A role for Trigger Factor and an Rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes

EMBO Journal

Volumn 17, Issue 21, 1998, Pages 6263-6275

  Lyon, William R ^a   Gibson, Carmela M ^a   Caparon, Michael G ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FK506; Peptidyl prolyl isomerase; RopA; RopB; SpeB

Indexed keywords

BACTERIAL ENZYME; CHAPERONE; CYSTEINE PROTEINASE; ISOMERASE; REGULATOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME RELEASE; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROCESSING; STREPTOCOCCUS PYOGENES; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CLONING, MOLECULAR; CYSTEINE ENDOPEPTIDASES; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PEPTIDYLPROLYL ISOMERASE; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOCOCCUS PYOGENES; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS PYOGENES;

EID: 0032476656     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.21.6263     Document Type: Article

References (78)

1. Altschul,S.F., Madden,T.F., Schaffer,A.A., Zhang,J., Zhang,Z., Miller,W. and Lipman,D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
2. Aono,R. (1992) Accumulation of alkaliphilic Bacillus penicillinase cleaved within the signal sequence in cytoplasm of Escherichia coli. Biosci, Biotech. Biochem., 56, 890-895.
3. Beck,E. and Bremer,E. (1980) Nucleotide sequence of the gene ompA coding the outer membrane protein II of Escherichia coli K-12. Nucleic Acids Res., 8, 3011-3027.
4. Berge,A. and Björck,L. (1995) Streptococcal cysteine proteinase releases biologically active fragments of Streptococcal surface proteins. J. Biol. Chem., 270, 9862-9867.
5. Bisno,A.L. and Stevens,D.L. (1996) Streptococcal infections of skin and soft tissues. N. Engl. J. Med., 334, 240-245.
6. Björck,L., Åkesson,P. Bohus,M., Torjner,J., Abrahamson,M., Olafsson,I. and Grubb,A. (1989) Bacterial growth blocked by a synthetic peptide based on the structure of a human proteinase inhibitor. Nature, 337, 385-386.
7. Boyer,H.W. and Roulland-Dussbix,D. (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol., 41, 459-472.
8. Bradford,M.M. (1976) A refined and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248.
9. Burns,E.H., Jr, Marciel,A.M. and Musser,J.M. (1996) Activation of a 66-kilodalton human endothelial cell matrix metalloproteinase by Streptococcus pyogenes extracellular cysteine protease. Infect. Immun., 64, 4744-4750.
10. Byrne,M.E., Rouch,D.A. and Skurray,R.A. (1989) Nucleotide sequence analysis of IS256 from the Staphylococcus aureus gentamicin-tobramycin-kanamycin-resistance transposon Tn4001. Gene, 81, 361-367.
11. Cao,J., Kapke,P.A. and Minion,F..C. (1994) Transformation of Mycoplasma gallisepticum with Tn916. Tn4001 and imegrative plasmid vectors. J. Bacteriol., 176, 4459-4462.
12. Caparon,M.G. and Scott,J.R. (1991) Genetic manipulation of the pathogenic streptococci. Methods Enzymol., 204, 556-586.
13. Chaussee,M.S., Gerlach,D., Yu,C. and Ferretti,J.J. (1993) Inactivation of the streptococcal erythrogenic toxin B gene (speB) in Streptococcus pyogenes. Infect. Immun., 61, 3719-3723.
14. Chaussee,M.S., Phillips,E.R. and Ferretti,J.J. (1997) Temporal production of streptococcal erythrogenic toxin B (streptococcal cysteine proteinase) in response to nutrient depletion. Infect. Immun., 65, 1956-1959.
15. Cheung,A.L., Eberhardt,K.J. and Fischetti,V.A. (1994) A method to isolate RNA from Gram-positive bacteria and mycobacteria. Anal. Biochem., 222, 511-514.
16. Chung,S.I., Lee,S.Y., Uchino,R. and Carmassi,F.. (1996) Factors that control extravascular fibrinolysis. Semin. Thromb. Hemost., 22, 479-488.
17. Corcoran,M.L., Kleiner,D.E. and Stetler-Stevenson,W.G. (1995) Regulation of matrix metalloproteinases during extracellular matrix turnover. Adv. Exp. Med. Biol., 385, 151-159.
