Solution structures of the linear leaderless bacteriocins enterocin 7A and 7B resemble carnocyclin A, a circular antimicrobial peptide

Biochemistry

Volumn 52, Issue 23, 2013, Pages 3987-3994

  Lohans, Christopher T ^a   Towle, Kaitlyn M ^a   Miskolzie, Mark ^a   McKay, Ryan T ^a   Van Belkum, Marco J ^a   McMullen, Lynn M ^a   Vederas, John C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL PEPTIDE; ENTEROCOCCUS FAECALIS; FOOD-BORNE PATHOGENS; GRAM-POSITIVE BACTERIUM; GRAM-POSITIVE ORGANISMS; ISOTHERMAL CALORIMETRY; SYNERGISTIC ACTIVITY; THREE-DIMENSIONAL STRUCTURE;

BACILLI; BINDING ENERGY; CLOSTRIDIUM; LISTERIA; POLYPEPTIDES; SEPARATION;

PEPTIDES;

BACTERIOCIN; CARNOCYCLIN A; ENTEROCIN 7A; ENTEROCIN 7B; POLYPEPTIDE ANTIBIOTIC AGENT; SPHINGOLIPID ACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; AQUEOUS SOLUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; COVALENT BOND; DRUG POTENTIATION; ENTEROCOCCUS FAECALIS; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; BACTERIOCINS; CIRCULAR DICHROISM; ENTEROCOCCUS FAECALIS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDES, CYCLIC; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; STRUCTURAL HOMOLOGY, PROTEIN;

CLOSTRIDIUM; ENTEROCOCCUS FAECALIS; LISTERIA; POSIBACTERIA;

EID: 84878922657     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400359z     Document Type: Article

References (41)

