A natural inactivating mutation in the CovS component of the CovRS regulatory operon in a pattern D streptococcal pyogenes strain influences virulence-associated genes

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6561-6573

  Liang, Zhong ^a   Zhang, Yueling ^a   Agrahari, Garima ^a   Chandrahas, Vishwanatha ^a   Glinton, Kristofor ^a   Donahue, Deborah L ^a   Balsara, Rashna D ^a   Ploplis, Victoria A ^a   Castellino, Francis J ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL SURFACES; DOWN-REGULATION; EXTRACELLULAR PROTEASE; HIGH AFFINITY; ISOGENIC STRAIN; MINIMAL EFFECTS; REGULATORY SYSTEMS; STREPTOCOCCUS PYOGENES; TWO-COMPONENT; VIRULENCE GENE;

HYALURONIC ACID; ORGANIC ACIDS; PHOSPHORYLATION; PROTEINS;

GENES;

BACTERIAL PROTEIN; CELL RECEPTOR; GENOMIC DNA; HYALURONIC ACID; PG BINDING GROUP A STREPTOCOCCAL M PROTEIN; PLASMIN; PLASMIN RECEPTOR; PLASMINOGEN; STREPTOCOCCAL PYROGENIC EXOTOXIN B; STREPTOKINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; CELL SURFACE; CONTROLLED STUDY; COVRS GENE; COVS GENE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE REGULATORY NETWORK; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULON; SIGNAL TRANSDUCTION; STREPTOCOCCUS PYOGENES; UPREGULATION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; EXOTOXINS; GENES, BACTERIAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MUTATION; OPERON; REPRESSOR PROTEINS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; STREPTOKINASE; VIRULENCE FACTORS;

EID: 84874771761     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.442657     Document Type: Article

References (64)

