Acyl carrier protein is a bacterial cytoplasmic target of cationic antimicrobial peptide LL-37

Biochemical Journal

Volumn 470, Issue 2, 2015, Pages 243-253

  Chung, Myung Chul ^a   Dean, Scott N ^a   Van Hoek, Monique L ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

Acyl carrier protein; Antimicrobial peptide; Cathelicidin; Drug target; Francisella

Indexed keywords

ACYL CARRIER PROTEIN; CATHELICIDIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CYTOPLASM PROTEIN; SHEEP MYELOID ANTIMICROBIAL PEPTIDE 29; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; FATTY ACID; PROTEIN BINDING;

ACPP GENE; ALPHA HELIX; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GENE; BIOTINYLATION; CONTROLLED STUDY; DIFFERENTIAL SCANNING FLUORIMETRY; DRUG MECHANISM; DRUG TARGETING; ESCHERICHIA COLI; FLUOROMETRY; FRANCISELLA NOVICIDA; GENE OVEREXPRESSION; INNER MEMBRANE; LIPID COMPOSITION; LIQUID CHROMATOGRAPHY; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CYTOPLASM; DRUG EFFECTS; FRANCISELLA; METABOLISM; MOLECULAR GENETICS;

ACYL CARRIER PROTEIN; AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; CYTOPLASM; FATTY ACIDS; FRANCISELLA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING;

EID: 84940378367     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150432     Document Type: Article

References (56)

