Signal transduction through CsrRS confers an invasive phenotype in group a Streptococcus

PLoS Pathogens

Volumn 7, Issue 10, 2011, Pages

  Tran Winkler, Hien J ^a,b   Love, John F ^a,b,c   Gryllos, Ioannis ^a,b   Wessels, Michael R ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE SDA1; EXOTOXIN; EXOTOXIN A; HYALURONIC ACID; LYSINE; MAGNESIUM; POLYSACCHARIDE; PROTEIN HISTIDINE KINASE; STREPTOLYSIN O; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CSRR; TRANSCRIPTION FACTOR CSRS; UNCLASSIFIED DRUG; VIRULENCE FACTOR; ANTIMICROBIAL CATIONIC PEPTIDE; BACTERIAL PROTEIN; CAP18 LIPOPOLYSACCHARIDE BINDING PROTEIN; CAP18 LIPOPOLYSACCHARIDE-BINDING PROTEIN; CSRR PROTEIN, STREPTOCOCCUS PYOGENES; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVITY; GAIN OF FUNCTION MUTATION; GENE ACTIVATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MOLECULAR CLONING; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REGULON; SIGNAL TRANSDUCTION; STREPTOCOCCUS GROUP A; STREPTOCOCCUS INFECTION; TRANSCRIPTION REGULATION; UPREGULATION; DRUG EFFECT; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; STREPTOCOCCUS PYOGENES;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS SP. 'GROUP A';

ANTIMICROBIAL CATIONIC PEPTIDES; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PHENOTYPE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; UP-REGULATION; VIRULENCE FACTORS;

EID: 80055079778     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002361     Document Type: Article

References (43)

