Solution Structures of Phenol-Soluble Modulins α1, α3, and β2, Virulence Factors from Staphylococcus aureus

Biochemistry

Volumn 55, Issue 34, 2016, Pages 4798-4806

  Towle, Kaitlyn M ^a   Lohans, Christopher T ^a   Miskolzie, Mark ^a   Acedo, Jeella Z ^a   Van Belkum, Marco J ^a   Vederas, John C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; MAGNETIC RESONANCE SPECTROSCOPY; METABOLITES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; PHENOLS;

BIOFILM FORMATION; HETEROLOGOUS EXPRESSION; HOST IMMUNE RESPONSE; PEPTIDE SYNTHESIS; SOLUTION STRUCTURES; STAPHYLOCOCCUS AUREUS; THREE-DIMENSIONAL STRUCTURE; VIRULENCE FACTORS;

IMMUNE SYSTEM;

BACTERIAL TOXIN; BACTERIOCIN; FORMYLMETHIONINE; PHENOL SOLUBLE MODULIN ALPHA1; PHENOL SOLUBLE MODULIN ALPHA3; PHENOL SOLUBLE MODULIN BETA2; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG; VIRULENCE FACTOR; PHENOL; RECOMBINANT PROTEIN; STAPHYLOCOCCAL DELTA TOXIN;

ALPHA HELIX; AMINO ACID SEQUENCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CIRCULAR DICHROISM; DRUG MANUFACTURE; DRUG PURIFICATION; DRUG SOLUBILITY; DRUG STRUCTURE; ESCHERICHIA COLI; HETEROLOGOUS EXPRESSION; HYDROPHOBICITY; NONHUMAN; NUCLEAR OVERHAUSER EFFECT; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SPATIAL ANALYSIS; STAPHYLOCOCCUS AUREUS; CHEMISTRY; GENETICS; HUMAN; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PATHOGENICITY; SOLUBILITY; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; BACTERIAL TOXINS; CIRCULAR DICHROISM; HUMANS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHENOL; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SOLUBILITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY; VIRULENCE FACTORS;

EID: 84984923502     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.6b00615     Document Type: Article

References (38)

