Structure-Function Analyses of a Staphylococcus epidermidis Autoinducing Peptide Reveals Motifs Critical for AgrC-type Receptor Modulation

ACS Chemical Biology

Volumn 11, Issue 7, 2016, Pages 1982-1991

  Yang, Tian ^a   Tal Gan, Yftah ^b   Paharik, Alexandra E ^c   Horswill, Alexander R ^c   Blackwell, Helen E ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF NEVADA   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRC RECEPTOR; ALANINE; AUTOINDUCING PEPTIDE; BACTERIAL PROTEIN; DEXTRO AMINO ACID; PEPTIDE; UNCLASSIFIED DRUG; AGRC PROTEIN, STAPHYLOCOCCUS; PROTEIN KINASE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL INFECTION; BIOFILM; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; QUORUM SENSING; REGULATOR GENE; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS EPIDERMIDIS INFECTION; STRUCTURE ACTIVITY RELATION; CHEMISTRY; METABOLISM;

BACTERIAL PROTEINS; PEPTIDES; PROTEIN KINASES; STAPHYLOCOCCUS EPIDERMIDIS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84978676780     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/acschembio.6b00120     Document Type: Article

References (66)

1. Vuong, C. and Otto, M. (2002) Staphylococcus epidermidis infections Microbes Infect. 4, 481-489 10.1016/S1286-4579(02)01563-0
2. von Eiff, C., Peters, G., and Heilmann, C. (2002) Pathogenesis of infections due to coagulase-negative staphylococci Lancet Infect. Dis. 2, 677-685 10.1016/S1473-3099(02)00438-3
3. Otto, M. (2009) Staphylococcus epidermidis - the 'accidental' pathogen Nat. Rev. Microbiol. 7, 555-567 10.1038/nrmicro2182
4. McCann, M. T., Gilmore, B. F., and Gorman, S. P. (2008) Staphylococcus epidermidis device-related infections: pathogenesis and clinical management J. Pharm. Pharmacol. 60, 1551-1571 10.1211/jpp.60.12.0001
5. Mertens, A. and Ghebremedhin, B. (2013) Genetic determinants and biofilm formation of clinical Staphylococcus epidermidis isolates from blood cultures and indwelling devises Eur. J. Microbiol. Immunol. 3, 111-119 10.1556/EuJMI.3.2013.2.4
6. Rogers, K. L., Fey, P. D., and Rupp, M. E. (2009) Coagulase-negative staphylococcal infections Infect. Dis. Clin. North Am. 23, 73-98 10.1016/j.idc.2008.10.001
7. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial biofilms: a common cause of persistent infections Science 284, 1318-1322 10.1126/science.284.5418.1318
8. Claessens, J., Roriz, M., Merckx, R., Baatsen, P., Van Mellaert, L., and Van Eldere, J. (2015) Inefficacy of vancomycin and teicoplanin in eradicating and killing Staphylococcus epidermidis biofilms in vitro Int. J. Antimicrob. Agents 45, 368-375 10.1016/j.ijantimicag.2014.11.011
9. Cheung, G. Y., Joo, H. S., 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
10. Kong, K. F., Vuong, C., and Otto, M. (2006) Staphylococcus quorum sensing in biofilm formation and infection Int. J. Med. Microbiol. 296, 133-139 10.1016/j.ijmm.2006.01.042
11. Vuong, C., Durr, M., Carmody, A. B., Peschel, A., Klebanoff, S. J., and Otto, M. (2004) Regulated expression of pathogen-associated molecular pattern molecules in Staphylococcus epidermidis: quorum-sensing determines pro-inflammatory capacity and production of phenol-soluble modulins Cell. Microbiol. 6, 753-759 10.1111/j.1462-5822.2004.00401.x
12. Wang, C., Li, M., Dong, D., Wang, J., Ren, J., Otto, M., and Gao, Q. (2007) Role of ClpP in biofilm formation and virulence of Staphylococcus epidermidis Microbes Infect. 9, 1376-1383 10.1016/j.micinf.2007.06.012
13. Yao, Y., Vuong, C., Kocianova, S., Villaruz, A. E., Lai, Y., Sturdevant, D. E., and Otto, M. (2006) Characterization of the Staphylococcus epidermidis accessory-gene regulator response: quorum-sensing regulation of resistance to human innate host defense J. Infect. Dis. 193, 841-848 10.1086/500246
14. Camilli, A. and Bassler, B. L. (2006) Bacterial small-molecule signaling pathways Science 311, 1113-1116 10.1126/science.1121357
