PptAB exports Rgg quorum-sensing peptides in Streptococcus

PLoS ONE

Volumn 11, Issue 12, 2016, Pages

  Chang, Jennifer C ^a   Federle, Michael J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PEPTIDE; PHEROMONE; PROTEIN PPTAB; RGG QUORUM SENSING PEPTIDE; SIGX INDUCING PEPTIDE; UNCLASSIFIED DRUG; ABC TRANSPORTER; BACTERIAL SECRETION SYSTEM; RGG PROTEIN, STREPTOCOCCUS; TRANSACTIVATOR PROTEIN; TRANSPOSON;

ARTICLE; BACTERIAL GENE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DELETION MUTANT; GENE LOCUS; GENE MAPPING; GENETIC CONSERVATION; GENETIC SCREENING; GENETIC TRANSCRIPTION; GENOTYPE; MUTAGENESIS; NONHUMAN; PPTAB GENE; PROTEIN LOCALIZATION; PROTEIN SECRETION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; START CODON; STREPTOCOCCUS MUTANS; TRANSPOSON; TRANSPOSON MUTAGENESIS; BACTERIAL SECRETION SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; QUORUM SENSING; SECRETION (PROCESS); STREPTOCOCCUS PYOGENES;

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; DNA TRANSPOSABLE ELEMENTS; MUTAGENESIS, INSERTIONAL; PEPTIDES; PROTEIN TRANSPORT; QUORUM SENSING; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PYOGENES; TRANS-ACTIVATORS;

EID: 85006932921     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0168461     Document Type: Article

References (32)

