Bacterial cell-cell communication in the host via RRNPP peptide-binding regulators

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Perez Pascual, David ^a   Monnet, Véronique ^a   Gardan, Rozenn ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Cell cell communication; Commensalism; Firmicutes; Quorum sensing; Virulence

Indexed keywords

BACTERIAL PROTEIN; RRNPP PEPTIDE; UNCLASSIFIED DRUG;

BACILLUS CEREUS; BACTERIAL INFECTION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; CELL COMMUNICATION; COMMENSALISM; DNA TRANSCRIPTION; ENTEROCOCCUS; FIRMICUTES; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; NONHUMAN; QUORUM SENSING; REPRESSOR GENE; SHORT SURVEY; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION REGULATION;

EID: 84973443041     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00706     Document Type: Short Survey

References (75)

1. Agaisse, H., Gominet, M., Okstad, O. A., Kolsto, A. B., and Lereclus, D. (1999). PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis. Mol. Microbiol. 32, 1043-1053. doi: 10.1046/j.1365-2958.1999.01419.x
2. Antunes, L. C., and Ferreira, R. B. (2009). Intercellular communication in bacteria. Crit. Rev. Microbiol. 35, 69-80. doi: 10.1080/10408410902733946
3. Atkinson, S., and Williams, P. (2009). Quorum sensing and social networking in the microbial world. J. R. Soc. Interface 6, 959-978. doi: 10.1098/rsif.2009.0203
4. Bergman, N. H., Anderson, E. C., Swenson, E. E., Janes, B. K., Fisher, N., Niemeyer, M. M., et al. (2007). Transcriptional profiling of Bacillus anthracis during infection of host macrophages. Infect. Immun. 75, 3434-3444. doi: 10.1128/IAI.01345-06
5. Bottone, E. J. (2010). Bacillus cereus, a volatile human pathogen. Clin. Microbiol. Rev. 23, 382-398. doi: 10.1128/CMR.00073-09
6. Callegan, M. C., Kane, S. T., Cochran, D. C., Gilmore, M. S., Gominet, M., and Lereclus, D. (2003). Relationship of plcR-regulated factors to Bacillus endophthalmitis virulence. Infect. Immun. 71, 3116-3124. doi: 10.1128/IAI.71.6.3116-3124.2003
7. Chandler, J. R., Flynn, A. R., Bryan, E. M., and Dunny, G. M. (2005). Specific control of endogenous cCF10 pheromone by a conserved domain of the pCF10-encoded regulatory protein PrgY in Enterococcus faecalis. J. Bacteriol. 187, 4830-4843. doi: 10.1128/JB.187.14.4830-4843.2005
8. Chang, J. C., Jimenez, J. C., and Federle, M. J. (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
9. Chang, J. C., LaSarre, B., Jimenez, J. C., Aggarwal, C., and Federle, M. J. (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
10. Chow, J. W., Perri, M. B., Thal, L. A., and Zervos, M. J. (1993). Mobilization of the penicillinase gene in Enterococcus faecalis. Antimicrob. Agents Chemother. 37, 1187-1189. doi: 10.1128/AAC.37.5.1187
11. Chuang-Smith, O. N., Wells, C. L., Henry-Stanley, M. J., and Dunny, G. M. (2010). Acceleration of Enterococcus faecalis biofilm formation by aggregation substance expression in an ex vivo model of cardiac valve colonization. PLoS ONE 5:e15798. doi: 10.1371/journal.pone.0015798
12. Clewell, D. B., Weaver, K. E., Dunny, G. M., Coque, T. M., Francia, M. V., and Hayes, F. (2014). "Extrachromosomal and mobile elements in Enterococci: transmission, maintenance, and epidemiology," in Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, eds M. S. Gilmore, D. B. Clewell, Y. Ike, and N. Shankar (Boston, MA: Massachusetts Eye and Ear Infirmary).