18. Crooke,E. and Wickner,W. (1987) Trigger Factor: a soluble protein that folds Pro-OmpA into a membrane-assembly-competem form. Proc. Natl Acad. Sci. USA. 84, 5216-5220.
19. Crooke,E., Brundage,L., Rice,M. and Wickner,W. (1988) ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes. EMBO J., 7, 1831-1835.
20. Douglas,M. Mitchell,D., Ann,S. and Rancis,S.C. (1991) Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res., 19, 1154.
21. Gerlach,D., Knoll,H., Kohler,W., Ozegowski,J.H. and Hribalova,V. (1983) Isolation and characterization of erythrogenic toxins. V. Communication: identity of erythrogenic toxin type B and streptococcal proteinase precursor. Zentrabl. Bakteriol. Mikrobiol. Hyg. A, 255, 221-233.
22. Goguen,J.D., Hoe,N.P. and Subrahmanyam,Y.V.B.K. (1995) Proteinases and bacterial virulence: a view from the trenches. Infectious Agents Dis., 4, 47-54.
23. Göthel,S.F., Schmid,R., Wipat,A., Carter,N.M., Emmerson,P.T., Harwood,C.R. and Marahiel,M.A. (1997) An internal FK506-binding domain is the catalytic core of the prolyl isomerase activity associated with the Bacillus subtilis trigger factor. Eur. J. Biochem., 244, 59-65.
24. Gottesman,S., Clark,W.P., de Crecy-Lagard,V. and Maurizi,M.R. (1993) ClpX, an alternate subunit for the ATP-dependent Clp protease of Escherichia coli. Sequence and in vivo activities. J. Biol. Cliem., 268, 22617-22626.
25. Guthrie,B. and Wickner,W. (1990) Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J. Bacteriol., 172, 5555-5562.
26. Haandrikman,A.J., Meesters,R., Laan,H., Konings,W.N., Kok,J. and Venema,G. (1991) Processing of the lactococcal extracellular serine proteinase. Appl. Environ, Microbiol., 57, 1899-1904.
27. Hanski,E. and Caparon,M.G. (1992) Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus, Streptococcus pyogenes. Proc. Natl Acad. Sci. USA. 89, 6172-6176.
28. Hauser,A.R. and Schlievert,P.M. (1990) Nucleotide sequence of the streptococcal pyrogenic exotoxin type B gene and relationship between the toxin and the streptococcal proteinase precursor. J. Bacteriol., 172, 4536-4542.
29. Herwald,H., Collin,M., Müller-Esterl,W. and Björck,L. (1996) Streptococcal cysteine proteinase releases kinins: a novel virulence mechanism. J. Exp. Med., 184, 665-673.
30. Hesterkamp,T. and Bukau,B. (1996) Identification of the prolyl isomerase domain of Escherichia coli trigger factor. FEBS Lett., 385, 67-71.
31. Ji,Y., McLandsborough,L., Kondagunta,A. and Cleary,P.P. (1996) C5a peptidase alters clearance and trafficking of group A streptococci by infected mice. Infect. Immun., 64, 503-510.
32. Kandror,O., Sherman,M., Rhode,M. and Goldberg,A.L. (1995) Trigger factor is involved in GroEL-dependent protein degradation in E.coli and promotes binding of GroEL. to unfolded proteins. EMBO J., 14, 6021-6027.
33. Kandror,O.A., Sherman,M.Y., Moerschell,R. and Goldberg,AL. (1997) Trigger factor associates with GroEL in vivo and promotes its binding to certain polypeptides. J. Biol. Chem., 272, 1730-1734.
34. Kapur,V., Majesky,M.W., Li,L., Black,R.A. and Musser,J.M. (1993a) Cleavage of the interleukin 1β (IL-1β) precursor to produce active IL-1β by a conserved extracellular cysteine protease from Streptococcus pyogenes. Proc. Natl Acad. Sci. USA, 90, 7676-7680.
35. Kapur,V., Topouzis,S., Majesky,M.W., Li,L., Hamrick,M.R., Hamill,RJ., Patti,J.M. and Musser,J.M. (1993b) A conserved Streptococcus pyogenes extracellular cysteine proteinase cleaves human fibronectin and degrades vitronectin. Microb. Path., 15, 327-346.
36. Kapur,V., Maffei,J.T., Greer,R.S., Li,L.L., Adams,G.J. and Musser,J.M. (1994) Vaccination with streptococcal extracellular cysteine protease (interleukin-1 beta convertase) protects mice against challenge with heterologous group A streptococci. Microb. Path., 16, 443-450.
37. Kidd,V.J. (1998) Proteolytic activities that mediate apoptosis. Annu. Rev. Physiol., 60, 533-573.