1. Cotter, P. D., Hill, C., and Ross, R. P. (2005) Bacteriocins: developing innate immunity for food Nat. Rev. Microbiol. 3, 777-788
2. Arnison, P. G., Bibb, M. J., Bierbaum, G., Bowers, A. A., Bugni, T. S., Bulaj, G., Camarero, J. A., Campopiano, D. J., Challis, G. L., and Clardy, J. 2013, Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature Nat. Prod. Rep. 30, 108-160
3. Oman, T. J. and van der Donk, W. A. (2010) Follow the leader: the use of leader peptides to guide natural product biosynthesis Nat. Chem. Biol. 6, 9-18
4. van Belkum, M. J., Worobo, R. W., and Stiles, M. E. (1997) Double-glycine type leader peptides direct secretion of bacteriocins by ABC transporters: colicin V secretion in Lactococcus lactis Mol. Microbiol. 23, 1293-1301
5. Patton, G. C., Paul, M., Cooper, L. E., Chatterjee, C., and van der Donk, W. A. (2008) The importance of the leader sequence for directing lanthionine formation in lacticin 481 Biochemistry 47, 7342-7351
6. Flühe, L., Knappe, T. A., Gattner, M. J., Schäfer, A., Burghaus, O., Linne, U., and Marahiel, M. A. (2012) The radical SAM enzyme AlbA catalyzes thioether bond formation in subtilosin A Nat. Chem. Biol. 8, 350-357
7. van Belkum, M. J., Martin-Visscher, L. A., and Vederas, J. C. (2011) Structure and genetics of circular bacteriocins Trends Microbiol. 19, 411-418
8. Masuda, Y., Zendo, T., and Sonomoto, K. (2012) New type non-lantibiotic bacteriocins: circular and leaderless bacteriocins Benefic. Microbes 3, 3-12
9. Iwatani, S., Horikiri, Y., Zendo, T., Nakayama, J., and Sonomoto, K. (2013) Bifunctional gene cluster lnqBCDEF mediates bacteriocin production and immunity with differential genetic requirements Appl. Environ. Microbiol. 79, 2446-2449
10. Netz, D. J. A., Pohl, R., Beck-Sickinger, A. G., Selmer, T., Pierik, A. J., Bastos, M. C. F., and Sahl, H.-G. (2002) Biochemical characterisation and genetic analysis of aureocin A53, a new, atypical bacteriocin from Staphylococcus aureus J. Mol. Biol. 319, 745-756
11. Liu, X., Vederas, J. C., Whittal, R. M., Zheng, J., Stiles, M. E., Carlson, D., Franz, C. M. A. P., McMullen, L. M., and van Belkum, M. J. (2011) Identification of an N-terminal formylated, two-peptide bacteriocin from Enterococcus faecalis 710C J. Agric. Food Chem. 59, 5602-5608
12. Cintas, L. M., Casaus, P., Holo, H., Hernandez, P. E., Nes, I. F., and HaÌŠvarstein, L. S. (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins J. Bacteriol. 180, 1988-1994
13. Yoneyama, F., Imura, Y., Ichimasa, S., Fujita, K., Zendo, T., Nakayama, J., Matsuzaki, K., and Sonomoto, K. (2009) Lacticin Q, a lactococcal bacteriocin, causes high-level membrane permeability in the absence of specific receptors Appl. Environ. Microbiol. 75, 538-541
14. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
15. Johnson, B. A. (2004) Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278, 313-352
16. 1H NMR of proteins. Experimental procedures J. Magn. Reson. 56, 207-234
17. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, pp 1-292, John Wiley & Sons, New York.
18. Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273, 283-298
19. Hauge, H. H., Mantzilas, D., Eijsink, V. G., and Nissen-Meyer, J. (1999) Membrane-mimicking entities induce structuring of the two-peptide bacteriocins plantaricin E/F and plantaricin J/K J. Bacteriol. 181, 740-747
20. Dolinsky, T. J., Nielsen, J. E., McCammon, J. A., and Baker, N. A. (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32, W665-W667
21. Fregeau Gallagher, N. L., Sailer, M., Niemczura, W. P., Nakashima, T. T., Stiles, M. E., and Vederas, J. C. (1997) Three-dimensional structure of leucocin A in trifluoroethanol and dodecylphosphocholine micelles: spatial location of residues critical for biological activity in type IIa bacteriocins from lactic acid bacteria Biochemistry 36, 15062-15072
22. Sit, C. S., Lohans, C. T., van Belkum, M. J., Campbell, C. D., Miskolzie, M., and Vederas, J. C. (2012) Substitution of a conserved disulfide in the type IIa bacteriocin, leucocin A, with L-leucine and L-serine residues: effects on activity and three-dimensional structure ChemBioChem 13, 35-38