13. Cook, L. C., and Federle, M. J. (2014). Peptide pheromone signaling in Streptococcus and Enterococcus. FEMS Microbiol. Rev. 38, 473-492. doi: 10.1111/1574-6976.12046
14. Cook, L. C., LaSarre, B., and Federle, M. J. (2013). Interspecies communication among commensal and pathogenic streptococci. MBio 4:e00382-13. doi: 10.1128/mBio.00382-13
15. Coque, T. M., and Murray, B. E. (1995). Identification of Enterococcus faecalis strains by DNA hybridization and pulsed-field gel electrophoresis. J. Clin. Microbiol. 33, 3368-3369.
16. Declerck, N., Bouillaut, L., Chaix, D., Rugani, N., Slamti, L., Hoh, F., et al. (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. doi: 10.1073/pnas.0704501104
17. Dubois, T., Faegri, K., Perchat, S., Lemy, C., Buisson, C., Nielsen-LeRoux, C., et al. (2012). Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog. 8:e1002629. doi: 10.1371/journal.ppat.1002629
18. Dubois, T., Perchat, S., Verplaetse, E., Gominet, M., Lemy, C., Aumont-Nicaise, M., et al. (2013). Activity of the Bacillus thuringiensis NprR-NprX cell-cell communication system is co-ordinated to the physiological stage through a complex transcriptional regulation. Mol. Microbiol. 88, 48-63. doi: 10.1111/mmi.12168
19. Dunny, G. M. (2007). The peptide pheromone-inducible conjugation system of Enterococcus faecalis plasmid pCF10: cell-cell signalling, gene transfer, complexity and evolution. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1185-1193. doi: 10.1098/rstb.2007.2043
20. Dunny, G. M. (2013). Enterococcal sex pheromones: signaling, social behavior, and evolution. Annu. Rev. Genet. 47, 457-482. doi: 10.1146/annurev-genet-111212-133449
21. Dunny, G. M., and Johnson, C. M. (2011). Regulatory circuits controlling enterococcal conjugation: lessons for functional genomics. Curr. Opin. Microbiol. 14, 174-180. doi: 10.1016/j.mib.2011.01.008
22. Fagerlund, A., Ween, O., Lund, T., Hardy, S. P., and Granum, P. E. (2004). Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology 150, 2689-2697. doi: 10.1099/mic.0.26975-0
23. Fleuchot, B., Gitton, C., Guillot, A., Vidic, J., Nicolas, P., Besset, C., et al. (2011). Rgg proteins associated with internalized small hydrophobic peptides: a new quorum-sensing mechanism in streptococci. Mol. Microbiol. 80, 1102-1119. doi: 10.1111/j.1365-2958.2011.07633.x
24. Fontaine, L., Boutry, C., de Frahan, M. H., Delplace, B., Fremaux, C., Horvath, P., et al. (2010). A novel pheromone quorum-sensing system controls the development of natural competence in Streptococcus thermophilus and Streptococcus salivarius. J. Bacteriol. 192, 1444-1454. doi: 10.1128/JB.01251-09
25. Fontaine, L., Goffin, P., Dubout, H., Delplace, B., Baulard, A., Lecat-Guillet, N., et al. (2013). Mechanism of competence activation by the ComRS signalling system in streptococci. Mol. Microbiol. 87, 1113-1132. doi: 10.1111/mmi.12157
26. Fontaine, L., Wahl, A., Flechard, M., Mignolet, J., and 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
27. Foxman, B., and Martin, E. T. (2015). Use of the microbiome in the practice of epidemiology: a primer on-omic technologies. Am. J. Epidemiol. 182, 1-8. doi: 10.1093/aje/kwv102