38. Knudtson,K.L. and Minion,F..C. (1993) Construction of Tn4001lac derivatives to be used as promoter probe vectors in mycoplasmas. Gene., 137, 217-222.
39. Kushner,S.R. (1978) An improved method for transformation of Escherichia coli with ColE1-derived plasmids. In Boyer,H.W. and Micosia,S. (eds), Genetic Engineering. Elsevier/North Holland Biomedical Press, New York, NY, pp. 17-23.
40. Lampe,M., Binnie,C., Schmidt,R. and Losick,R. (1988) Cloned gene encoding the delta subunit of Bacillus subtilis RNA polymerase. Gene, 67, 13-19.
41. Lantz,M.S. (1997) Are bacterial proteases important virulence factors? J. Periodent. Res., 32, 126-132.
42. LeBlanc,D.L., Lee,L.N. and Inamine,J.M. (1991) Cloning and nucleotide base sequence analysis of a spectinomycin adenyltransferase AAD (9) determinant from Enterococcus faecalis. Antimicrob. Agents Chemother., 35, 1804-1810.
43. Lecker,S., Lill,R., Ziegelhoffer,T., Georgopoulos,C., Bassford,P.J., Kumamoto,C.A. and Wickner,W. (1989) Three pure chaparone proteins of Escherichia coli-SecB, trigger factor and GroEL-form soluble complexes with precursor proteins in vitro. EMBO J., 8, 2703-2709.
44. Lill,R., Crooke,E., Guthrie,B. and Wickner,W. (1988) The 'trigger factor cycle' includes ribosomes, presecretory proteins and the plasma membrane. Cell, 54, 1013-1018.
45. Lukomski,S., Sreevatsan,W., Amberg,C., Reichardt.W., Woischnik,M., Podbielski,A. and Musser,J.M. (1997) Inactivation of Streptococcus pyogenes extracellular cysteine protease significantly decreases mouse lethality of serotypes M3 and M49 strains. J. Clin. Invest., 99, 2574-2580.
46. Lukomski,S., Burns,E.H., Wyde,P.R., Podbielski,A., Rurangirwa,J., Moore-Poveda,D.K. and Musser,J.M. (1998) Genetic inactivation of an extracellular cysteine protease (SpeB) expressed by Streptococcus pyogenes decreases resistance to phagocytosis and dissemination to organs. Infect. Immun., 66, 771-776.
47. Lunsford,R.D. (1995) A Tn4001 delivery system for Streptococcus gordonii (Challis). Plasmid, 33, 153-157.
48. Lunsford,R.D. and Roble,A.G. (1997) comYA, a gene similar to comGA of Bacillus subtilis, is essential for competence-factor-dependent DNA transformation in Streptococcus gordonii. J. Bacteriol., 179, 3122-3126.
49. Mahairas,G.G., Lyon,B.R., Skurray,R.A. and Pattee,P.A. (1989) Genetic analysis of Staphylococcus aureus with Tn4001. J. Bacteriol., 171, 3968-3972.
50. Manoil,C. and Beckwith,J. (1985) TnphoA: a transposon probe for protein export signals. Proc. Natl Acad. Sci. USA, 82, 8129-8133.
51. Masure,S. and Opdenakker,G. (1989) Cytokine-mediated proteolysis in tissue remodeling. Experientia, 45, 542-549.
52. Musser,J.M., Stockbauer,K., Kapur,V. and Rudgers,G.W. (1996) Substitution of cysteine 192 in a highly conserved Streptococcus pyogenes extracellular cysteine protease (interleukin 1β convertase) alters proteolytic activity and ablates zymogen processing. Infect. Immun., 64. 1913-1917.
53. Okada,N., Geist,R.T. and Caparon,M.G. (1993) Positive transcriptional control of mry regulates virulence in the group A streptococcus. Mol. Microbiol., 7, 893-903.
54. Pancholi,V. and Fischetti,V.A. (1989) Identification of an endogenous membrane anchor-cleaving enzyme for group A streptococcal M protein. Its implication for the attachment of surface proteins in Gram-positive bacteria. J. Exp. Med., 170, 2119-2133.
55. Pancholi,V. and Fischetti,V.A. (1992) A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med., 176, 415-426.
56. Pancholi,V. and Fischetti,V.A. (1998) Alpha-enolase, a novel strong plasmin (ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem., 273, 14503-14515.
57. Pepper,M.S., Montesano,R., Mandroita,S.J., Orci,L. and Vassalli,J.D. (1996) Angiogenesis: a paradigm for balanced extracellular proteolysis during cell migration and morphogenesis. Enzyme Protein, 49, 138-162.
58. 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 the receptor proteins of two-component regulatory systems. J. Bacteriol., 173, 2617-2624.