1. Pieters, R.J., Arnusch, C.J. and Breukink, E. (2009) Membrane permeabilization by multivalent anti-microbial peptides. Protein Pept. Lett. 16, 736-742 CrossRef PubMed
2. Nicias, P. (2009) Multifunctional host defense peptides: intracellular-targeting antimicrobial peptides. FEBS J 276, 6483-6496 CrossRef PubMed
3. Chan, D.I., Prenner, E.J. and Vogel, H.J. (2006) Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim. Biophys. Acta 1758, 1184-1202 CrossRef PubMed
4. Dean, S.N., Bishop, B.M. and van Hoek, M.L. (2011) Susceptibility of Pseudomonas aeruginosa biofilm to alpha-helical peptides: D-enantiomer of LL-37. Front. Microbiol. 2: 128. CrossRef PubMed
5. Dean, S.N., Bishop, B.M. and van Hoek, M.L. (2011) Natural and synthetic cathelicidin peptides with anti-microbial and anti-biofilm activity against Staphylococcus aureus. BMC Microbiol. 11, 114 CrossRef PubMed
6. Giuliani, A., Pirri, G. and Rinaldi, A.C. (2010) Antimicrobial peptides: the LPS connection. Methods Mol. Biol. 618, 137-154 CrossRef PubMed
7. Sochacki, K.A., Barns, K.J., Bucki, R. and Weisshaar, J.C. (2011) Real-time attack on single Escherichia coli cells by the human antimicrobial peptide LL-37. Proc. Natl. Acad. Sci. U.S.A. 108, E77-E81 CrossRef PubMed
8. Shelton, C.L., Raffel, F.K., Beatty, W.L., Johnson, S.M. and Mason, K.M. (2011) Sap transporter mediated import and subsequent degradation of antimicrobial peptides in Haemophilus. PLoS Pathog. 7, e1002360 CrossRef PubMed
9. Duplantier, A.J. and van Hoek, M.L. (2013) The human cathelicidin antimicrobial peptide LL-37 as a potential treatment for polymicrobial infected wounds. Front. Immunol. 4, 143 CrossRef PubMed
10. Lee, C.C., Sun, Y., Qian, S. and Huang, H.W. (2011) Transmembrane pores formed by human antimicrobial peptide LL-37. Biophys. J. 100, 1688-1696 CrossRef PubMed
11. Sood, R., Domanov, Y., Pietiäinen, M., Kontinen, V.P. and Kinnunen, P.K. (2008) Binding of LL-37 to model biomembranes: insight into target vs host cell recognition. Biochim. Biophys. Acta 1778, 983-996 CrossRef PubMed
12. De la Fuente-Núñez, C, Reffuveille, F., Haney, E.F., Straus, S.K. and Hancock, R.E.W. (2014) Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 10, e1004152 CrossRef PubMed
13. Limoli, D.H., Rockel, A.B., Host, K.M., Jha, A., Kopp, B.T., Hollis, T. and Wozniak, D.J. (2014) Cationic antimicrobial peptides promote microbial mutagenesis and pathoadaptation in chronic infections. PLoS Pathog 10, e1004083 CrossRef PubMed
14. Mookherjee, N., Lippert, D.N.D., Hamill, P., Falsafi, R., Nijnik, A., Kindrachuk, J., Pistolic, J., Gardy, J., Miri, P., Naseer, M. et al. (2009) Intracellular receptor for human host defense peptide LL-37 in monocytes. J. Immunol. 183, 2688-2696 CrossRef PubMed
15. Zhang, Y. and Cronan, J.E. (1996) Polar allele duplication for transcriptional analysis of consecutive essential genes: application to a cluster of Escherichia coli fatty acid biosynthetic genes. J. Bacteriol. 178, 3614-3620 PubMed
16. Good, L., Awasthi, S.K., Dryselius, R., Larsson, O. and Nielsen, P.E. (2001) Bactericidal antisense effects of peptide-PNA conjugates. Nat. Biotechnol. 19, 360-364 CrossRef PubMed
17. Maier, T.M., Havig, A., Casey, M., Nano, F.E., Frank, D.W. and Zahrt, T.C. (2004) Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl. Environ. Microbiol. 70, 7511-7519 CrossRef PubMed
18. Chung, M.C., Popova, T.G., Millis, B.A., Mukherjee, D.V., Zhou, W., Liotta, L.A., Petricoin, E.F., Chandhoke, V., Bailey, C. and Popov, S.G. (2006) Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J. Biol. Chem. 281, 31408-31418 CrossRef PubMed
19. Pierson, T., Matrakas, D., Taylor, Y. U., Manyam, G., Morozov, V.N., Zhou, W. and van Hoek, M.L. (2010) Proteomic characterization and functional analysis of outer membrane vesicles of Francisella novicida suggests possible role in virulence and use as a vaccine. J. Proteome Res. 10, 954-967 CrossRef
20. Niesen, F.H., Berglund, H. and Vedadi, M. (2007) The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2, 2212-2221 CrossRef PubMed
21. Mohapatra, N.P., Soni, S., Bell, B.L., Warren, R., Ernst, R.K., Muszynski, A., Carlson, R.W. and Gunn, J. S. (2007) Identification of an orphan response regulator required for the virulence of Francisella spp. and transcription of pathogenicity island genes. Infect. Immun. 75, 3305-3314 CrossRef PubMed
22. Amer, L.S., Bishop, B.M. and van Hoek, M.L. (2010) Antimicrobial and antibiofilm activity of cathelicidins and short, synthetic peptides against Francisella . Biochem. Biophys. Res. Commun. 396, 246-251 CrossRef PubMed
23. Gaudy, A.F., Abu-Niaaj, F. and Gaudy, E.T. (1963) Statistical study of the spot-plate technique for viable-cell counts. Appl. Microbiol. 11, 305-309 PubMed
24. Epand, R.M. and Vogel, H.J. (1999) Diversity of antimicrobial peptides and their mechanisms of action. Biochim. Biophys. Acta 1462, 11-28 CrossRef PubMed
25. Peterson, A.A., Fesik, S.W. and McGroarty, E.J. (1987) Decreased binding of antibiotics to lipopolysaccharides from polymyxin-resistant strains of Escherichia coli and Salmonella typhimurium. Antimicrob. Agents Chemother. 31, 230-237 CrossRef PubMed
26. Worsham, L., Tucker, M. and Ernst-Fonberg, M. (1990) Behavior of acyl carrier proteins on western blots. Biochim. Biophys. Acta 1043, 198-202 CrossRef PubMed
27. Moreau, M.J., Morin, I., Askin, S.P., Cooper, A., Moreland, N.J., Vasudevan, S.G. and Schaeffer, P.M. (2012) Rapid determination of protein stability and ligand binding by differential scanning fluorimetry of GFP-tagged proteins. RSC Adv 2, 11892-11900 CrossRef