28. Gohar, M., Faegri, K., Perchat, S., Ravnum, S., Okstad, O. A., Gominet, M., et al. (2008). The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3:e2793. doi: 10.1371/journal.pone.0002793
29. Gohar, M., Okstad, O. A., Gilois, N., Sanchis, V., Kolsto, A. B., and Lereclus, D. (2002). Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2, 784-791. doi: 10.1002/1615-9861(200206)2:6<784::AID-PROT784>3.0.CO;2-R
30. Grenha, R., Slamti, L., Nicaise, M., Refes, Y., Lereclus, D., and Nessler, S. (2013). Structural basis for the activation mechanism of the PlcR virulence regulator by the quorum-sensing signal peptide PapR. Proc. Natl. Acad. Sci. U.S.A. 110, 1047-1052. doi: 10.1073/pnas.1213770110
31. Guillemet, E., Cadot, C., Tran, S. L., Guinebretiere, M. H., Lereclus, D., and Ramarao, N. (2010). The InhA metalloproteases of Bacillus cereus contribute concomitantly to virulence. J. Bacteriol. 192, 286-294. doi: 10.1128/JB.00264-09
32. Hardy, S. P., Lund, T., and Granum, P. E. (2001). CytK toxin of Bacillus cereus forms pores in planar lipid bilayers and is cytotoxic to intestinal epithelia. FEMS Microbiol. Lett. 197, 47-51. doi: 10.1111/j.1574-6968.2001.tb10581.x
33. Hirt, H., Schlievert, P. M., and Dunny, G. M. (2002). In vivo induction of virulence and antibiotic resistance transfer in Enterococcus faecalis mediated by the sex pheromone-sensing system of pCF10. Infect. Immun. 70, 716-723. doi: 10.1128/IAI.70.2.716-723.2002
34. Hoover, S. E., Perez, A. J., Tsui, H. C., Sinha, D., Smiley, D. L., DiMarchi, R. D., et al. (2015). A new quorum-sensing system (TprA/PhrA) for Streptococcus pneumoniae D39 that regulates a lantibiotic biosynthesis gene cluster. Mol. Microbiol. 97, 229-243. doi: 10.1111/mmi.13029
35. Huycke, M. M., Gilmore, M. S., Jett, B. D., and Booth, J. L. (1992). Transfer of pheromone-inducible plasmids between Enterococcus faecalis in the Syrian hamster gastrointestinal tract. J. Infect. Dis. 166, 1188-1191. doi: 10.1093/infdis/166.5.1188
36. Ibrahim, M., Guillot, A., Wessner, F., Algaron, F., Besset, C., Courtin, P., et al. (2007a). Control of the transcription of a short gene encoding a cyclic peptide in Streptococcus thermophilus: a new quorum-sensing system? J. Bacteriol. 189, 8844-8854. doi: 10.1128/JB.01057-07
37. Ibrahim, M., Nicolas, P., Bessieres, P., Bolotin, A., Monnet, V., and Gardan, R. (2007b). A genome-wide survey of short coding sequences in streptococci. Microbiology 153, 3631-3644. doi: 10.1099/mic.0.2007/006205-0
38. Jessberger, N., Dietrich, R., Bock, S., Didier, A., and Martlbauer, E. (2014). Bacillus cereus enterotoxins act as major virulence factors and exhibit distinct cytotoxicity to different human cell lines. Toxicon 77, 49-57. doi: 10.1016/j.toxicon.2013.10.028
39. Kolsto, A. B., Tourasse, N. J., and Okstad, O. A. (2009). What sets Bacillus anthracis apart from other Bacillus species? Annu. Rev. Microbiol. 63, 451-476. doi: 10.1146/annurev.micro.091208.073255
40. Kreft, B., Marre, R., Schramm, U., and Wirth, R. (1992). Aggregation substance of Enterococcus faecalis mediates adhesion to cultured renal tubular cells. Infect. Immun. 60, 25-30.