23. Wang, Y., Henz, M. E., Fregeau-Gallagher, N. L., Chai, S., Gibbs, A. C., Yan, L. Z., Stiles, M. E., Wishart, D. S., and Vederas, J. C. (1999) Solution structure of carnobacteriocin B2 and implications for structure-activity relationships among type IIa bacteriocins from lactic acid bacteria Biochemistry 38, 15438-15447
24. Martin, N. I., Sprules, T., Carpenter, M. R., Cotter, P. D., Hill, C., Ross, R. P., and Vederas, J. C. (2004) Structural characterization of lacticin 3147, a two-peptide lantibiotic with synergistic activity Biochemistry 43, 3049-3056
25. Martin-Visscher, L. A., Gong, X., Duszyk, M., and Vederas, J. C. (2009) The three-dimensional structure of carnocyclin A reveals that many circular bacteriocins share a common structural motif J. Biol. Chem. 284, 28674-28681
26. Murphy, K., O'Sullivan, O., Rea, M. C., Cotter, P. D., Ross, R. P., and Hill, C. (2011) Genome mining for radical SAM protein determinants reveals multiple sactibiotic-like gene clusters PLoS One 6, e20852
27. Sit, C. S., McKay, R. T., Hill, C., Ross, R. P., and Vederas, J. C. (2011) The 3D structure of thuricin CD, a two-component bacteriocin with cysteine sulfur to α-carbon cross-links J. Am. Chem. Soc. 133, 7680-7683
28. Sit, C. S., van Belkum, M. J., McKay, R. T., Worobo, R. W., and Vederas, J. C. (2011) The 3D solution structure of thurincin H, a bacteriocin with four sulfur to α-carbon crosslinks Angew. Chem., Int. Ed. 50, 8718-8721
29. Yoneyama, F., Imura, Y., Ohno, K., Zendo, T., Nakayama, J., Matsuzaki, K., and Sonomoto, K. (2009) Peptide-lipid huge toroidal pore, a new antimicrobial mechanism mediated by a lactococcal bacteriocin, lacticin Q Antimicrob. Agents Chemother. 53, 3211-3217
30. Netz, D. J. A., Bastos, M. C. F., and Sahl, H.-G. (2002) Mode of action of the antimicrobial peptide aureocin A53 from Staphylococcus aureus Appl. Environ. Microbiol. 68, 5274-5280
31. Lohans, C. T. and Vederas, J. C. (2012) Development of class IIa bacteriocins as therapeutic agents Int. J. Microbiol. 2012, 386410
32. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega Mol. Syst. Biol. 7, 539
33. Miskolzie, M. and Kotovych, G. (2003) The NMR-derived conformation of neuropeptide AF, an orphan G-protein coupled receptor peptide Biopolymers 69, 201-215
34. Nissen-Meyer, J., Rogne, P., OppegaÌŠrd, C., Haugen, H. S., and Kristiansen, P. E. (2009) Structure-function relationships of the non-lanthionine-containing peptide (class II) bacteriocins produced by Gram-positive bacteria Curr. Pharm. Biotechnol. 10, 19-37
35. Gong, X., Martin-Visscher, L. A., Nahirney, D., Vederas, J. C., and Duszyk, M. (2009) The circular bacteriocin, carnocyclin A, forms anion-selective channels in lipid bilayers Biochim. Biophys. Acta 1788, 1797-1803
36. González, C., Langdon, G. M., Bruix, M., Gálvez, A., Valdivia, E., Maqueda, M., and Rico, M. (2000) Bacteriocin AS-48, a microbial cyclic polypeptide structurally and functionally related to mammalian NK-lysin Proc. Natl. Acad. Sci. U. S. A. 97, 11221-11226
37. Sánchez-Barrena, M. J., Martínez-Ripoll, M., Gálvez, A., Valdivia, E., Maqueda, M., Cruz, V., and Albert, A. (2003) Structure of bacteriocin AS-48: from soluble state to membrane-bound state J. Mol. Biol. 334, 541-549
38. Gálvez, A., Maqueda, M., Martínez-Bueno, M., and Valdivia, E. (1991) Permeation of bacterial cells, permeation of cytoplasmic and artificial membrane vesicles, and channel formation on lipid bilayers by peptide antibiotic AS-48 J. Bacteriol. 173, 886-892
39. Netz, D. J. A., Sahl, H.-G., Marcelino, R., Nascimento, J. S., Oliveira, S. S., Soares, M. B., and Bastos, M. C. F. (2001) Molecular characterization of aureocin A70, a multi-peptide bacteriocin isolated from Staphylococcus aureus J. Mol. Biol. 311, 939-949
40. Criado, R., Diep, D. B., Aakra, A., Gutiérrez, J., Nes, I. F., Hernández, P. E., and Cintas, L. M. (2006) Complete sequence of the enterocin Q-encoding plasmid pCIZ2 from the multiple bacteriocin producer Enterococcus faecium L50 and genetic characterization of enterocin Q production and immunity Appl. Environ. Microbiol. 72, 6653-6666
41. Cogen, A. L., Yamasaki, K., Sanchez, K. M., Dorschner, R. A., Lai, Y., MacLeod, D. T., Torpey, J. W., Otto, M., Nizet, V., Kim, J. E., and Gallo, R. L. (2010) Selective antimicrobial action is provided by phenol-soluble modulins derived from Staphylococcus epidermidis, a normal resident of the skin J. Invest. Dermatol. 130, 192-200