59. Pissavin,C. and Hugovieux-Cotte-Pattat,N. (1997) Characterization of a periplasmic peptidyl-prolyl isomerase in Erwinia chrysanthemi. FEMS Microbiol. Lett., 157, 59-65.
60. Podbielski,A., Pohl,B., Woischnik,M., Korner,C., Schmidt,K., Rozdzinski,E. and Leonard,B.A.B. (1996) Molecular characterization of group A streptococcal (GAS) oligopeptide perrnease (Opp) and its effect on cysteine protease production. Mol. Microbiol, 21, 1087-1099.
61. Rahfeld,J.U., Rucknagel,K.P., Schelbert,B., Ludwig,B., Hacker,J., Mann,K. and Fischer,G. (1994) Confirmation of the existence of a third family among peptidyl-prolyl cis/trans isomerases. Amino acid sequence and recombinant production of parvulin. FEBS Lett., 352, 180-184.
62. Rosenthal,A.L. and Lacks,S.A. (1977) Nuclease detection in SDS-PAGE gel electrophoresis. Anal. Biochem., 80, 76-90.
63. Ruiz,N., Wang,B., Pentland,A. and Caparon,M. (1998) Streptolysin O and adherence synergistically modulate proinflammatory responses of keratinocytes to group A streptococci. Mol. Microbiol., 27, 337-346.
64. Sanders,J.W., Leenhouts,K., Burghoorn,J., Brands,J.R., Venema,G. and Kok,J. (1998) A chloride-inducible acid resistance mechanism in Lactococcus lactis and its regulation. Mol. Microbiol., 27, 299-310.
65. Scott,J.R. (1972) A turbid plaque-forming mutant of phage P1 that cannot lysogenize Escherichia coli. Virology, 62, 344-349.
66. Southern,E.M. (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol., 98, 503-517.
67. Stoller,G., Rucknagel,K.P., Nierhaus,K.H., Schmid,F..X., Fischer,G. and Rahfeld,J. (1995) A ribosome-associated peptidyl-prolyl cis/trans isomerase identified as the trigger factor. EMBO J., 14, 4939-4948.
68. Stoller,G., Tradler,T., Rucknagel,K.P., Rahfeld,J. and Fischer,G. (1996) An 11,8kDa proteolytic fragment of the E.coli trigger factor represents the domain carrying the peptidyl-prolyl cis/trans isomerase activity. FEBS Lett., 384, 117-122.
69. Sulavik,M.C., Tardif,G. and Clewell,D.B. (1992) Identification of a gene, rgg, which regulates expression of glucosyltransferase and influences the Spp phenotype of Streptococcus gordonii Challis. J. Bacteriol., 174, 3577-3586.
70. Tai,P.C., Lian,J., Yu,N., Fandl,J., Xu,H. and Vidugiriene,J. (1992) On protein translocation across cytoplasmic membranes. Ant. Leeuwenhoek, 61, 105-109.
71. Talkington,D.F., Schwartz,B., Black,C.M., Todd,J.K., Elliot,J., Breiman,R.F. and Facklum,R. (1993) Association of phenotypic and genotypic characteristics of invasive Streptococcus pyogenes isolates with clinical components of streptococcal toxic shock syndrome. Infect. Immun., 61, 3369-3374.
72. Tsai,P., Kuo,C., Lin,K., Lin,Y., Lei,H., Chen,F.., Wang,J. and Wu,J. (1998) Effect of group A streptococcal cysteine protease on invasion of epithelial cells. Infect. Immun., 66, 1460-1466.
73. Vickerman,M.M., Sulavik,M.C., Nowak,J.D., Gardner,N.M., Jones,G.W. and Clewell,D.B. (1997) Nucleotide sequence analysis of the Streptococcus gordonii glucosyltransferase gene, gtfG. DNA Seq., 7, 83-95.
74. Wandersman,C. (1989) Secretion, processing and activation of bacterial extracellular proteases. Mol. Microbiol., 3, 1825-1831.
75. Warth,R., Briand,P.A. and Picard,D. (1997) Functional analysis of the yeast 40 kDa cyclophilin Cyp40 and its role for viability and steroid receptor regulation. Biol. Chem., 378, 381-391.
76. Wong,W.W. (1998) ICE family proteases in inflammation and apoptosis. Agents Actions Suppl., 49, 5-13.
77. Yu,C.-E, and Ferretti,J.J. (1991) Frequency of the erythrogenic toxin B and C genes (speB and speC) among clinical isolates of group A streptococci. Infect. Immun., 59, 211-215.
78. Zarnt,T., Tradler,J., Stoller,G., Scholz,C., Schmid,F..X. and Fischer,G. (1997) Modular structure of the trigger factor required for high activity in protein folding. J. Mol. Biol., 271, 827-837.