Functional characterization of SbmA, a bacterial inner membrane transporter required for importing the antimicrobial peptide Bac7(1-35)

Journal of Bacteriology

Volumn 195, Issue 23, 2013, Pages 5343-5351

  Runti, Giulia ^a   Lopez Ruiz, Maria del Carmen ^b,c,d   Stoilova, Tatiana ^a   Hussain, Rohanah ^e   Jennions, Matthew ^b,c,d   Choudhury, Hassanul G ^b,c,d   Benincasa, Monica ^a   Gennaro, Renato ^a   Beis, Konstantinos ^b,c,d   Scocchi, Marco ^a  

^a UNIVERSITY OF TRIESTE   (Italy)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c Harwell Science and Innovation Campus   (United Kingdom)

^d RUTHERFORD APPLETON LABORATORY   (United Kingdom)

^e DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL PEPTIDE BAC7(1-35); ARSENIC ACID; BACTERIAL PROTEIN; GLYCOPEPTIDE; HOMODIMER; IONOPHORE; MEMBRANE PROTEIN; OLIGOMER; PEPTIDE NUCLEIC ACID; POLYPEPTIDE ANTIBIOTIC AGENT; PROLINE; PROTEIN BACA; PROTEIN SBMA; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; ARTICLE; BRUCELLA ABORTUS; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTROCHEMISTRY; GRAM NEGATIVE BACTERIUM; INTERNALIZATION; LIGHT SCATTERING; MULTIANGLE LASER LIGHT SCATTERING; MYCOBACTERIUM TUBERCULOSIS; PLANT CELL; PRIORITY JOURNAL; PROTEIN TRANSPORT; SINORHIZOBIUM MELILOTI; TWO HYBRID SYSTEM;

ADENOSINE TRIPHOSPHATE; ANTIMICROBIAL CATIONIC PEPTIDES; CIRCULAR DICHROISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE TRANSPORT PROTEINS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN BINDING; PROTONS; RECOMBINANT FUSION PROTEINS;

EID: 84887512140     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00818-13     Document Type: Article

References (38)

