Identification of quorum-sensing inhibitors disrupting signaling between rgg and short hydrophobic peptides in streptococci

mBio

Volumn 6, Issue 3, 2015, Pages 1-11

  Aggarwal, Chaitanya ^a   Jimenez, Juan Cristobal ^b   Lee, Hyun ^a   Chlipala, George E ^a   Ratia, Kiira ^a   Federle, Michael J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CHLORAMPHENICOL; CYCLOSPORIN A; ERYTHROMYCIN; FLUORESCEIN ISOTHIOCYANATE; OLMESARTAN; PEPTIDE DERIVATIVE; PROTEIN TYROSINE PHOSPHATASE SHP; QUORUM SENSING INHIBITOR; SAQUINAVIR; SIMVASTATIN; SPECTINOMYCIN; TELMISARTAN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RGG; TRANSCRIPTION FACTOR RGG2; TRANSCRIPTION FACTOR RGG3; UNCLASSIFIED DRUG; VALSPODAR; CYCLOSPORIN; CYCLOSPORIN DERIVATIVE; PEPTIDE; PHEROMONE; RGG PROTEIN, STREPTOCOCCUS; TRANSACTIVATOR PROTEIN;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BINDING AFFINITY; BIOFILM; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG SCREENING; FLUORESCENCE POLARIZATION IMMUNOASSAY; GENE FUNCTION; HYDROPHOBICITY; IN VITRO STUDY; MICROBIAL ACTIVITY; NONHUMAN; PRIORITY JOURNAL; QUORUM SENSING; SIGNAL TRANSDUCTION; STREPTOCOCCUS; STREPTOCOCCUS PYOGENES; TRANSCRIPTION REGULATION; DRUG EFFECTS; FLUORESCENCE POLARIZATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; STREPTOCOCCAL INFECTIONS;

BACTERIA (MICROORGANISMS); FIRMICUTES; STREPTOCOCCUS; STREPTOCOCCUS PYOGENES;

BACTERIAL PROTEINS; BIOFILMS; CYCLOSPORINE; CYCLOSPORINS; FLUORESCENCE POLARIZATION; HUMANS; PEPTIDES; PHEROMONES; QUORUM SENSING; SIGNAL TRANSDUCTION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; TRANS-ACTIVATORS;

EID: 84936937594     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00393-15     Document Type: Article

References (71)

1. Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319-346. http://dx.doi.org/ 10.1146/annurev.cellbio.21.012704.131001.
2. Antunes LC, Ferreira RB, Buckner MM, Finlay BB. 2010. Quorum sensing in bacterial virulence. Microbiology 156:2271-2282. http:// dx.doi.org/10.1099/mic.0.038794-0.
3. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2:012427. http://dx.doi.org/10.1101/cshperspect.a012427.
4. Romero M, Acuña L, Otero A. 2012. Patents on quorum quenching: interfering with bacterial communication as a strategy to fight infections. Recent Pat Biotechnol 6:2-12. http://dx.doi.org/10.2174/ 187220812799789208.
5. LaSarre B, Federle MJ. 2013. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73-111. http://dx.doi.org/ 10.1128/MMBR.00046-12.
6. Cunningham MW. 2000. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13:470-511. http://dx.doi.org/10.1128/ CMR.13.3.470-511.2000.
7. Nizet V. 2007. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J Allergy Clin Immunol 120:13-22. http://dx.doi.org/10.1016/j.jaci.2007.06.005.
8. DeMuri GP, Wald ER. 2014. The group A streptococcal carrier state reviewed: still an enigma. J Pediatr Infect Dis Soc 3:336-342. http:// dx.doi.org/10.1093/jpids/piu030.
9. Stollerman GH. 1991. Rheumatogenic streptococci and autoimmunity. Clin Immunol Immunopathol 61:131-142. http://dx.doi.org/10.1016/ S0090-1229(05)80019-4.
10. StollermanGH. 2001. Rheumatic fever in the 21st century. Clin Infect Dis 33:806-814. http://dx.doi.org/10.1086/322665.