1. Smeesters, P. R., McMillan, D. J., and Sriprakash, K. S. (2010) The streptococcal M protein. A highly versatile molecule. Trends Microbiol. 18, 275-282
2. Perez-Casal, J., Caparon, M. G., and Scott, J. R. (1991) Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems. J. Bacteriol. 173, 2617-2624
3. Hondorp, E. R., and McIver, K. S. (2007) The Mga virulence regulon: infection where the grass is greener. Mol. Microbiol. 66, 1056-1065
4. Stenberg, L., O'Toole, P., and Lindahl, G. (1992) Many group A streptococcal strains express two different immunoglobulin-binding proteins, encoded by closely linked genes. Characterization of the proteins expressed by four strains of different M-type. Mol. Microbiol. 6, 1185-1194
5. Simpson, W. J., LaPenta, D., Chen, C., and Cleary, P. P. (1990) Coregulation of type 12Mprotein and streptococcal C5a peptidase genes in group A streptococci: evidence for a virulence regulon controlled by the virR locus. J. Bacteriol. 172, 696-700
6. Roberts, S. A., Churchward, G. G., and Scott, J. R. (2007) Unraveling the regulatory network in Streptococcus pyogenes. The global response regulator CovR represses rivR directly. J. Bacteriol. 189, 1459-1463
7. Bisno, A. L., Brito, M. O., and Collins, C. M. (2003) Molecular basis of group A streptococcal virulence. Lancet Infect. Dis. 3, 191-200
8. Kalia, A., and Bessen, D. E. (2004) Natural selection and evolution of streptococcal virulence genes involved in tissue-specific adaptations. J. Bacteriol. 186, 110-121
9. Lähteenmäki, K., Kuusela, P., and Korhonen, T. K. (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552
10. McKay, F. C., McArthur, J. D., Sanderson-Smith, M. L., Gardam, S., Currie, B. J., Sriprakash, K. S., Fagan, P. K., Towers, R. J., Batzloff, M. R., Chhatwal, G. S., Ranson, M., and Walker, M. J. (2004) Plasminogen binding by groupAstreptococcal isolates from a region of hyperendemicity for streptococcal skin infection and a high incidence of invasive infection. Infect. Immun. 72, 364-370
11. Berge, A., and Sjöbring, U. (1993) PAM, a novel plasminogen-binding protein from Streptococcus pyogenes. J. Biol. Chem. 268, 25417-25424
12. Winram, S. B., and Lottenberg, R. (1996) The plasmin-binding protein Plr of group A streptococci is identified as glyceraldehyde-3-phosphate dehydrogenase. Microbiology 142, 2311-2320
13. Pancholi, V., and Fischetti, V. A. (1998) α-Enolase, a novel strong plasmin-(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273, 14503-14515
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. Kondo, H., Nakagawa, A., Nishihira, J., Nishimura, Y., Mizuno, T., and Tanaka, I. (1997) Escherichia coli positive regulator OmpR has a large loop structure at the putative RNA polymerase interaction site. Nat. Struct. Biol. 4, 28-31
16. Dalton, T. L., and Scott, J. R. (2004) CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J. Bacteriol. 186, 3928-3937
17. Gryllos, I., Levin, J. C., and Wessels, M. R. (2003) The CsrR/CsrS twocomponent system of group A Streptococcus responds to environmental Mg2+. Proc. Natl. Acad. Sci. U.S.A. 100, 4227-4232
18. Alves, R., and Savageau, M. A. (2003) Comparative analysis of prototype two-component systems with either bifunctional or monofunctional sensors. Differences in molecular structure and physiological function. Mol. Microbiol. 48, 25-51
19. Wistedt, A. C., Kotarsky, H., Marti, D., Ringdahl, U., Castellino, F. J., Schaller, J., and Sjöbring, U. (1998) Kringle 2 mediates high affinity binding of plasminogen to an internal sequence in streptococcal surface protein PAM. J. Biol. Chem. 273, 24420-24424
20. Ben Nasr, A., Wistedt, A., Ringdahl, U., and Sjöbring, U. (1994) Streptokinase activates plasminogen bound to human group C and G streptococci through M-like proteins. Eur. J. Biochem. 222, 267-276
21. Bessen, D. E., Sotir, C. M., Readdy, T. L., and Hollingshead, S. K. (1996) Genetic correlates of throat and skin isolates of group A streptococci. J. Infect. Dis. 173, 896-900
22. Sanderson-Smith, M. L., Dinkla, K., Cole, J. N., Cork, A. J., Maamary, P. G., McArthur, J. D., Chhatwal, G. S., and Walker, M. J. (2008) M proteinmediated plasminogen binding is essential for the virulence of an invasive Streptococcus pyogenes isolate. FASEB J. 22, 2715-2722
23. Roberts, S. A., and Scott, J. R. (2007) RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon. Mol. Microbiol. 66, 1506-1522