1. Tanz RR, Shulman ST, (1998) Streptococcal pharyngitis: the carrier state, definition, and management. Pediatr Ann 27: 281-285.
2. Wessels MR, (2011) Clinical practice. Streptococcal pharyngitis. N Engl J Med 364: 648-655.
3. Eriksson BK, Andersson J, Holm SE, Norgren M, (1998) Epidemiological and clinical aspects of invasive group A streptococcal infections and the streptococcal toxic shock syndrome. Clin Infect Dis 27: 1428-1436.
4. Stevens DL, (2000) Streptococcal toxic shock syndrome associated with necrotizing fasciitis. Ann Rev Med 51: 271-288.
5. Cunningham MW, (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13: 470-511.
6. Kreikemeyer B, McIver KS, Podbielski A, (2003) Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol 11: 224-232.
7. Beier D, Gross R, (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9: 143-152.
8. Laub MT, Goulian M, (2007) Specificity in two-component signal transduction pathways. Ann Rev Genetics 41: 121-145.
9. Dalton TL, Collins JT, Barnett TC, Scott JR, (2006) RscA, a member of the MDR1 family of transporters, is repressed by CovR and required for growth of Streptococcus pyogenes under heat stress. J Bacteriol 188: 77-85.
10. Graham MR, Smoot LM, Migliaccio CA, Virtaneva K, Sturdevant DE, et al. (2002) Virulence control in group A Streptococcus by a two-component gene regulatory system: Global expression profiling and in vivo infection modeling. Proc Natl Acad Sci U S A 99: 13855-13860.
11. Gryllos I, Grifantini R, Colaprico A, Jiang S, Deforce E, et al. (2007) Mg(2+) signalling defines the group A streptococcal CsrRS (CovRS) regulon. Mol Microbiol 65: 671-683.
12. Levin JC, Wessels MR, (1998) Identification of csrR/csrS, a genetic locus that regulates hyaluronic acid capsule synthesis in group A Streptococcus. Mol Microbiol 30: 209-219.
13. Dalton TL, Scott JR, (2004) CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J Bacteriol 186: 3928-3937.
14. Churchward G, (2007) The two faces of Janus: virulence gene regulation by CovR/S in group A streptococci. Mol Microbiol 64: 34-41.
15. Gusa AA, Gao J, Stringer V, Churchward G, Scott JR, (2006) Phosphorylation of the group A Streptococcal CovR response regulator causes dimerization and promoter-specific recruitment by RNA polymerase. J Bacteriol 188: 4620-4626.
16. Gryllos I, Levin JC, Wessels MR, (2003) The CsrR/CsrS two-component system of group A Streptococcus responds to environmental Mg2+. Proc Natl Acad Sci U S A 100: 4227-4232.
17. Gryllos I, Tran-Winkler HJ, Cheng MF, Chung H, Bolcome R, 3rd, et al. (2008) Induction of group A Streptococcus virulence by a human antimicrobial peptide. Proc Natl Acad Sci U S A 105: 16755-16760.
18. Engleberg NC, Heath A, Miller A, Rivera C, DiRita VJ, (2001) Spontaneous mutations in the CsrRS two-component regulatory system of Streptococcus pyogenes result in enhanced virulence in a murine model of skin and soft tissue infection. J Infect Dis 183: 1043-1054.
19. Ikebe T, Ato M, Matsumura T, Hasegawa H, Sata T, et al. (2010) Highly frequent mutations in negative regulators of multiple virulence genes in group A streptococcal toxic shock syndrome isolates. PLoS Pathog 6: e1000832.
20. Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM, (2006) Genome-wide analysis of group a streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog 2: e5.
21. Walker MJ, Hollands A, Sanderson-Smith ML, Cole JN, Kirk JK, et al. (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13: 981-985.
22. Aziz RK, Kotb M, (2008) Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 14: 1511-1517.
23. Cleary PP, Kaplan EL, Handley JP, Wlazlo A, Kim MH, et al. (1992) Clonal basis for resurgence of serious Streptococcus pyogenes disease in the 1980s. Lancet 339: 518-521.
24. Musser JM, Kapur V, Szeto JXP, Swanson D, Martin D, (1995) Genetic diversity and relationships among Streptococcus pyogenes strains expressing serotype M1 protein: recent intercontinental spread of a subclone causing episodes of invasive disease. Infect Immun 63: 994-1003.
25. Sumby P, Porcella SF, Madrigal AG, Barbian KD, Virtaneva K, et al. (2005) Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 192: 771-782.
26. Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, et al. (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 98: 4658-4663.
27. Beres SB, Sylva GL, Barbian KD, Lei B, Hoff JS, et al. (2002) Genome sequence of a serotype M3 strain of group A Streptococcus: phage- encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 99: 10078-10083.
28. Sumby P, Barbian KD, Gardner DJ, Whitney AR, Welty DM, et al. (2005) Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci U S A 102: 1679-1684.
29. Groisman EA, (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183: 1835-1842.
30. Waldburger CD, Sauer RT, (1996) Signal detection by the PhoQ sensor-transmitter. Characterization of the sensor domain and a response-impaired mutant that identifies ligand- binding determinants. J Biol Chem 271: 26630-26636.
31. Lancefield RC, (1962) Current knowledge of the type specific M antigens of group A streptococci. J Immunol 89: 307-313.
32. Varughese KI, (2002) Molecular recognition of bacterial phosphorelay proteins. Curr Opin Microbiol 5: 142-148.
33. Lukat GS, Lee BH, Mottonen JM, Stock AM, Stock JB, (1991) Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J Biol Chem 266: 8348-8354.
34. Aziz RK, Edwards RA, Taylor WW, Low DE, McGeer A, et al. (2005) Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 187: 3311-3318.
35. Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, et al. (2006) DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16: 396-400.
36. Raeder R, Woischnik M, Podbielski A, Boyle MD, (1998) A secreted streptococcal cysteine protease can cleave a surface-expressed M1 protein and alter the immunoglobulin binding properties. Res Microbiol 149: 539-548.
37. Simon D, Ferretti JJ, (1991) Electrotransformation of Streptococcus pyogenes with plasmid and linear DNA. FEMS Microbiol Lett 66: 219-224.
38. Ashbaugh CD, Warren HB, Carey VJ, Wessels MR, (1998) Molecular analysis of the role of the group A streptococcal cysteine protease, hyaluronic acid capsule, and M protein in a murine model of human invasive soft-tissue infection. J Clin Invest 102: 550-560.
39. Sawai MV, Waring AJ, Kearney WR, McCray PB Jr, Forsyth WR, et al. (2002) Impact of single-residue mutations on the structure and function of ovispirin/novispirin antimicrobial peptides. Protein Eng 15: 225-232.
40. Perez-Casal J, Price JA, Maguin E, Scott JR, (1993) An M protein with a single C repeat prevents phagocytosis of Streptococcus pyogenes: use of a temperature-sensitive shuttle vector to deliver homologous sequences to the chromosome of S. pyogenes. Mol Microbiol 8: 809-819.
41. Michos A, Gryllos I, Hakansson A, Srivastava A, Kokkotou E, et al. (2006) Enhancement of streptolysin O activity and intrinsic cytotoxic effects of the group A streptococcal toxin, NAD-glycohydrolase. J Biol Chem 281: 8216-8223.
42. Aziz RK, Ismail SA, Park HW, Kotb M, (2004) Post-proteomic identification of a novel phage-encoded streptodornase, Sda1, in invasive M1T1 Streptococcus pyogenes. Mol Micobiol 54: 184-197.
43. Gryllos I, Grifantini R, Colaprico A, Cary ME, Hakansson A, et al. (2008) PerR confers phagocytic killing resistance and allows pharyngeal colonization by group A Streptococcus. PLoS Pathog 4: e1000145.