, Yamaguchi A. 2009. Regulation and physiological function of multidrug efflux pumps in Escherichia coli and Salmonella. Biochim. Biophys. Acta 1794:834-843.
4. Zgurskaya HI. 2009. Multicomponent drug efflux complexes: architecture and mechanism of assembly. Future Microbiol. 4:919-932.
5. Kobayashi N, Nishino K, Yamaguchi A. 2001. Novel macrolide-specific abc-type efflux transporter in Escherichia coli. J. Bacteriol. 183:5639-5644.
6. Tikhonova EB, Devroy VK, Lau SY, Zgurskaya HI. 2007. Reconstitution of the Escherichia coli macrolide transporter: the periplasmic membrane fusion protein MacA stimulates the ATPase activity of MacB. Mol. Microbiol. 63:895-910.
7. Guisbert E, Yura T, Rhodius VA, Gross CA. 2008. Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol. Mol. Biol. Rev. 72:545-554.
8. Nishino K, Latifi T, Groisman EA. 2006. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 59:126-141.
9. Modali SD, Zgurskaya HI. 2011. The periplasmic membrane proximal domain of MacA acts as a switch in stimulation of ATP hydrolysis by MacB transporter. Mol. Microbiol. 81:937-951.
10. Yamanaka H, Kobayashi H, Takahashi E, Okamoto K. 2008. MacAB is involved in the secretion of Escherichia coli heat-stable enterotoxin ii. J. Bacteriol. 190:7693-7698.
11. Kobayashi R, Suzuki T, Yoshida M. 2007. Escherichia coli phage-shock protein a (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66:100-109.
12. Wade JT, Roa DC, Grainger DC, Hurd D, Busby SJ, Struhl K, Nudler E. 2006. Extensive functional overlap between sigma factors in Escherichia coli. Nat. Struct. Mol. Biol. 13:806-814.
13. Murray SR, Bermudes D, de Felipe KS, Low KB. 2001. Extragenic suppressors of growth defects in MsbB Salmonella. J. Bacteriol. 183:5554-5561.
14. Lesse AJ, Campagnari AA, Bittner WE, Apicella MA. 1990. Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J. Immunol. Methods 126:109-117.
15. Schagger H, von Jagow G. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
16. Weissbach A, Hurwitz J. 1959. The formation of 2-keto-3-deoxyheptonic acid in extracts of Escherichia coli b. I. Identification. J. Biol. Chem. 234: 705-709.
17. Tikhonova EB, Wang Q, Zgurskaya HI. 2002. Chimeric analysis of the multicomponent multidrug efflux transporters from gram-negative bacteria. J. Bacteriol. 184:6499-6507.
18. Tikhonova EB, Zgurskaya HI. 2004. AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J. Biol. Chem. 279:32116-32124.
19. Stevenson G, Neal B, Liu D, Hobbs M, Packer NH, Batley M, Redmond JW, Lindquist L, Reeves P. 1994. Structure of the o antigen of Escherichia coli k-12 and the sequence of its rfb gene cluster. J. Bacteriol. 176:4144-4156.
20. Imperi F, Tiburzi F, Visca P. 2009. Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 106:20440-20445.
21. Ferguson AD. Welte W, Hofmann E, Lindner B, Holst O, Coulton JW, Diederichs K. 2000. A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Structure 8:585-592.
22. Lu S, Zgurskaya HI. 2012. Role of ATP binding and hydrolysis in assembly of MacAB-TolC macrolide transporter. Mol. Microbiol. 86:1132-1143.
23. Yum S, Xu Y, Piao S, Sim SH, Kim HM, Jo WS, Kim KJ, Kweon HS, Jeong MH, Jeon H, Lee K, Ha NC. 2009. Crystal structure of the periplasmic component of a tripartite macrolide-specific efflux pump. J. Mol. Biol. 387:1286-1297.
24. Mikolosko J, Bobyk K, Zgurskaya HI, Ghosh P. 2006. Conformational flexibility in the multidrug efflux system protein AcrA. Structure 14:577-587.
25. Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V. 2009. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc. Natl. Acad. Sci. U. S. A. 106:7173-7178.
26. De Angelis F, Lee JK, O'Connell JD, Miercke LJW, Verschueren KH, Srinivasan V, Bauvois C, Govaerts C, Robbins RA, Ruysschaert J-M, Stroud RM, Vandenbussche G. 2010. Metal-induced conformational changes in ZneB suggest an active role of membrane fusion proteins in efflux resistance systems. Proc. Natl. Acad. Sci. U. S. A. 107:11038-11043.
27. Su CC, Yang F, Long F, Reyon D, Routh MD, Kuo DW, Mokhtari AK, Van Ornam JD, Rabe KL, Hoy JA, Lee YJ, Rajashankar KR, Yu EW. 2009. Crystal structure of the membrane fusion protein CusB from Escherichia coli. J. Mol. Biol. 393:342-355.
28. Silhavy TJ, Kahne D, Walker S. 2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:a000414. doi:10.1101/cshperspect.a000414.
29. Woebking B, Reuter G, Shilling RA, Velamakanni S, Shahi S, Venter H, Balakrishnan L, van Veen HW. 2005. Drug-lipid a interactions on the Escherichia coli abc transporter MsbA. J. Bacteriol. 187:6363-6369.
30. Balakrishnan L, Hughes C, Koronakis V. 2001. Substrate-triggered recruitment of the TolC channel-tunnel during type I export of hemolysin by Escherichia coli. J. Mol. Biol. 313:501-510.
31. Pimenta AL, Racher K, Jamieson L, Blight MA, Holland IB. 2005. Mutations in HlyD, part of the type 1 translocator for hemolysin secretion, affect the folding of the secreted toxin. J. Bacteriol. 187:7471-7480.