1. Glazebrook J, Ichige A, Walker GC. 1993. A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev. 7:1485-1497.
2. LeVier K, Phillips RW, Grippe VK, Roop RM, II, Walker GC. 2000. Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492-2493.
3. Domenech P, Kobayashi H, LeVier K, Walker GC, Barry CE, III. 2009. BacA, an ABC transporter involved in maintenance of chronic murine infections with Mycobacterium tuberculosis. J. Bacteriol. 191:477-485.
4. Salomon RA, Farias RN. 1995. The peptide antibiotic microcin 25 is imported through the TonB pathway and the SbmA protein. J. Bacteriol. 177:3323-3325.
5. Mattiuzzo M, Bandiera A, Gennaro R, Benincasa M, Pacor S, Antcheva N, Scocchi M. 2007. Role of the Escherichia coli SbmA in the antimicrobial activity of proline-rich peptides. Mol. Microbiol. 66:151-163.
6. Marlow VL, Haag AF, Kobayashi H, Fletcher V, Scocchi M, Walker GC, Ferguson GP. 2009. Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J. Bacteriol. 191:1519-1527.
7. Ichige A, Walker GC. 1997. Genetic analysis of the Rhizobium meliloti bacA gene: functional interchangeability with the Escherichia coli sbmA gene and phenotypes of mutants. J. Bacteriol. 179:209-216.
8. Wehmeier S, Arnold MF, Marlow VL, Aouida M, Myka KK, Fletcher V, Benincasa M, Scocchi M, Ramotar D, Ferguson GP. 2010. Internalization of a thiazole-modified peptide in Sinorhizobium meliloti occurs by BacA-dependent and -independent mechanisms. Microbiology 156:2702-2713.
9. Yorgey P, Lee J, Kordel J, Vivas E, Warner P, Jebaratnam D, Kolter R. 1994. Posttranslational modifications in microcin B17 define an additional class of DNA gyrase inhibitor. Proc. Natl. Acad. Sci. U.S.A. 91:4519-4523.
10. LeVier K, Walker GC. 2001. Genetic analysis of the Sinorhizobium meliloti BacA protein: differential effects of mutations on phenotypes. J. Bacteriol. 183:6444-6453.
11. Lavina M, Pugsley AP, Moreno F. 1986. Identification, mapping, cloning and characterization of a gene (sbmA) required for microcin B17 action on Escherichia coli K12. J. Gen. Microbiol. 132:1685-1693.
12. Pranting M, Negrea A, Rhen M, Andersson DI. 2008. Mechanism and fitness costs of PR-39 resistance in Salmonella enterica serovar Typhimurium LT2. Antimicrob. Agents Chemother. 52:2734-2741.
13. Puckett SE, Reese KA, Mitev GM, Mullen V, Johnson RC, Pomraning KR, Mellbye BL, Tilley LD, Iversen PL, Freitag M, Geller BL. 2012. Bacterial resistance to antisense peptide phosphorodiamidate morpholino oligomers. Antimicrob. Agents Chemother. 56:6147-6153.
14. Ghosal A, Vitali A, Stach JE, Nielsen PE. 2013. Role of SbmA in the uptake of peptide nucleic acid (PNA)-peptide conjugates in E. coli. ACS Chem. Biol. 8:360-367.
15. Haag AF, Baloban M, Sani M, Kerscher B, Pierre O, Farkas A, Longhi R, Boncompagni E, Herouart D, Dall'angelo S, Kondorosi E, Zanda M, Mergaert P, Ferguson GP. 2011. Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biol. 9:e1001169. doi:10.1371/journal.pbio.1001169.
16. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, Satiat-Jeunemaitre B, Alunni B, Bourge M, Kucho K, Abe M, Kereszt A, Maroti G, Uchiumi T, Kondorosi E, Mergaert P. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122-1126.
17. Arnold MF, Haag AF, Capewell S, Boshoff HI, James EK, McDonald R, Mair I, Mitchell AM, Kerscher B, Mitchell TJ, Mergaert P, Barry CE, III, Scocchi M, Zanda M, Campopiano DJ, Ferguson GP. 2013. Partial complementation of Sinorhizobium meliloti bacA mutant phenotypes by the Mycobacterium tuberculosis BacA protein. J. Bacteriol. 195:389-398.
18. Davidson AL, Chen J. 2004. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73:241-268.
19. Scocchi M, Mattiuzzo M, Benincasa M, Antcheva N, Tossi A, Gennaro R. 2008. Investigating the mode of action of proline-rich antimicrobial peptides using a genetic approach: a tool to identify new bacterial targets amenable to the design of novel antibiotics. Methods Mol. Biol. 494:161-176.
20. Drew D, Lerch M, Kunji E, Slotboom DJ, de Gier JW. 2006. Optimization of membrane protein overexpression and purification using GFP fusions. Nat. Methods 3:303-313.
21. Miller JH (ed). 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
22. Griffith KL, Wolf RE, Jr. 2002. Measuring beta-galactosidase activity in bacteria: cell growth, permeabilization, and enzyme assays in 96-well arrays. Biochem. Biophys. Res. Commun. 290:397-402.
23. Javorfi T, Hussain R, Myatt D, Siligardi G. 2010. Measuring circular dichroism in a capillary cell using the b23 synchrotron radiation CD beamline at diamond light source. Chirality 22(Suppl 1):E149-E153.
24. Siligardi G, Panaretou B, Meyer P, Singh S, Woolfson DN, Piper PW, Pearl LH, Prodromou C. 2002. Regulation of Hsp90 ATPase activity by the co-chaperone Cdc37p/p50cdc37. J. Biol. Chem. 277:20151-20159.
25. Cascales E, Gavioli M, Sturgis JN, Lloubes R. 2000. Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol. Microbiol. 38:904-915.
26. Karimova G, Pidoux J, Ullmann A, Ladant D. 1998. A bacterial twohybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U.S.A. 95:5752-5756.
27. Slotboom DJ, Duurkens RH, Olieman K, Erkens GB. 2008. Static light scattering to characterize membrane proteins in detergent solution. Methods 46:73-82.
28. Putman M, van Veen HW, Konings WN. 2000. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 64:672-693.
29. Paulsen IT, Brown MH, Skurray RA. 1996. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60:575-608.
30. Venter H, Shilling RA, Velamakanni S, Balakrishnan L, Van Veen HW. 2003. An ABC transporter with a secondary-active multidrug translocator domain. Nature 426:866-870.
31. Kuroda M, Dey S, Sanders OI, Rosen BP. 1997. Alternate energy coupling of ArsB, the membrane subunit of the Ars anion-translocating ATPase. J. Biol. Chem. 272:326-331.
32. Corbalan N, Runti G, Adler C, Covaceuszach S, Ford RC, Lamba D, Beis K, Scocchi M, Vincent PA. 2013. Functional and structural study of the dimeric inner membrane protein SbmA. J. Bacteriol. 195:5352-5361.
33. Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G. 2005. Global topology analysis of the Escherichia coli inner membrane proteome. Science 308:1321-1323.
34. Detmers FJ, Kunji ER, Lanfermeijer FC, Poolman B, Konings WN. 1998. Kinetics and specificity of peptide uptake by the oligopeptide transport system of Lactococcus lactis. Biochemistry 37:16671-16679.
35. Miroux B, Walker JE. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260:289-298.
36. Provencher SW, Glockner J. 1981. Estimation of globular protein secondary structure from circular dichroism. Biochemistry 20:33-37.
37. Sreerama N, Woody RW. 2000. Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287:252-260.
38. van Stokkum IH, Spoelder HJ, Bloemendal M, van Grondelle R, Groen FC. 1990. Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal. Biochem. 191:110-118.