1. Arnold, S. R., Elias, D., Buckingham, S. C., Thomas, E. D., Novais, E., Arkader, A., and Howard, C. (2006) Changing patterns of acute hematogenous osteomyelitis and septic arthritis: emergence of community-associated methicillin-resistant Staphylococcus aureus J. Pediatr. Orthop. 26, 703-708 10.1097/01.bpo.0000242431.91489.b4
2. DeLeo, F. R., Otto, M., Kreiswirth, B. N., and Chambers, H. F. (2010) Community-associated meticillin-resistant Staphylococcus aureus Lancet 375, 1557-1568 10.1016/S0140-6736(09)61999-1
3. Lowy, F. D. (1998) Staphylococcus aureus Infections N. Engl. J. Med. 339, 520-532 10.1056/NEJM199808203390806
4. Novick, R. P., Schlievert, P., and Ruzin, A. (2001) Pathogenicity and resistance islands of staphylococci Microbes Infect. 3, 585-594 10.1016/S1286-4579(01)01414-9
5. Otto, M. (2014) Staphylococcus aureus toxins Curr. Opin. Microbiol. 17, 32-37 10.1016/j.mib.2013.11.004
6. Wang, R., Braughton, K. R., Kretschmer, D., Bach, T. H. L., Queck, S. Y., Li, M., Kennedy, A. D., Dorward, D. W., Klebanoff, S. J., Peschel, A., DeLeo, F. R., and Otto, M. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA Nat. Med. 13, 1510-1514 10.1038/nm1656
7. Cheung, G. Y. C., Joo, H., Chatterjee, S. S., and Otto, M. (2014) Phenol-soluble modulins-critical determinants of staphylococcal virulence FEMS Microbiol. Rev. 38, 698-719 10.1111/1574-6976.12057
8. Kretschmer, D., Gleske, A., Rautenberg, M., Wang, R., Köberle, M., Bohn, E., Schöneberg, T., Rabiet, M., Boulay, F., Klebanoff, S. J., van Kessel, K. A., van Strijp, J. A., Otto, M., and Peschel, A. (2010) Human Formyl Peptide Receptor 2 Senses Highly Pathogenic Staphylococcus aureus Cell Host Microbe 7, 463-473 10.1016/j.chom.2010.05.012
9. Cheung, G. Y. C., Kretschmer, D., Queck, S. Y., Joo, H., Wang, R., Duong, A. C., Nguyen, T. H., Bach, T. L., Porter, A. R., DeLeo, F. R., Peschel, A., and Otto, M. (2014) Insight into structure-function relationship in phenol-soluble modulins using an alanine screen of the phenol-soluble modulin (PSM) alpha 3 peptide FASEB J. 28, 153-161 10.1096/fj.13-232041
10. Costerton, J. W. (1999) Bacterial Biofilms: A Common Cause of Persistent Infections Science 284, 1318-1322 10.1126/science.284.5418.1318
11. Wang, R., Khan, B. A., Cheung, G. Y., Bach, T. H., Jameson-Lee, M., Kong, K. F., Queck, S. Y., and Otto, M. (2011) Staphylococcus epidermidis surfactant peptides promote biofilm maturation and dissemination of biofilm-associated infection in mice J. Clin. Invest. 121, 238-248 10.1172/JCI42520
12. Tsompanidou, E., Denham, E. L., and van Dijl, J. M. (2013) Phenol-soluble modulins, hellhounds from the staphylococcal virulence-factor pandemonium Trends Microbiol. 21, 313-315 10.1016/j.tim.2013.04.007
13. Periasamy, S., Joo, H. S., Duong, A. C., Bach, T. H., Tan, V. Y., Chatterjee, S. S., Cheung, G. Y., and Otto, M. (2012) How Staphylococcus aureus biofilms develop their characteristic structure Proc. Natl. Acad. Sci. U. S. A. 109, 1281-1286 10.1073/pnas.1115006109
14. Cheung, G. Y. C., Rigby, K., Wang, R., Queck, S. Y., Braughton, K. R., Whitney, A. R., Teintze, M., DeLeo, F. R., and Otto, M. (2010) Staphylococcus epidermidis Strategies to Avoid Killing by Human Neutrophils PLoS Pathog. 6, e1001133 10.1371/journal.ppat.1001133
15. Rasigade, J., Trouillet-Assant, S., Ferry, T., Diep, B. A., Sapin, A., Lhoste, Y., Ranfaing, J., Badiou, C., Benito, Y., Bes, M., Couzon, F., Tigaud, S., Lina, G., Etienne, J., Vandenesch, F., and Laurent, F. (2013) PSMs of Hypervirulent Staphylococcus aureus Act as Intracellular Toxins That Kill Infected Osteoblasts PLoS One 8, e63176 10.1371/journal.pone.0063176
16. Joo, H. S., Cheung, G. Y., and Otto, M. (2011) Antimicrobial activity of community-associated methicillin-resistant Staphylococcus aureus is caused by phenol-soluble modulin derivatives J. Biol. Chem. 286, 8933-8940 10.1074/jbc.M111.221382
17. Gonzalez, D. J., Okumura, C. Y., Hollands, A., Kersten, R., Akong-Moore, K., Pence, M. A., Malone, C. L., Derieux, J., Moore, B. S., Horswill, A. R., Dixon, J. E., Dorrestein, P. C., and Nizet, V. (2012) Novel phenol-soluble modulin derivatives in community-associated methicillin-resistant Staphylococcus aureus identified through imaging mass spectrometry J. Biol. Chem. 287, 13889-13898 10.1074/jbc.M112.349860