41. Lasarre, B., Aggarwal, C., and Federle, M. J. (2013). Antagonistic Rgg regulators mediate quorum sensing via competitive DNA binding in Streptococcus pyogenes. MBio 3:e00333-12. doi: 10.1128/mBio.00333-12
42. Le Doare, K., and Heath, P. T. (2013). An overview of global GBS epidemiology. Vaccine 31(Suppl. 4), D7-D12. doi: 10.1016/j.vaccine.2013.01.009
43. Marks, L. R., Mashburn-Warren, L., Federle, M. J., and Hakansson, A. P. (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
44. Mashburn-Warren, L., Morrison, D. A., and Federle, M. J. (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
45. Mashburn-Warren, L., Morrison, D. A., and Federle, M. J. (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
46. Monnet, V., and Gardan, R. (2015). Quorum-sensing regulators in Gram-positive bacteria: 'cherchez le peptide.' Mol. Microbiol. 97, 181-184. doi: 10.1111/mmi.13060
47. Olmsted, S. B., Dunny, G. M., Erlandsen, S. L., and Wells, C. L. (1994). A plasmid-encoded surface protein on Enterococcus faecalis augments its internalization by cultured intestinal epithelial cells. J. Infect. Dis. 170, 1549-1556. doi: 10.1093/infdis/170.6.1549
48. Parashar, V., Aggarwal, C., Federle, M. J., and Neiditch, M. B. (2015). Rgg protein structure-function and inhibition by cyclic peptide compounds. Proc. Natl. Acad. Sci. U.S.A. 112, 5177-5182. doi: 10.1073/pnas.1500357112
49. Perchat, S., Dubois, T., Zouhir, S., Gominet, M., Poncet, S., Lemy, C., et al. (2011). A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol. Microbiol. 82, 619-633. doi: 10.1111/j.1365-2958.2011.07839.x
50. 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:e02306-14. doi: 10.1128/mBio.02306-14
51. Pottathil, M., and Lazazzera, B. A. (2003). The extracellular Phr peptide-Rap phosphatase signaling circuit of Bacillus subtilis. Front. Biosci. 8, d32-d45. doi: 10.2741/913
52. Rakita, R. M., Quan, V. C., Jacques-Palaz, K., Singh, K. V., Arduino, R. C., Mee, M., et al. (2000). Specific antibody promotes opsonization and PMN-mediated killing of phagocytosis-resistant Enterococcus faecium. FEMS Immunol. Med. Microbiol. 28, 291-299. doi: 10.1111/j.1574-695X.2000.tb01489.x
53. Ramarao, N., and Lereclus, D. (2006). Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively. Microbes Infect. 8, 1483-1491. doi: 10.1016/j.micinf.2006.01.005
54. Ramarao, N., and Sanchis, V. (2013). The pore-forming haemolysins of Bacillus cereus: a review. Toxins (Basel) 5, 1119-1139. doi: 10.3390/toxins5061119
55. Rice, A. J., Woo, J. K., Khan, A., Szypulinski, M. Z., Johnson, M. E., Lee, H., et al. (2015). Over-expression, purification, and confirmation of Bacillus anthracis transcriptional regulator NprR. Protein Expr. Purif. doi: 10.1016/j.pep.2015.08.030 [Epub ahead of print]
56. Rocha-Estrada, J., Aceves-Diez, A. E., Guarneros, G., and de la Torre, M. (2010). The RNPP family of quorum-sensing proteins in Gram-positive bacteria. Appl. Microbiol. Biotechnol. 87, 913-923. doi: 10.1007/s00253-010-2651-y
57. Salamitou, S., Ramisse, F., Brehelin, M., Bourguet, D., Gilois, N., Gominet, M., et al. (2000). The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 146, 2825-2832. doi: 10.1099/00221287-146-11-2825
58. Samen, U. M., Eikmanns, B. J., and Reinscheid, D. J. (2006). The transcriptional regulator RovS controls the attachment of Streptococcus agalactiae to human epithelial cells and the expression of virulence genes. Infect. Immun. 74, 5625-5635. doi: 10.1128/IAI.00667-06
59. Sartingen, S., Rozdzinski, E., Muscholl-Silberhorn, A., and Marre, R. (2000). Aggregation substance increases adherence and internalization, but not translocation, of Enterococcus faecalis through different intestinal epithelial cells in vitro. Infect. Immun. 68, 6044-6047. doi: 10.1128/IAI.68.10.6044-6047.2000
60. Schlievert, P. M., Gahr, P. J., Assimacopoulos, A. P., Dinges, M. M., Stoehr, J. A., Harmala, J. W., et al. (1998). Aggregation and binding substances enhance pathogenicity in rabbit models of Enterococcus faecalis endocarditis. Infect. Immun. 66, 218-223.