24. Schmittgen, T. D., and Livak, K. J. (2008) Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 3, 1101-1108
25. Enright, M. C., Spratt, B. G., Kalia, A., Cross, J. H., and Bessen, D. E. (2001) Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect. Immun. 69, 2416-2427
26. Cole, J. N., McArthur, J. D., McKay, F. C., Sanderson-Smith, M. L., Cork, A. J., Ranson, M., Rohde, M., Itzek, A., Sun, H., Ginsburg, D., Kotb, M., Nizet, V., Chhatwal, G. S., and Walker, M. J. (2006) Trigger for group A streptococcal M1T1 invasive disease. FASEB J. 20, 1745-1747
27. Zhang, Y., Liang, Z., Hsueh, H. T., Ploplis, V. A., and Castellino, F. J. (2012) Characterization of streptokinases from group A streptococci reveals a strong functional relationship that supports the coinheritance of plasminogen- binding M protein and cluster 2b streptokinase. J. Biol. Chem. 287, 42093-42103
28. Nilsen, S. L., and Castellino, F. J. (1999) Expression of human plasminogen in Drosophila Schneider S2 cells. Protein Expr. Purif. 16, 136-143
29. Hytönen, J., Haataja, S., Gerlach, D., Podbielski, A., and Finne, J. (2001) The SpeB virulence factor of Streptococcus pyogenes, a multifunctional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol. Microbiol. 39, 512-519
30. Zimmerlein, B., Park, H. S., Li, S., Podbielski, A., and Cleary, P. P. (2005) The M protein is dispensable for maturation of streptococcal cysteine protease SpeB. Infect. Immun. 73, 859-864
31. Schrager, H. M., Rheinwald, J. G., and Wessels, M. R. (1996) Hyaluronic acid capsule and the role of streptococcal entry into keratinocytes in invasive skin infection. J. Clin. Invest. 98, 1954-1958
32. Sun, H., Ringdahl, U., Homeister, J. W., Fay, W. P., Engleberg, N. C., Yang, A. Y., Rozek, L. S., Wang, X., Sjöbring, U., and Ginsburg, D. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305, 1283-1286
33. Ringdahl, U., Svensson, M., Wistedt, A. C., Renné, T., Kellner, R., Müller- Esterl, W., and Sjöbring, U. (1998) Molecular co-operation between protein PAM and streptokinase for plasmin acquisition by Streptococcus pyogenes. J. Biol. Chem. 273, 6424-6430
34. Liang, Z., Breman, A. M., Grimes, B. R., and Rosen, E. D. (2008) Identifying and genotyping transgene integration loci. Transgenic Res. 17, 979-983
35. Kreikemeyer, B., McIver, K. S., and Podbielski, A. (2003) Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen-host interactions. Trends Microbiol. 11, 224-232
36. Ferretti, J. J., McShan, W. M., Ajdic, D., Savic, D. J., Savic, G., Lyon, K., Primeaux, C., Sezate, S., Suvorov, A. N., Kenton, S., Lai, H. S., Lin, S. P., Qian, Y., Jia, H. G., Najar, F. Z., Ren, Q., Zhu, H., Song, L., White, J., Yuan, X., Clifton, S. W., Roe, B. A., and McLaughlin, R. (2001) Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc. Natl. Acad. Sci. U.S.A. 98, 4658-4663
37. Cnudde, S. E., Prorok, M., Castellino, F. J., and Geiger, J. H. (2006) X-ray crystallographic structure of the angiogenesis inhibitor, angiostatin, bound to a peptide from the group A streptococcal surface protein PAM. Biochemistry 45, 11052-11060
38. Fu, Q., Figuera-Losada, M., Ploplis, V. A., Cnudde, S., Geiger, J. H., Prorok, M., and Castellino, F. J. (2008) The lack of binding of VEK-30, an internal peptide from the group A streptococcal M-like protein, PAM, to murine plasminogen is due to two amino acid replacements in the plasminogen kringle-2 domain. J. Biol. Chem. 283, 1580-1587
39. Schenone, M. M., Warder, S. E., Martin, J. A., Prorok, M., and Castellino, F. J. (2000) An internal histidine residue from the bacterial surface protein, PAM, mediates its binding to the kringle-2 domain of human plasminogen. J. Pept. Res. 56, 438-445
40. Podbielski, A. (1993) Three different types of organization of the vir regulon in group A streptococci. Mol. Gen. Genet. 237, 287-300
41. Levin, J. C., and Wessels, M. R. (1998) Identification of csrR/csrS, a genetic locus that regulates hyaluronic acid capsule synthesis in group A Streptococcus. Mol. Microbiol. 30, 209-219
42. Heath, A., DiRita, V. J., Barg, N. L., and Engleberg, N. C. (1999) A twocomponent regulatory system, CsrR-CsrS, represses expression of three Streptococcus pyogenes virulence factors, hyaluronic acid capsule, streptolysin S, and pyrogenic exotoxin B. Infect. Immun. 67, 5298-5305
43. Treviño, J., Perez, N., Ramirez-Peña, E., Liu, Z., Shelburne, S. A., 3rd, Musser, J. M., and Sumby, P. (2009) CovS simultaneously activates and inhibits the CovR-mediated repression of distinct subsets of group A Streptococcus virulence factor-encoding genes. Infect. Immun. 77, 3141-3149