11. Dillon HC, Derrick CW, Dillon MS. 1974. M-antigens common to pyoderma and acute glomerulonephritis. J Infect Dis 130:257-267. http:// dx.doi.org/10.1093/infdis/130.3.257.
12. Silva F. 1998. Acute postinfectious glomerulonephritis and glomerulonephritis complicating persistent bacterial infection. Hepinstall's pathology of the kidney, 5th ed., p 389-453. Lippincott Raven Publishers, Philadelphia, PA.
13. Carapetis JR, Steer AC, Mulholland EK, Weber M. 2005. The global burden of group A streptococcal diseases. Lancet Infect Dis 5:685-694. http://dx.doi.org/10.1016/S1473-3099(05)70267-X.
14. Shulman ST, Bisno AL, Clegg HW, Gerber MA, Kaplan EL, Lee G, Martin JM, Van Beneden C. 2012. Clinical practice guideline for the diagnosis and management of group A streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America. Clin Infect Dis 55: 1279-1282. http://dx.doi.org/10.1093/cid/cis847.
15. Kaplan EL, Johnson DR. 2001. Unexplained reduced microbiological efficacy of intramuscular benzathine penicillinGand of oral penicillinVin eradication of group A streptococci from children with acute pharyngitis. Pediatrics 108:1180-1186. http://dx.doi.org/10.1542/peds.108.5.1180.
16. Pichichero ME, Casey JR, Mayes T, Francis AB, Marsocci SM, Murphy AM, Hoeger W. 2000. Penicillin failure in streptococcal tonsillopharyngitis: causes and remedies. Pediatr Infect Dis J 19:917-923. http://dx.doi.org/ 10.1097/00006454-200009000-00035.
17. Pichichero ME, Casey JR. 2007. Systematic review of factors contributing to penicillin treatment failure in Streptococcus pyogenes pharyngitis. Otolaryngol Head Neck Surg 137:851-857. http://dx.doi.org/10.1016/ j.otohns.2007.07.033.
18. Martin JM, Green M, Barbadora KA, Wald ER. 2002. Erythromycinresistant group A streptococci in schoolchildren in Pittsburgh. N Engl J Med 346:1200-1206. http://dx.doi.org/10.1056/NEJMoa013169.
19. Robinson DA, Sutcliffe JA, Tewodros W, Manoharan A, Bessen DE. 2006. Evolution and global dissemination of macrolide-resistant group A streptococci. Antimicrob Agents Chemother 50:2903-2911. http:// dx.doi.org/10.1128/AAC.00325-06.
20. Chang JC, Lasarre B, Jimenez JC, Aggarwal C, Federle MJ. 2011. Two group A Streptococcal Peptide Pheromones act through Opposing Rgg regulators to control biofilm development. PLoS Pathog 7:e1002190. http://dx.doi.org/10.1371/journal.ppat.1002190.
21. Aggarwal C, Jimenez JC, Nanavati D, Federle MJ. 2014. Multiple length peptide-pheromone variants produced by Streptococcus pyogenes directly bind Rgg proteins to confer transcriptional regulation. J Biol Chem 289:22427-22436. http://dx.doi.org/10.1074/jbc.M114.583989.
22. Declerck N, Bouillaut L, Chaix D, Rugani N, Slamti L, Hoh F, Lereclus D, Arold ST. 2007. Structure of PlcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc Natl Acad Sci U S A 104:18490-18495. http://dx.doi.org/10.1073/ pnas.0704501104.
23. Rocha-Estrada J, Aceves-Diez AE, Guarneros G, de la Torre M. 2010. The RNPP family of quorum-sensing proteins in Gram-positive bacteria. Appl Microbiol Biotechnol 87:913-923. http://dx.doi.org/10.1007/s00253-010-2651-y.
24. Shi K, Brown CK, Gu ZY, Kozlowicz BK, Dunny GM, Ohlendorf DH, Earhart CA. 2005. Structure of peptide sex pheromone receptor PrgX and PrgX/pheromone complexes and regulation of conjugation in Enterococcus faecalis. Proc Natl Acad SciUSA102:18596-18601. http://dx.doi.org/ 10.1073/pnas.0506163102.