15. Rutherford, S. T. and Bassler, B. L. (2012) Bacterial quorum sensing: its role in virulence and possibilities for its control Cold Spring Harbor Perspect. Med. 2, a012427 10.1101/cshperspect.a012427
16. Lyon, G. J. and Novick, R. P. (2004) Peptide signaling in Staphylococcus aureus and other Gram-positive bacteria Peptides 25, 1389-1403 10.1016/j.peptides.2003.11.026
17. Novick, R. P. and Geisinger, E. (2008) Quorum sensing in staphylococci Annu. Rev. Genet. 42, 541-564 10.1146/annurev.genet.42.110807.091640
18. Thoendel, M., Kavanaugh, J. S., Flack, C. E., and Horswill, A. R. (2011) Peptide signaling in the staphylococci Chem. Rev. 111, 117-151 10.1021/cr100370n
19. George, E. A. and Muir, T. W. (2007) Molecular mechanisms of agr quorum sensing in virulent staphylococci ChemBioChem 8, 847-855 10.1002/cbic.200700023
20. Ji, G., Beavis, R. C., and Novick, R. P. (1995) Cell density control of staphylococcal virulence mediated by an octapeptide pheromone Proc. Natl. Acad. Sci. U. S. A. 92, 12055-12059 10.1073/pnas.92.26.12055
21. Kavanaugh, J. S., Thoendel, M., and Horswill, A. R. (2007) A role for type I signal peptidase in Staphylococcus aureus quorum sensing Mol. Microbiol. 65, 780-798 10.1111/j.1365-2958.2007.05830.x
22. Wang, B., Zhao, A., Novick, R. P., and Muir, T. W. (2014) Activation and inhibition of the receptor histidine kinase AgrC occurs through opposite helical transduction motions Mol. Cell 53, 929-940 10.1016/j.molcel.2014.02.029
23. George Cisar, E. A., Geisinger, E., Muir, T. W., and Novick, R. P. (2009) Symmetric signalling within asymmetric dimers of the Staphylococcus aureus receptor histidine kinase AgrC Mol. Microbiol. 74, 44-57 10.1111/j.1365-2958.2009.06849.x
24. Novick, R. P., Ross, H. F., Projan, S. J., Kornblum, J., Kreiswirth, B., and Moghazeh, S. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule EMBO J. 12, 3967-3975
25. Otto, M. (2014) Phenol-soluble modulins Int. J. Med. Microbiol. 304, 164-169 10.1016/j.ijmm.2013.11.019
26. Buttner, H., Mack, D., and Rohde, H. (2015) Structural basis of Staphylococcus epidermidis biofilm formation: mechanisms and molecular interactions Front. Cell. Infect. Microbiol. 5, 14 10.3389/fcimb.2015.00014
27. Otto, M. (2004) Virulence factors of the coagulase-negative staphylococci Front. Biosci., Landmark Ed. 9, 841-863 10.2741/1295
28. Mack, D., Davies, A. P., Harris, L. G., Rohde, H., Horstkotte, M. A., and Knobloch, J. K. (2007) Microbial interactions in Staphylococcus epidermidis biofilms Anal. Bioanal. Chem. 387, 399-408 10.1007/s00216-006-0745-2
29. Vuong, C., Gerke, C., Somerville, G. A., Fischer, E. R., and Otto, M. (2003) Quorum-sensing control of biofilm factors in Staphylococcus epidermidis J. Infect. Dis. 188, 706-718 10.1086/377239
30. 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
31. Le, K. Y., Dastgheyb, S., Ho, T. V., and Otto, M. (2014) Molecular determinants of staphylococcal biofilm dispersal and structuring Front. Cell. Infect. Microbiol. 4, 167 10.3389/fcimb.2014.00167
32. Boles, B. R. and Horswill, A. R. (2008) agr-mediated dispersal of Staphylococcus aureus biofilms PLoS Pathog. 4, e1000052 10.1371/journal.ppat.1000052
33. Vuong, C., Kocianova, S., Yao, Y., Carmody, A. B., and Otto, M. (2004) Increased colonization of indwelling medical devices by quorum-sensing mutants of Staphylococcus epidermidis in vivo J. Infect. Dis. 190, 1498-1505 10.1086/424487
34. Otto, M. (2004) Quorum-sensing control in Staphylococci - a target for antimicrobial drug therapy? FEMS Microbiol. Lett. 241, 135-141 10.1016/j.femsle.2004.11.016
35. Otto, M. (2013) Staphylococcal infections: mechanisms of biofilm maturation and detachment as critical determinants of pathogenicity Annu. Rev. Med. 64, 175-188 10.1146/annurev-med-042711-140023