28. Martinez Molina, D., Jafari, R., Ignatushchenko, M., Seki, T., Larsson, E.A., Dan, C., Sreekumar, L., Cao, Y. and Nordlund, P. (2013) Monitoring drug target engagement in cells and tissues using the cellular thermal shift assay. Science 341, 84-87 CrossRef PubMed
29. Chan, D.I. and Vogel, H.J. (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem. J. 430, 1-19 CrossRef PubMed
30. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 CrossRef PubMed
31. Macindoe, G., Mavridis, L., Venkatraman, V., Devignes, M.D. and Ritchie, D.W. (2010) HexServer: an FFT-based protein docking server powered by graphics processors. Nucleic Acids Res 38, W445-W449 CrossRef PubMed
32. Crosby, J., Sherman, D.H., Bibb, M.J., Revill, W.P., Hopwood, D.A. and Simpson, T.J. (1995) Polyketide synthase acyl carrier proteins from Streptomyces: expression in Escherichia coli, purification and partial characterization. Biochim. Biophys. Acta 1251, 32-42 CrossRef PubMed
33. Rock, C.O. and Cronan, J.E. (1996) Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim. Biophys. Acta 1302, 1-16 CrossRef PubMed
34. Smith, S. (1994) The animal fatty acid synthase: one gene, one polypeptide, seven enzymes. FASEB J 8, 1248-1259 PubMed
35. Xu, H.H., Real, L. and Bailey, M.W. (2006) An array of Escherichia coli clones over-expressing essential proteins: a new strategy of identifying cellular targets of potent antibacterial compounds. Biochem. Biophys. Res. Commun. 349, 1250-1257 CrossRef PubMed
36. Chopra, I. (1998) Over-expression of target genes as a mechanism of antibiotic resistance in bacteria. J. Antimicrob. Chemother. 41, 584-588 CrossRef PubMed
37. Ojcius, D.M. and Young, J.D. (1991) Cytolytic pore-forming proteins and peptides: is there a common structural motif? Trends Biochem. Sci 16, 225-229 CrossRef PubMed
38. Brogden, K.A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250 CrossRef PubMed
39. Lin, Y.M., Wu, S.J., Chang, T.W., Wang, C.F., Suen, C.S., Hwang, M.J., Chang, M.D., Chen, Y.T. and Liao, Y.D. (2010) Outer membrane protein I of Pseudomonas aeruginosa is a target of cationic antimicrobial peptide/protein. J. Biol. Chem. 285, 8985-8994 CrossRef PubMed
40. Chang, T.W., Lin, Y.M., Wang, C.F. and Liao, Y.D. (2012) Outer membrane lipoprotein Lpp is Gram-negative bacterial cell surface receptor for cationic antimicrobial peptides. J. Biol. Chem. 287, 418-428 CrossRef PubMed
41. Pag, U., Oedenkoven, M., Sass, V., Shai, Y., Shamova, O., Antcheva, N., Tossi, A. and Sahl, H.G. (2008) Analysis of in vitro activities and modes of action of synthetic antimicrobial peptides derived from an alpha-helical "sequence template.". J. Antimicrob. Chemother. 61, 341-352 CrossRef PubMed
42. Tomasinsig, L. and Zanetti, M. (2005) Protein Pept. Sci. 6, 23-34 CrossRef
43. Geller, B.L., Deere, J.D., Stein, D.A., Kroeker, A.D., Moulton, H.M. and Iversen, P.L. (2003) Inhibition of gene expression in Escherichia coli by antisense phosphorodiamidate morpholino oligomers. Antimicrob. Agents Chemother. 47, 3233-3239 CrossRef PubMed
44. Geller, B.L., Marshall-Batty, K., Schnell, F.J., McKnight, M.M., Iversen, P.L. and Greenberg, D.E. (2013) Gene-silencing antisense oligomers inhibit acinetobacter growth in vitro and in vivo. J. Infect. Dis. 208, 1553-1560 CrossRef PubMed
45. Ghosal, A. and Nielsen, P.E. (2012) Potent antibacterial antisense peptide-peptide nucleic acid conjugates against Pseudomonas aeruginosa . Nucleic Acid Ther. 22, 323-334 PubMed
46. Rajasekaran, P., Alexander, J.C., Seleem, M.N., Jain, N., Sriranganathan, N., Wattam, A.R., Setubal, J.C. and Boyle, S.M. (2013) Peptide nucleic acids inhibit growth of Brucella suis in pure culture and in infected murine macrophages. Int. J. Antimicrob. Agents 41, 358-362 CrossRef PubMed
47. Mitev, G.M., Mellbye, B.L., Iversen, P.L. and Geller, B.L. (2009) Inhibition of intracellular growth of Salmonella enterica serovar Typhimurium in tissue culture by antisense peptide-phosphorodiamidate morpholino oligomer. Antimicrob. Agents Chemother. 53, 3700-3704 CrossRef PubMed
48. Zornetzer, G.A., Tanem, J., Fox, B.G. and Markley, J.L. (2010) The length of the bound fatty acid influences the dynamics of the acyl carrier protein and the stability of the thioester bond. Biochemistry 49, 470-477 CrossRef PubMed
49. Roujeinikova, A., Baldock, C., Simon, W.J., Gilroy, J., Baker, P.J., Stuitje, A.R., Rice, D.W., Slabas, A.R. and Rafferty, J.B. (2002) X-ray crystallographic studies on butyryl-ACP reveal flexibility of the structure around a putative acyl chain binding site. Structure 10, 825-835 CrossRef PubMed
50. Schimke, R.T., Kaufman, R.J., Alt, F.W. and Kellems, R.F. (1978) Gene amplification and drug resistance in cultured murine cells. Science 202, 1051-1055 CrossRef PubMed
51. Chen, Y., Pi, B., Zhou, H., Yu, Y. and Li, L. (2009) Triclosan resistance in clinical isolates of Acinetobacter baumannii. J. Med. Microbiol. 58, 1086-1091 CrossRef PubMed
52. Banerjee, A., Dubnau, E., Quemard, A., Balasubramanian, V., Um, K.S., Wilson, T., Collins, D., de Lisle, G. and Jacobs, Jr, W.R. (1994) inhA , a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263, 227-230 CrossRef PubMed
53. Sugden, C.J., Roper, J.R. and Williams, J.G. (2005) Engineered gene over-expression as a method of drug target identification. Biochem. Biophys. Res. Commun. 334, 555-560 CrossRef PubMed
54. Palmer, A.C. and Kishony, R. (2014) Opposing effects of target overexpression reveal drug mechanisms. Nat. Commun. 5, 4296 CrossRef PubMed
55. Hancock, R.E. and Rozek, A. (2002) Role of membranes in the activities of antimicrobial cationic peptides. FEMS Microbiol. Lett. 206, 143-149 CrossRef PubMed
56. Ernst-Fonberg, M.L., Williams, S.G. and Worsham, L.M. (1990) Acyl carrier protein interacts with melittin. Biochim. Biophys. Acta 1046, 111-119 CrossRef PubMed