18. Chatterjee, S. S., Joo, H. S., Duong, A. C., Dieringer, T. D., Tan, V. Y., Song, Y., Fischer, E. R., Cheung, G. Y., Li, M., and Otto, M. (2013) Essential Staphylococcus aureus toxin export system Nat. Med. 19, 364-367 10.1038/nm.3047
19. Cheung, G. Y. C., Wang, R., Khan, B. A., Sturdevant, D. E., and Otto, M. (2011) Role of the Accessory Gene Regulator agr in Community-Associated Methicillin-Resistant Staphylococcus aureus Pathogenesis Infect. Immun. 79, 1927-1935 10.1128/IAI.00046-11
20. Peschel, A. and Otto, M. (2013) Phenol-soluble modulins and staphylococcal infection Nat. Rev. Microbiol. 11, 667-673 10.1038/nrmicro3110
21. Tappin, M. J., Pastore, A., Norton, R. S., Freer, J. H., and Campbell, I. D. (1988) High-resolution proton NMR study of the solution structure of.delta.-hemolysin Biochemistry 27, 1643-1647 10.1021/bi00405a038
22. Gladstone, G. P. and Yoshida, A. (1967) The cytopathic action of purified staphylococcal delta-hemolysin Br. J. Exp. Pathol. 48, 11-19
23. Laabei, M., Jamieson, W. D., Yang, Y., van den Elsen, J., and Jenkins, A. T. A. (2014) Investigating the lytic activity and structural properties of Staphylococcus aureus phenol soluble modulin (PSM) peptide toxins Biochim. Biophys. Acta, Biomembr. 1838, 3153-3161 10.1016/j.bbamem.2014.08.026
24. Acedo, J. Z., van Belkum, M. J., Lohans, C. T., Towle, K. M., Miskolzie, M., and Vederas, J. C. (2016) Nuclear Magnetic Resonance Solution Structures of Lacticin Q and Aureocin A53 Reveal a Structural Motif Convserved among Leaderless Bacteriocins with Broad-Spectrum Activity Biochemistry 55, 733-742 10.1021/acs.biochem.5b01306
25. Cintas, L. M., Casaus, P., Holo, H., Hernandez, P. E., Nes, I. F., and Håvarstein, L. S. (1998) Enterocins L50A and L50B, two novel bacteriocins from Enterococcus faecium L50, are related to staphylococcal hemolysins J. Bacteriol. 180, 1988-1994
26. Lohans, C. T., Towle, K. M., Miskolzie, M., McKay, R. T., van Belkum, M. J., McMullen, L. M., and Vederas, J. C. (2013) Solution Structures of the Linear Leaderless Bacteriocins Enterocin 7A and 7B Resemble Carnocyclin A, a Circular Antimicrobial Peptide Biochemistry 52, 3987-3994 10.1021/bi400359z
27. Zhang, L., Goldammer, C., Henkel, B., Zühl, F., Panhaus, G., Jung, G., and Bayer, E. (1994) in 3rd International Symposium on Innovation and Perspectives in SPPS, Oxford UK, Mayflower Scientific Ltd: Birmingham, Vol. 711.
28. Kaiser, E., Colescott, R. L., Bossinger, C. D., and Cook, P. I. (1970) Color test for detection of free terminal amino groups in solid-phase synthesis of peptides Anal. Biochem. 34, 595-598 10.1016/0003-2697(70)90146-6
29. Hwang, T. L. and Shaka, A. J. (1995) Water Suppression That Works. Excitation Sculpting Using Arbitrary Wave-Forms and Pulsed-Field Gradients J. Magn. Reson., Ser. A 112, 275-279 10.1006/jmra.1995.1047
30. Morrow, J. A., Segall, M. L., Lund-Katz, S., Phillips, M. C., Knapp, M., Rupp, B., and Weisgraber, K. H. (2000) Differences in Stability among the Human Apolipoprotein E isoforms Determined by the Amino-Terminal Domain Biochemistry 39, 11657-11666 10.1021/bi000099m
31. Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program Dyana1 J. Mol. Biol. 273, 283-298 10.1006/jmbi.1997.1284
32. Kretschmer, D., Nikola, N., Dürr, M., Otto, M., and Peschel, A. (2012) The Virulence Regulator Agr Controls the Staphylococcal Capacity to Activate Human Neutrophils via the Formyl Peptide Receptor 2 J. Innate Immun. 4, 201-212 10.1159/000332142
33. Kumar, S. and Nussinov, R. (2002) Close-Range Electrostatic Interactions in Proteins ChemBioChem 3, 604-617 10.1002/1439-7633(20020703)3:7<604::AID-CBIC604>3.0.CO;2-X
34. Krittanai, C. and Johnson, W. C., Jr. (1997) Correcting the Circular Dichroism Spectra of Peptides for Contributions of Absorbing Side Chains Anal. Biochem. 253, 57-64 10.1006/abio.1997.2366
35. Verdon, J., Girardin, N., Lacombe, C., Berjeaud, J. M., and Hechard, Y. (2009) Delta-Hemolysin, an Update on a Membrane-Interacting Peptide Peptides 30, 817-823 10.1016/j.peptides.2008.12.017
36. Sievers, F. and Higgins, D. G. (2014) Clustal omega Current Protocols in Bioinformatics 48, 3.13.1-3.13.16 10.1002/0471250953.bi0313s48
37. The PyMOL Molecular Graphics System, version 1.8 (2015) Schrödinger, LLC, Portland, OR.
38. 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, W665-7 10.1093/nar/gkh381