25. Zouhir S, Perchat S, Nicaise M, Perez J, Guimaraes B, Lereclus D, Nessler S. 2013. Peptide-binding dependent conformational changes regulate the transcriptional activity of the quorum-sensor NprR. Nucleic Acids Res 41:7920-7933. http://dx.doi.org/10.1093/nar/gkt546.
26. Parashar V, Mirouze N, Dubnau DA, Neiditch MB. 2011. Structural basis of response regulator dephosphorylation by Rap phosphatases. PLoS Biol 9:e1000589. http://dx.doi.org/10.1371/journal.pbio.1000589.
27. Perego M, Higgins CF, Pearce SR, Gallagher MP, Hoch JA. 1991. The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol Microbiol 5:173-185. http://dx.doi.org/ 10.1111/j.1365-2958.1991.tb01838.x.
28. Linton KJ, Higgins CF. 2007. Structure and function of ABC transporters: the ATP switch provides flexible control. Pflugers Arch 453:555-567. http://dx.doi.org/10.1007/s00424-006-0126-x.
29. Fleuchot B, Gitton C, Guillot A, Vidic J, Nicolas P, Besset C, Fontaine L, Hols P, Leblond-Bourget N, Monnet V, Gardan R. 2011. Rgg proteins associated with internalized small hydrophobic peptides: a new quorumsensing mechanism in streptococci. Mol Microbiol 80:1102-1119. http:// dx.doi.org/10.1111/j.1365-2958.2011.07633.x.
30. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167-193. http:// dx.doi.org/10.1128/CMR.15.2.167-193.2002.
31. Fux CA, Costerton JW, Stewart PS, Stoodley P. 2005. Survival strategies of infectious biofilms. Trends Microbiol 13:34-40. http://dx.doi.org/ 10.1016/j.tim.2004.11.010.
32. Kania RE, Lamers GE, Vonk MJ, Huy PT, Hiemstra PS, Bloemberg GV, Grote JJ. 2007. Demonstration of bacterial cells and glycocalyx in biofilms on human tonsils. Arch Otolaryngol Head Neck Surg 133:115-121. http:// dx.doi.org/10.1001/archotol.133.2.115.
33. Cook LC, LaSarre B, Federle MJ. 2013. Interspecies communication among commensal and pathogenic streptococci. mBio 4:e00382-13. http://dx.doi.org/10.1128/mBio.00382-13.
34. Fleuchot B, Guillot A, Mézange C, Besset C, Chambellon E, Monnet V, Gardan R. 2013. Rgg-associated SHP signaling peptides mediate crosstalk in streptococci. PLoS One 8:e66042. http://dx.doi.org/10.1371/ journal.pone.0066042.
35. Mashburn-Warren L, Morrison DA, Federle MJ. 2010. A novel doubletryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol Microbiol 78:589-606. http://dx.doi.org/ 10.1111/j.1365-2958.2010.07361.x.
36. Fontaine L, Boutry C, de Frahan MH, Delplace B, Fremaux C, Horvath P, Boyaval P, Hols P. 2010. A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J Bacteriol 192:1444-1454. http:// dx.doi.org/10.1128/JB.01251-09.
37. Mashburn-Warren L, Morrison DA, Federle MJ. 2012. The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J Bacteriol 194:4589-4600. http://dx.doi.org/10.1128/ JB.00830-12.
38. Rüegger A, Kuhn M, Lichti H, Loosli HR, Huguenin R, Quiquerez C, von Wartburg A. 1976. Cyclosporin A, a peptide metabolite from Trichoderma polysporum (link ex Pers.) Rifai, with a remarkable immunosuppressive activity. Helv Chim Acta 59:1075-1092. http://dx.doi.org/ 10.1002/hlca.19760590412.
39. Matsuda S, Koyasu S. 2000. Mechanisms of action of cyclosporine. Immunopharmacology 47:119-125. http://dx.doi.org/10.1016/S0162-3109(00)00192-2.
