Internalization of a thiazole-modified peptide in Sinorhizobium meliloti occurs by BacA-dependent and -independent mechanisms

References

1. Alunni B., Kevei Z., Redondo-Nieto M., Kondorosi A., Mergaert P., Kondorosi E. 2007; Genomic organisation and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. Mol Plant Microbe Interact 20:1138–1148
   [Google Scholar]
2. Aouida M., Leduc A., Wang H., Ramotar D. 2004; Characterization of a transport and detoxification pathway for the antitumour drug bleomycin in Saccharomyces cerevisiae. Biochem J 384:47–58
   [Google Scholar]
3. Aouida M., Leduc A., Poulin R., Ramotar D. 2005; AGP2 encodes the major permease for high affinity polyamine import in Saccharomyces cerevisiae. J Biol Chem 280:24267–24276
   [Google Scholar]
4. Benincasa M., Scocchi M., Podda E., Skerlavaj B., Dolzani L., Gennaro R. 2004; Antimicrobial activity of Bac7 fragments against drug-resistant clinical isolates. Peptides 25:2055–2061
   [Google Scholar]
5. Benincasa M., Pacor S., Gennaro R., Scocchi M. 2009; Rapid and reliable detection of antimicrobial peptide penetration into Gram-negative bacteria based on fluorescence quenching. Antimicrob Agents Chemother 53:3501–3504
   [Google Scholar]
6. Davidson A. L., Chen J. 2004; ATP-binding cassette transporters in bacteria. Annu Rev Biochem 73:241–268
   [Google Scholar]
7. Ditta G., Schmidhauser T., Yakobson E., Lu P., Liang X.-W., Finlay D. R., Guiney D., Helinski D. R. 1985; Plasmids related to the broad host range vector, pRK290, useful for gene cloning and for monitoring gene expression. Plasmid 13:149–153
   [Google Scholar]
8. Domenech P., Kobayashi H., Levier K., Walker G. C., Barry C. E. III 2009; BacA: an ABC transporter involved in maintenance of chronic murine infections with Mycobacterium tuberculosis. J Bacteriol 191:477–485
   [Google Scholar]
9. Ferguson G. P., Battista J. R., Lee A. T., Booth I. R. 2000; Protection of the DNA during the exposure of Escherichia coli cells to a toxic metabolite: the role of the KefB and KefC potassium channels. Mol Microbiol 35:113–122
   [Google Scholar]
10. Ferguson G. P., Roop R. M. II, Walker G. C. 2002; Deficiency of Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of cell envelope. J Bacteriol 184:5625–5632
    [Google Scholar]
11. Ferguson G. P., Datta A., Baumgartner J., Roop R. M. II, Carlson R. W., Walker G. C. 2004; Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci U S A 101:5012–5017
    [Google Scholar]
12. Ferguson G. P., Datta A., Carlson R. W., Walker G. C. 2005; Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol Microbiol 56:68–80
    [Google Scholar]
13. Ferguson G. P., Jansen A., Marlow V. L., Walker G. C. 2006; BacA-mediated bleomycin sensitivity in Sinorhizobium meliloti is independent of the unusual lipid A modification. J Bacteriol 188:3143–3148
    [Google Scholar]
14. Finan T. M., Kunkel B., de Vos G. F., Signer E. R. 1986; Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167:66–72
    [Google Scholar]
15. Frank R. W., Gennaro R., Schneider K., Przybylski M., Romeo D. 1990; Amino acid sequences of two proline-rich bactenecins. Antimicrobial peptides of bovine neutrophils. J Biol Chem 265:18871–18874
    [Google Scholar]
16. Franz D. R., Jahrling P. B., Friedlander A. M., McClain D. J., Hoover D. L., Bryne W. R., Pavlin J. A., Christopher G. W., Eitzen E. M. Jr 1997; Clinical recognition and management of patients exposed to biological warfare agents. JAMA 278:399–411
    [Google Scholar]
17. Galibert F., Finan T. M., Long S. R., Puhler A., Abola P., Ampe F., Barloy-Hubler F., Barnett M. J., Becker A. other authors 2001; The composite genome of the legume symbiont Sinorhizobium meliloti. Science 293:668–672
    [Google Scholar]
18. Gennaro R., Zanetti M., Benincasa M., Podda E., Miani M. 2002; Pro-rich antimicrobial peptides from animals: structure, biological functions and mechanism of action. Curr Pharm Des 8:763–778
    [Google Scholar]
19. Gibson K. E., Kobayashi H., Walker G. C. 2008; Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42:413–441
    [Google Scholar]
20. Glazebrook J., Ichige A., Walker G. C. 1993; A Rhizobium meliloti homolog of the Escherichia coli peptide-antibiotic transport protein SbmA is essential for bacteroid development. Genes Dev 7:1485–1497
    [Google Scholar]
21. Grzesiuk E., Janion C. 1996; MMS-induced mutagenesis and DNA repair in Escherichia coli dnaQ49: contribution of UmuD′ to DNA repair. Mutat Res 362:147–154
    [Google Scholar]
22. Haag A. F., Wehmeier S., Beck S., Marlow V. L., Fletcher V., James E. K., Ferguson G. P. 2009; The Sinorhizobium meliloti LpxXL and AcpXL proteins play important roles in bacteroid development within alfalfa. J Bacteriol 191:4681–4686
    [Google Scholar]