36. Olson, M. E., Todd, D. A., Schaeffer, C. R., Paharik, A. E., Van Dyke, M. J., Buttner, H., Dunman, P. M., Rohde, H., Cech, N. B., Fey, P. D., and Horswill, A. R. (2014) Staphylococcus epidermidis agr quorum-sensing system: signal identification, cross talk, and importance in colonization J. Bacteriol. 196, 3482-3493 10.1128/JB.01882-14
37. Klug, D., Wallet, F., Kacet, S., and Courcol, R. J. (2003) Involvement of adherence and adhesion Staphylococcus epidermidis genes in pacemaker lead-associated infections J. Clin. Microbiol. 41, 3348-3350 10.1128/JCM.41.7.3348-3350.2003
38. Hellmark, B., Soderquist, B., Unemo, M., and Nilsdotter-Augustinsson, A. (2013) Comparison of Staphylococcus epidermidis isolated from prosthetic joint infections and commensal isolates in regard to antibiotic susceptibility, agr type, biofilm production, and epidemiology Int. J. Med. Microbiol. 303, 32-39 10.1016/j.ijmm.2012.11.001
39. Lianhua, Y., Yunchao, H., Guangqiang, Z., Kun, Y., Xing, L., and Fengli, G. (2014) The effect of iatrogenic Staphylococcus epidermidis intercellar adhesion operon on the formation of bacterial biofilm on polyvinyl chloride surfaces Surg. Infect. (Larchmt) 15, 768-773 10.1089/sur.2013.129
40. Schaeffer, C. R., Woods, K. M., Longo, G. M., Kiedrowski, M. R., Paharik, A. E., Buttner, H., Christner, M., Boissy, R. J., Horswill, A. R., Rohde, H., and Fey, P. D. (2015) Accumulation-associated protein enhances Staphylococcus epidermidis biofilm formation under dynamic conditions and is required for infection in a rat catheter model Infect. Immun. 83, 214-226 10.1128/IAI.02177-14
41. Carmody, A. B. and Otto, M. (2004) Specificity grouping of the accessory gene regulator quorum-sensing system of Staphylococcus epidermidis is linked to infection Arch. Microbiol. 181, 250-253 10.1007/s00203-003-0644-2
42. Ji, G., Beavis, R., and Novick, R. P. (1997) Bacterial interference caused by autoinducing peptide variants Science 276, 2027-2030 10.1126/science.276.5321.2027
43. Mayville, P., Ji, G., Beavis, R., Yang, H., Goger, M., Novick, R. P., and Muir, T. W. (1999) Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence Proc. Natl. Acad. Sci. U. S. A. 96, 1218-1223 10.1073/pnas.96.4.1218
44. Wright, J. S., 3rd, Jin, R., and Novick, R. P. (2005) Transient interference with staphylococcal quorum sensing blocks abscess formation Proc. Natl. Acad. Sci. U. S. A. 102, 1691-1696 10.1073/pnas.0407661102
45. Otto, M. (2001) Staphylococcus aureus and Staphylococcus epidermidis peptide pheromones produced by the accessory gene regulator agr system Peptides 22, 1603-1608 10.1016/S0196-9781(01)00495-8
46. Otto, M., Echner, H., Voelter, W., and Gotz, F. (2001) Pheromone cross-inhibition between Staphylococcus aureus and Staphylococcus epidermidis Infect. Immun. 69, 1957-1960 10.1128/IAI.69.3.1957-1960.2001
47. Otto, M., Sussmuth, R., Vuong, C., Jung, G., and Gotz, F. (1999) Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives FEBS Lett. 450, 257-262 10.1016/S0014-5793(99)00514-1
48. Fleming, V., Feil, E., Sewell, A. K., Day, N., Buckling, A., and Massey, R. C. (2006) Agr interference between clinical Staphylococcus aureus strains in an insect model of virulence J. Bacteriol. 188, 7686-7688 10.1128/JB.00700-06
49. Lina, G., Boutite, F., Tristan, A., Bes, M., Etienne, J., and Vandenesch, F. (2003) Bacterial Competition for Human Nasal Cavity Colonization: Role of Staphylococcal agr Alleles Appl. Environ. Microbiol. 69, 18-23 10.1128/AEM.69.1.18-23.2003
50. Amara, N., Krom, B. P., Kaufmann, G. F., and Meijler, M. M. (2011) Macromolecular inhibition of quorum sensing: enzymes, antibodies, and beyond Chem. Rev. 111, 195-208 10.1021/cr100101c
51. Galloway, W. R., Hodgkinson, J. T., Bowden, S., Welch, M., and Spring, D. R. (2012) Applications of small molecule activators and inhibitors of quorum sensing in Gram-negative bacteria Trends Microbiol. 20, 449-458 10.1016/j.tim.2012.06.003
52. Praneenararat, T., Palmer, A. G., and Blackwell, H. E. (2012) Chemical methods to interrogate bacterial quorum sensing pathways Org. Biomol. Chem. 10, 8189-8199 10.1039/c2ob26353j