44. Hauser, A. R., Stevens, D. L., Kaplan, E. L., and Schlievert, P. M. (1991) Molecular analysis of pyrogenic exotoxins from Streptococcus pyogenes isolates associated with toxic shock-like syndrome. J. Clin. Microbiol. 29, 1562-1567
45. Federle, M. J., and Scott, J. R. (2002) Identification of binding sites for the group A streptococcal global regulator CovR. Mol. Microbiol. 43, 1161-1172
46. Churchward, G., Bates, C., Gusa, A. A., Stringer, V., and Scott, J. R. (2009) Regulation of streptokinase expression by CovR/S in Streptococcus pyogenes. CovR acts through a single high affinity binding site. Microbiology 155, 566-575
47. Rezcallah, M. S., Boyle, M. D., and Sledjeski, D. D. (2004) Mouse skin passage of Streptococcus pyogenes results in increased streptokinase expression and activity. Microbiology 150, 365-371
48. Cole, J. N., Pence, M. A., von Köckritz-Blickwede, M., Hollands, A., Gallo, R. L., Walker, M. J., and Nizet, V. (2010) M protein and hyaluronic acid capsule are essential for in vivo selection of covRS mutations characteristic of invasive serotype M1T1 group A Streptococcus. MBio. 1, e00191-10
49. Walker, M. J., Hollands, A., Sanderson-Smith, M. L., Cole, J. N., Kirk, J. K., Henningham, A., McArthur, J. D., Dinkla, K., Aziz, R. K., Kansal, R. G., Simpson, A. J., Buchanan, J. T., Chhatwal, G. S., Kotb, M., and Nizet, V. (2007) DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat. Med. 13, 981-985
50. Haanes, E. J., Heath, D. G., and Cleary, P. P. (1992) Architecture of the vir regulons of groupAstreptococci parallels opacity factor phenotype andM protein class. J. Bacteriol. 174, 4967-4976
51. Podbielski, A., Flosdorff, A., and Weber-Heynemann, J. (1995) The group A streptococcal virR49 gene controls expression of four structural vir regulon genes. Infect. Immun. 63, 9-20
52. McIver, K. S., Heath, A. S., Green, B. D., and Scott, J. R. (1995) Specific binding of the activator Mga to promoter sequences of the emm and scpA genes in the group A Streptococcus. J. Bacteriol. 177, 6619-6624
53. Ribardo, D. A., and McIver, K. S. (2006) Defining the Mga regulon. Comparative transcriptome analysis reveals both direct and indirect regulation by Mga in the group A Streptococcus. Mol. Microbiol. 62, 491-508
54. Gardiner, D., Hartas, J., Currie, B., Mathews, J. D., Kemp, D. J., and Sriprakash, K. S. (1995) Vir typing: a long-PCR typing method for group A streptococci. PCR Methods Appl. 4, 288-293
55. Sanderson-Smith, M. L., Walker, M. J., and Ranson, M. (2006) The maintenance of high affinity plasminogen binding by group A streptococcal plasminogen-binding M-like protein is mediated by arginine and histidine residues within the a1 and a2 repeat domains. J. Biol. Chem. 281, 25965-25971
56. Svensson, M. D., Sjöbring, U., and Bessen, D. E. (1999) Selective distribution of a high affinity plasminogen-binding site among group A streptococci associated with impetigo. Infect. Immun. 67, 3915-3920
57. Federle, M. J., McIver, K. S., and Scott, J. R. (1999) A response regulator that represses transcription of several virulence operons in the group A Streptococcus. J. Bacteriol. 181, 3649-3657
58. Engleberg, N. C., Heath, A., Miller, A., Rivera, C., and DiRita, V. J. (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
59. Graham, M. R., Smoot, L. M., Migliaccio, C. A., Virtaneva, K., Sturdevant, D. E., Porcella, S. F., Federle, M. J., Adams, G. J., Scott, J. R., and Musser, J. M. (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
60. Bernish, B., and van de Rijn, I. (1999) Characterization of a two-component system in Streptococcus pyogenes which is involved in regulation of hyaluronic acid production. J. Biol. Chem. 274, 4786-4793
61. Werb, Z. (1997)ECMand cell surface proteolysis. Regulating cellular ecology. Cell 91, 439-442
62. Cleary, P. P., Kaplan, E. L., Handley, J. P., Wlazlo, A., Kim, M. H., Hauser, A. R., and Schlievert, P. M. (1992) Clonal basis for resurgence of serious Streptococcus pyogenes disease in the 1980s. Lancet 339, 518-521
63. Schmidt, K. H., and Wadström, T. (1990) A secreted receptor related to M1 protein of Streptococcus pyogenes binds to fibrinogen, IgG, and albumin. Zentralbl. Bakteriol. 273, 216-228
64. Carapetis, J. R., Steer, A. C., Mulholland, E. K., and Weber, M. (2005) The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5, 685-694