23. Ichige A., Walker G. C. 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
    [Google Scholar]
24. Igarashi K., Kashiwagi K. 1999; Polyamine transport in bacteria and yeast. Biochem J 344:633–642
    [Google Scholar]
25. Imlay J. A., Linn S. 1988; DNA damage and oxygen radical toxicity. Science 240:1302–1309
    [Google Scholar]
26. Johnson J. L. 1994; Similarity analysis of DNAs. In Methods for General and Molecular Bacteriology pp 655–682 Edited by Gerhardt P., Murray R. G. E., Wood W. A., Kreig N. R. Washington, DC: American Society of Microbiology;
    [Google Scholar]
27. Jones K. M., Kobayashi H., Davies B. W., Taga M. E., Walker G. C. 2007; How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat Rev Microbiol 5:619–633
    [Google Scholar]
28. Kane S. A., Hecht S. M. 1994; Polynucleotide recognition and degradation by bleomycin. Prog Nucleic Acid Res Mol Biol 49:313–352
    [Google Scholar]
29. Laviña M., Pugsley A. P., 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
    [Google Scholar]
30. Leigh J. A., Signer E. R., Walker G. C. 1985; Exopolysaccharide-deficient mutants of Rhizobium meliloti that form ineffective nodules. Proc Natl Acad Sci U S A 82:6231–6235
    [Google Scholar]
31. LeVier K., Walker G. C. 2001; Genetic analysis of the Sinorhizobium meliloti BacA protein: differential effects of mutations on phenotypes. J Bacteriol 183:6444–6453
    [Google Scholar]
32. LeVier K., Phillips R. W., Grippe V. K., Roop R. M. II, Walker G. C. 2000; Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492–2493
    [Google Scholar]
33. Lim S. T., Jue C. K., Moore C. W., Lipke P. N. 1995; Oxidative cell wall damage mediated by bleomycin-Fe(II) in Saccharomyces cerevisiae. J Bacteriol 177:3534–3539
    [Google Scholar]
34. Marlow V. L., Haag A. F., Kobayashi H., Fletcher V., Scocchi M., Walker G. C., Ferguson G. P. 2009; Essential role for the BacA protein in the uptake of a truncated eukaryotic peptide in Sinorhizobium meliloti. J Bacteriol 191:1519–1527
    [Google Scholar]
35. 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
    [Google Scholar]
36. McLaughlin S. 1972; The mechanism of action of DNP on phospholipid bilayer membranes. J Membr Biol 9:361–372
    [Google Scholar]
37. Meade H. M., Long S. R., Ruvkun G. B., Brown S. E., Ausubel F. M. 1982; Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn 5 mutagenesis. J Bacteriol 149:114–122
    [Google Scholar]
38. Mergaert P., Nikovics K., Keleman Z., Maunoury N., Vaubert D., Kondorosi A., Kondorosi E. 2003; A novel family of Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 132:161–173
    [Google Scholar]
39. Mergaert P., Uchiumi T., Alunni B., Evanno G., Cheron A., Catrice O., Mausett A. E., Barloy-Hubler F., Galibert F. other authors 2006; Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium–legume symbiosis. Proc Natl Acad Sci U S A 103:5230–5235
    [Google Scholar]
40. Otsuji N., Murayama I. 1972; Deoxyribonucleic acid damage by monofunctional mitomycins and its repair in Escherichia coli. J Bacteriol 109:475–483
    [Google Scholar]
41. Pedreno E., Lopez-Contreras A. J., Cremades A., Penafiel R. 2005; Protecting or promoting effects of spermine on DNA strand breakage induced by iron or copper ions as a function of metal concentration. J Inorg Biochem 99:2074–2080
    [Google Scholar]
42. Raetz C. R., Whitfield C. 2002; Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635–700
    [Google Scholar]
43. Rivas-Santiago B., Serrano C. J., Enciso-Moreno J. A. 2009; Susceptibility to infectious diseases based on antimicrobial peptide production. Infect Immun 77:4690–4695
    [Google Scholar]
44. Sambrook J., Fritsch E. F., Maniatis T. 1982 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
45. 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
    [Google Scholar]
46. Sharypova L. A., Niehaus K., Scheidle H., Holst O., Becker A. 2003; Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide. J Biol Chem 278:12946–12954
    [Google Scholar]
47. Umezawa H., Maeda K., Takeuchi T., Okami Y. 1966; New antibiotics, bleomycin A and B. J Antibiot (Tokyo 19:200–209
    [Google Scholar]
48. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A. other authors 2010; Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327:1122–1126
    [Google Scholar]
49. Wells D. H., Long S. R. 2002; The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis. Mol Microbiol 43:1115–1127
    [Google Scholar]
50. Wilson K. 1987; Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology pp 2.4.1–2.4.5 Edited by Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. New York: Green Publishing & Wiley-Interscience;
    [Google Scholar]
51. 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
    [Google Scholar]