53. McDowell, P., Affas, Z., Reynolds, C., Holden, M. T., Wood, S. J., Saint, S., Cockayne, A., Hill, P. J., Dodd, C. E., Bycroft, B. W., Chan, W. C., and Williams, P. (2001) Structure, activity and evolution of the group I thiolactone peptide quorum-sensing system of Staphylococcus aureus Mol. Microbiol. 41, 503-512 10.1046/j.1365-2958.2001.02539.x
54. Lyon, G. J., Mayville, P., Muir, T. W., and Novick, R. P. (2000) Rational design of a global inhibitor of the virulence response in Staphylococcus aureus, based in part on localization of the site of inhibition to the receptor-histidine kinase, AgrC Proc. Natl. Acad. Sci. U. S. A. 97, 13330-13335 10.1073/pnas.97.24.13330
55. Lyon, G. J., Wright, J. S., Muir, T. W., and Novick, R. P. (2002) Key determinants of receptor activation in the agr autoinducing peptides of Staphylococcus aureus Biochemistry 41, 10095-10104 10.1021/bi026049u
56. Scott, R. J., Lian, L. Y., Muharram, S. H., Cockayne, A., Wood, S. J., Bycroft, B. W., Williams, P., and Chan, W. C. (2003) Side-chain-to-tail thiolactone peptide inhibitors of the staphylococcal quorum-sensing system Bioorg. Med. Chem. Lett. 13, 2449-2453 10.1016/S0960-894X(03)00497-9
57. George, E. A., Novick, R. P., and Muir, T. W. (2008) Cyclic peptide inhibitors of staphylococcal virulence prepared by Fmoc-based thiolactone peptide synthesis J. Am. Chem. Soc. 130, 4914-4924 10.1021/ja711126e
58. Fowler, S. A., Stacy, D. M., and Blackwell, H. E. (2008) Design and synthesis of macrocyclic peptomers as mimics of a quorum sensing signal from Staphylococcus aureus Org. Lett. 10, 2329-2332 10.1021/ol800908h
59. Tal-Gan, Y., Stacy, D. M., Foegen, M. K., Koenig, D. W., and Blackwell, H. E. (2013) Highly potent inhibitors of quorum sensing in Staphylococcus aureus revealed through a systematic synthetic study of the group-III autoinducing peptide J. Am. Chem. Soc. 135, 7869-7882 10.1021/ja3112115
60. Tal-Gan, Y., Stacy, D. M., and Blackwell, H. E. (2014) N-Methyl and peptoid scans of an autoinducing peptide reveal new structural features required for inhibition and activation of AgrC quorum sensing receptors in Staphylococcus aureus Chem. Commun. (Cambridge, U. K.) 50, 3000-3003 10.1039/c4cc00117f
61. Johnson, J. G., Wang, B., Debelouchina, G. T., Novick, R. P., and Muir, T. W. (2015) Increasing AIP Macrocycle Size Reveals Key Features of agr Activation in Staphylococcus aureus ChemBioChem 16, 1093-1100 10.1002/cbic.201500006
62. Otto, M., Sussmuth, R., Jung, G., and Gotz, F. (1998) Structure of the pheromone peptide of the Staphylococcus epidermidis agr system FEBS Lett. 424, 89-94 10.1016/S0014-5793(98)00145-8
63. Khan, B. A., Yeh, A. J., Cheung, G. Y., and Otto, M. (2015) Investigational therapies targeting quorum-sensing for the treatment of Staphylococcus aureus infections Expert Opin. Invest. Drugs 24, 689-704 10.1517/13543784.2015.1019062
64. Tal-Gan, Y., Ivancic, M., Cornilescu, G., Cornilescu, C. C., and Blackwell, H. E. (2013) Structural characterization of native autoinducing peptides and abiotic analogues reveals key features essential for activation and inhibition of an AgrC quorum sensing receptor in Staphylococcus aureus J. Am. Chem. Soc. 135, 18436-18444 10.1021/ja407533e
65. Kirchdoerfer, R. N., Garner, A. L., Flack, C. E., Mee, J. M., Horswill, A. R., Janda, K. D., Kaufmann, G. F., and Wilson, I. A. (2011) Structural basis for ligand recognition and discrimination of a quorum-quenching antibody J. Biol. Chem. 286, 17351-17358 10.1074/jbc.M111.231258
66. Kratochvil, M. J., Tal-Gan, Y., Yang, T., Blackwell, H. E., and Lynn, D. M. (2015) Nanoporous Superhydrophobic Coatings that Promote the Extended Release of Water-Labile Quorum Sensing Inhibitors and Enable Long-Term Modulation of Quorum Sensing in Staphylococcus aureus ACS Biomater. Sci. Eng. 1, 1039-1049 10.1021/acsbiomaterials.5b00313