40. Steiner JP, Connolly MA, Valentine HL, Hamilton GS, Dawson TM, Hester L, Snyder SH. 1997. Neurotrophic actions of nonimmunosuppressive analogues of immunosuppressive drugs FK506, rapamycin and cyclosporin A. Nat Med 3:421-428. http://dx.doi.org/10.1038/nm0497-421.
41. Wei L, Steiner JP, Hamilton GS, Wu YQ. 2004. Synthesis and neurotrophic activity of nonimmunosuppressant cyclosporin A derivatives. Bioorg Med Chem Lett 14:4549-4551. http://dx.doi.org/10.1016/ j.bmcl.2004.06.028.
42. Jonsson B, Nilsson K, Nygren P, Larsson R. 1992. SDZ PSC-833-a novel potent in vitro chemosensitizer in multiple myeloma. Anti Cancer Drugs 3:641-646. http://dx.doi.org/10.1097/00001813-199212000-00013.
43. Loughman JA, Caparon M. 2006. Regulation of SpeB in Streptococcus pyogenes by pH and NaCl: a model for in vivo gene expression. J Bacteriol 188:399-408. http://dx.doi.org/10.1128/JB.188.2.399-408.2006.
44. Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ. 2008. The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 6:17-27. http://dx.doi.org/10.1038/nrmicro1818.
45. Bjarnsholt T, Ciofu O, Molin S, Givskov M, Høiby N. 2013. Applying insights from biofilm biology to drug development-can a new approach be developed? Nat Rev Drug Discov 12:791-808. http://dx.doi.org/ 10.1038/nrd4000.
46. Allen RC, Popat R, Diggle SP, Brown SP. 2014. Targeting virulence: can we make evolution-proof drugs? Nat Rev Microbiol 12:300-308. http:// dx.doi.org/10.1038/nrmicro3232.
47. Dreyfuss M, Härri E, Hofmann H, Kobel H, Pache W, Tscherter H. 1976. Cyclosporin A and C. Eur J Appl Microbiol 3:125-133. http:// dx.doi.org/10.1007/BF00928431.
48. Borel JF, Feurer C, Gubler HU, Stähelin H. 1994. Biological effects of cyclosporin A: a new antilymphocytic agent. Agents Actions 43:179-186. http://dx.doi.org/10.1007/BF01986686.
49. Krönke M, Leonard WJ, Depper JM, Arya SK, Wong-Staal F, Gallo RC, Waldmann TA, Greene WC. 1984. Cyclosporin A inhibits T-cell growth factor gene expression at the level of mRNA transcription. Proc Natl Acad Sci U S A 81:5214-5218. http://dx.doi.org/10.1073/pnas.81.16.5214.
50. Handschumacher RE, Harding MW, Rice J, Drugge RJ, Speicher DW. 1984. Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226:544-547. http://dx.doi.org/10.1126/science.6238408.
51. Herold KC, Lancki DW, Moldwin RL, Fitch FW. 1986. Immunosuppressive effects of cyclosporin A on cloned T cells. J Immunol 136: 1315-1321.
52. Gaveriaux C. 1991. SDZ PSC 833, a non-immunosuppressive cyclosporin analog, is a very potent multidrug-resistance modifier. J Cell Pharmacol 2:225-234.
53. Archinal-Mattheis A, Rzepka RW, Watanabe T, Kokubu N, Itoh Y, Combates NJ, Bair KW, Cohen D. 1995. Analysis of the interactions of SDZ PSC 833 ([3=-keto-Bmt1]-Val2]-cyclosporine), a multidrug resistance modulator, with P-glycoprotein. Oncol Res 7:603-610.
54. Lasarre B, Aggarwal C, Federle MJ. 2013. Antagonistic Rgg regulators mediate quorum sensing via competitive DNA binding in Streptococcus pyogenes. mBio 3:e00333-12. http://dx.doi.org/10.1128/mBio.00333-12.