61. Schubert, A., Zakikhany, K., Pietrocola, G., Meinke, A., Speziale, P., Eikmanns, B. J., et al. (2004). The fibrinogen receptor FbsA promotes adherence of Streptococcus agalactiae to human epithelial cells. Infect. Immun. 72, 6197-6205. doi: 10.1128/IAI.72.11.6197-6205.2004
62. Shak, J. R., Ludewick, H. P., Howery, K. E., Sakai, F., Yi, H., Harvey, R. M., et al. (2013). Novel role for the Streptococcus pneumoniae toxin pneumolysin in the assembly of biofilms. MBio 4:e00655-13. doi: 10.1128/mBio.00655-13
63. Slamti, L., and Lereclus, D. (2002). A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J. 21, 4550-4559. doi: 10.1093/emboj/cdf450
64. Slamti, L., Perchat, S., Huillet, E., and Lereclus, D. (2014). Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins (Basel) 6, 2239-2255. doi: 10.3390/toxins6082239
65. Stenfors Arnesen, L. P., Fagerlund, A., and Granum, P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32, 579-606. doi: 10.1111/j.1574-6976.2008.00112.x
66. Sussmuth, S. D., Muscholl-Silberhorn, A., Wirth, R., Susa, M., Marre, R., and Rozdzinski, E. (2000). Aggregation substance promotes adherence, phagocytosis, and intracellular survival of Enterococcus faecalis within human macrophages and suppresses respiratory burst. Infect. Immun. 68, 4900-4906. doi: 10.1128/IAI.68.9.4900-4906.2000
67. Tran, S. L., Guillemet, E., Ngo-Camus, M., Clybouw, C., Puhar, A., Moris, A., et al. (2011). Haemolysin II is a Bacillus cereus virulence factor that induces apoptosis of macrophages. Cell Microbiol. 13, 92-108. doi: 10.1111/j.1462-5822.2010.01522.x
68. van Opijnen, T., and Camilli, A. (2012). A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res. 22, 2541-2551. doi: 10.1101/gr.137430.112
69. Verplaetse, E., Slamti, L., Gohar, M., and Lereclus, D. (2015). Cell differentiation in a Bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection. MBio 6:e00138-15. doi: 10.1128/mBio.00138-15
70. Waters, C. M., Antiporta, M. H., Murray, B. E., and Dunny, G. M. (2003). Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185, 3613-3623. doi: 10.1128/JB.185.12.3613-3623.2003
71. Waters, C. M., Hirt, H., McCormick, J. K., Schlievert, P. M., Wells, C. L., and Dunny, G. M. (2004). An amino-terminal domain of Enterococcus faecalis aggregation substance is required for aggregation, bacterial internalization by epithelial cells and binding to lipoteichoic acid. Mol. Microbiol. 52, 1159-1171. doi: 10.1111/j.1365-2958.2004.04045.x
72. Wells, C. L., Moore, E. A., Hoag, J. A., Hirt, H., Dunny, G. M., and Erlandsen, S. L. (2000). Inducible expression of Enterococcus faecalis aggregation substance surface protein facilitates bacterial internalization by cultured enterocytes. Infect. Immun. 68, 7190-7194. doi: 10.1128/IAI.68.12.7190-7194.2000
73. Wilkening, R. V., Chang, J. C., and Federle, M. J. (2015). PepO, a CovRS-controlled endopeptidase, disrupts Streptococcus pyogenes quorum sensing. Mol. Microbiol. 99, 71-87. doi: 10.1111/mmi.13216
74. Zheng, F., Ji, H., Cao, M., Wang, C., Feng, Y., Li, M., et al. (2011). Contribution of the Rgg transcription regulator to metabolism and virulence of Streptococcus suis serotype 2. Infect. Immun. 79, 1319-1328. doi: 10.1128/IAI.00193-10
75. Zutkis, A. A., Anbalagan, S., Chaussee, M. S., and Dmitriev, A. V. (2014). Inactivation of the Rgg2 transcriptional regulator ablates the virulence of Streptococcus pyogenes. PLoS ONE 9:e114784. doi: 10.1371/journal.pone.0114784