1. Chaussee MS, Ajdic D, Ferretti JJ (1999) The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production. Infect Immun 67: 1715-1722. PMID: 10085009
2. Hollands A, Aziz RK, Kansal R, Kotb M, Nizet V, Walker MJ (2008) A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PLoS One 3: e4102. doi: 10.1371/journal.pone.0004102 PMID: 19116661
3. Lyon WR, Gibson CM, Caparon MG (1998) A role for trigger factor and an rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. Embo J 17: 6263-6275. doi: 10.1093/emboj/17.21.6263 PMID: 9799235
4. Chang JC, Jimenez JC, Federle MJ (2015) Induction of a quorum sensing pathway by environmental signals enhances group A streptococcal resistance to lysozyme. Mol Microbiol 97: 1097-1113. doi: 10. 1111/mmi.13088 PMID: 26062094
5. 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. doi: 10.1371/journal.ppat.1002190 PMID: 21829369
6. 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. doi: 10.1128/JB. 00830-12 PMID: 22730123
7. Varahan S, Harms N, Gilmore MS, Tomich JM, Hancock LE (2014) An ABC transporter is required for secretion of peptide sex pheromones in Enterococcus faecalis. MBio 5: e01726-01714. doi: 10.1128/mBio.01726-14 PMID: 25249282
8. Perez-Pascual D, Gaudu P, Fleuchot B, Besset C, Rosinski-Chupin I, Guillot A, et al. (2015) RovS and its associated signaling peptide form a cell-to-cell communication system required for Streptococcus agalactiae pathogenesis. MBio 6.
9. Mashburn-Warren L, Morrison DA, Federle MJ (2010) A novel double-tryptophan peptide pheromone controls competence in Streptococcus spp. via an Rgg regulator. Mol Microbiol 78: 589-606. doi: 10. 1111/j.1365-2958.2010.07361.x PMID: 20969646
10. Fontaine L, Wahl A, Flechard M, Mignolet J, Hols P (2015) Regulation of competence for natural transformation in streptococci. Infect Genet Evol 33: 343-360. doi: 10.1016/j.meegid.2014.09.010 PMID: 25236918
11. Shanker E, Morrison DA, Talagas A, Nessler S, Federle MJ, Prehna G (2016) Pheromone recognition and selectivity by ComR proteins among Streptococcus species. PLoS Pathog 12: e1005979. doi: 10. 1371/journal.ppat.1005979 PMID: 27907154
12. Khan R, Rukke HV, Ricomini Filho AP, Fimland G, Arntzen MO, Thiede B, et al. (2012) Extracellular identification of a processed type II ComR/ComS pheromone of Streptococcus mutans. J Bacteriol 194: 3781-3788. doi: 10.1128/JB.00624-12 PMID: 22609914
13. 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. doi: 10.1074/jbc.M114.583989 PMID: 24958729
14. Hale JD, Heng NC, Jack RW, Tagg JR (2005) Identification of nlmTE, the locus encoding the ABC transport system required for export of nonlantibiotic mutacins in Streptococcus mutans. J Bacteriol 187: 5036-5039. doi: 10.1128/JB.187.14.5036-5039.2005 PMID: 15995224
15. Hidalgo-Grass C, Ravins M, Dan-Goor M, Jaffe J, Moses AE, Hanski E (2002) A locus of group A Streptococcus involved in invasive disease and DNA transfer. Mol Microbiol 46: 87-99. PMID: 12366833
16. van de Rijn I, Kessler RE (1980) Growth characteristics of group A streptococci in a new chemically defined medium. Infect Immun 27: 444-448. PMID: 6991416
17. Howell-Adams B, Seifert HS (2000) Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37: 1146-1158. PMID: 10972832
18. Degnan BA, Fontaine MC, Doebereiner AH, Lee JJ, Mastroeni P, Dougan G, et al. (2000) Characterization of an isogenic mutant of Streptococcus pyogenes Manfredo lacking the ability to make streptococcal acid glycoprotein. Infect Immun 68: 2441-2448. PMID: 10768929
19. Wilkening RV, Chang JC, Federle MJ (2016) PepO, a CovRS-controlled endopeptidase, disrupts Streptococcus pyogenes quorum sensing. Mol Microbiol 99: 71-87. doi: 10.1111/mmi.13216 PMID: 26418177
20. Le Breton Y, McIver KS (2013) Genetic manipulation of Streptococcus pyogenes (the Group A Streptococcus, GAS). Curr Protoc Microbiol 30: Unit 9D 3.
21. Lasarre B, Aggarwal C, Federle MJ (2013) Antagonistic Rgg regulators mediate quorum sensing via competitive DNA binding in Streptococcus pyogenes. MBio 3.
22. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, et al. (2010) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38: D396-400. doi: 10.1093/nar/gkp919 PMID: 19906701
23. LaSarre B, Chang JC, Federle MJ (2013) Redundant group a streptococcus signaling peptides exhibit unique activation potentials. J Bacteriol 195: 4310-4318. doi: 10.1128/JB.00684-13 PMID: 23873915
24. Desai K, Mashburn-Warren L, Federle MJ, Morrison DA (2012) Development of competence for genetic transformation of Streptococcus mutans in a chemically defined medium. J Bacteriol 194: 3774-3780. doi: 10.1128/JB.00337-12 PMID: 22609913
25. Marks LR, Mashburn-Warren L, Federle MJ, Hakansson AP (2014) Streptococcus pyogenes biofilm growth in vitro and in vivo and its role in colonization, virulence, and genetic exchange. J Infect Dis 210: 25-34. doi: 10.1093/infdis/jiu058 PMID: 24465015
26. Wenderska IB, Lukenda N, Cordova M, Magarvey N, Cvitkovitch DG, Senadheera DB (2012) A novel function for the competence inducing peptide, XIP, as a cell death effector of Streptococcus mutans. FEMS Microbiol Lett 336: 104-112. doi: 10.1111/j.1574-6968.2012.02660.x PMID: 22900705
27. Guo Q, Ahn SJ, Kaspar J, Zhou X, Burne RA (2014) Growth phase and pH influence peptide signaling for competence development in Streptococcus mutans. J Bacteriol 196: 227-236. doi: 10.1128/JB. 00995-13 PMID: 24163340
28. Gardan R, Besset C, Gitton C, Guillot A, Fontaine L, Hols P, et al. (2013) Extracellular life cycle of ComS, the competence-stimulating peptide of Streptococcus thermophilus. J Bacteriol 195: 1845-1855. doi: 10.1128/JB.02196-12 PMID: 23396911
29. Leskela S, Kontinen VP, SarvasM (1996) Molecular analysis of an operon in Bacillus subtilis encoding a novel ABC transporter with a role in exoprotein production, sporulation and competence. Microbiology 142 (Pt 1): 71-77.
30. Leskela S, Wahlstrom E, Hyyrylainen HL, Jacobs M, Palva A, Sarvas M, et al. (1999) Ecs, an ABC transporter of Bacillus subtilis: dual signal transduction functions affecting expression of secreted proteins as well as their secretion. Mol Microbiol 31: 533-543. PMID: 10027970
31. Kontinen VP, SarvasM (1988) Mutants of Bacillus subtilis defective in protein export. J Gen Microbiol 134: 2333-2344. doi: 10.1099/00221287-134-8-2333 PMID: 3150980
32. Jonsson IM, Juuti JT, Francois P, AlMajidi R, Pietiainen M, Girard M, et al. (2010) Inactivation of the Ecs ABC transporter of Staphylococcus aureus attenuates virulence by altering composition and function of bacterial wall. PLoS One 5: e14209. doi: 10.1371/journal.pone.0014209 PMID: 21151985