55. Roberts AL, Connolly KL, Kirse DJ, Evans AK, Poehling KA, Peters TR, Reid SD. 2012. Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage. BMC Pediatr 12:3. http://dx.doi.org/10.1186/1471-2431-12-3.
56. Connolly KL, Roberts AL, Holder RC, Reid SD. 2011. Dispersal of group A streptococcal biofilms by the cysteine protease SpeB leads to increased disease severity in a murine model. PLoS One 6:e18984. http://dx.doi.org/ 10.1371/journal.pone.0018984.
57. Howell-Adams B, Seifert HS. 2000. Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37:1146-1158. http://dx.doi.org/10.1046/j.1365-2958.2000.02067.x.
58. Miroux B, Walker JE. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J Mol Biol 260:289-298. http://dx.doi.org/ 10.1006/jmbi.1996.0399.
59. LaSarre B, Chang JC, Federle MJ. 2013. Redundant group a streptococcus signaling peptides exhibit unique activation potentials. J Bacteriol 195: 4310-4318. http://dx.doi.org/10.1128/JB.00684-13.
60. Husmann LK, Scott JR, Lindahl G, Stenberg L. 1995. Expression of the Arp protein, a member of theMprotein family, is not sufficient to inhibit phagocytosis of Streptococcus pyogenes. Infect Immun 63:345-348.
61. Zhang J-H, Chung TDY, Oldenburg KR. 1999. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screening 4:67-73. http://dx.doi.org/10.1177/ 108705719900400206.
62. Rossi AM, Taylor CW. 2011. Analysis of protein-ligand interactions by fluorescence polarization. Nat Protoc 6:365-387. http://dx.doi.org/ 10.1038/nprot.2011.305.
63. Bachmann H, Kleerebezem M, van Hylckama Vlieg JE. 2008. Highthroughput identification and validation of in situ-expressed genes of Lactococcus lactis. Appl Environ Microbiol 74:4727-4736. http://dx.doi.org/ 10.1128/AEM.00297-08.
64. McShan WM, Ferretti JJ, Karasawa T, Suvorov AN, Lin S, Qin B, Jia H, Kenton S, Najar F, Wu H, Scott J, Roe BA, Savic DJ. 2008. Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 190:7773-7785. http://dx.doi.org/10.1128/ JB.00672-08.
65. Degnan BA, Fontaine MC, Doebereiner AH, Lee JJ, Mastroeni P, Dougan G, Goodacre JA, Kehoe MA. 2000. Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. Infect Immun 68:2441-2448. http://dx.doi.org/10.1128/IAI.68.5.2441-2448.2000.
66. Beres SB, Sylva GL, Barbian KD, Lei B, Hoff JS, Mammarella ND, Liu MY, Smoot JC, Porcella SF, Parkins LD, Campbell DS, Smith TM, McCormick JK, Leung DY, Schlievert PM, Musser JM. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phageencoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 99:10078-10083. http://dx.doi.org/10.1073/ pnas.152298499.
67. Ajdić D, McShan WM, McLaughlin RE, Savić G, Chang J, Carson MB, Primeaux C, et al. 2002. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci U S A 99(2):14434-14439.
68. Lancefield RC, McCarty M, Everly WN. 1975. Multiple mouseprotective antibodies directed against group B streptococci. Special reference to antibodies effective against protein antigens. J Exp Med 142: 165-179. http://dx.doi.org/10.1084/jem.142.1.165.
69. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarity Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O'Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome." Proc Natl Acad Sci U S A 102:13950-13955. http://dx.doi.org/10.1073/ pnas.0506758102.
70. Bentley RW, Leigh JA, CollinsMD. 1991. Intrageneric structure of Streptococcus based on comparative analysis of small-subunit rRNA sequences. Int J Syst Bacteriol 41:487-494. http://dx.doi.org/10.1099/00207713-41-4-487.
71. McShan WM, McLaughlin RE, Nordstrand A, Ferretti JJ. 1998. Vectors containing streptococcal bacteriophage integrases for site-specific gene insertion. Methods Cell Sci:51-57. http://dx.doi.org/10.1023/ A:1009773309163.