Streptococcus pyogenes c-di-AMP Phosphodiesterase, GdpP, Influences SpeB Processing and Virulence

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Cho, Kyu Hong ^a   Kang, Song Ok ^b  

^a SOUTHERN ILLINOIS UNIVERSITY   (United States)

^b SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; CYCLIC AMP PHOSPHODIESTERASE; CYSTEINE PROTEINASE; GUANOSINE DIPHOSPHATE; MEMBRANE PROTEIN; PSEUDOMONAS EXOTOXIN; STREPTOCOCCUS PYOGENES EXOTOXIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOGENESIS; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME SYNTHESIS; EXPRESSION VECTOR; GENE DELETION; GENE LOCATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PLASMID; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOFT TISSUE INFECTION; STREPTOCOCCUS PYOGENES;

AMPICILLIN; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DINUCLEOSIDE PHOSPHATES; DRUG RESISTANCE, BACTERIAL; EXOTOXINS; GENE DELETION; MICE; MICE, HAIRLESS; MICROBIAL SENSITIVITY TESTS; PHOSPHORIC DIESTER HYDROLASES; STREPTOCOCCUS PYOGENES; VIRULENCE;

EID: 84880283738     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069425     Document Type: Article

References (46)

1. Hengge R, (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273. doi:10.1038/nrmicro2109. PubMed: 19287449.
2. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103: 2839-2844. doi:10.1073/pnas.0511090103. PubMed: 16477007.
3. Holland LM, O'Donnell ST, Ryjenkov DA, Gomelsky L, Slater SR, et al. (2008) A staphylococcal GGDEF domain protein regulates biofilm formation independently of cyclic dimeric GMP. J Bacteriol 190: 5178-5189. doi:10.1128/JB.00375-08. PubMed: 18502872.
4. Rao F, See RY, Zhang D, Toh DC, Ji Q, et al. (2010) YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J Biol Chem 285: 473-482. doi:10.1074/jbc.M109.040238. PubMed: 19901023.
5. Corrigan RM, Abbott JC, Burhenne H, Kaever V, Gründling A, (2011) c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLOS Pathog 7: e1002217. PubMed: 21909268.
6. Kamegaya T, Kuroda K, Hayakawa Y, (2011) Identification of a Streptococcus pyogenes SF370 gene involved in production of c-di-AMP. Nagoya J Med Sci 73: 49-57. PubMed: 21614937.
7. Woodward JJ, Iavarone AT, Portnoy DA, (2010) c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328: 1703-1705. doi:10.1126/science.1189801. PubMed: 20508090.
8. Bai Y, Yang J, Zhou X, Ding X, Eisele LE, et al. (2012) Mycobacterium tuberculosis Rv3586 (DacA) is a diadenylate cyclase that converts ATP or ADP into c-di-AMP. PLOS ONE 7: e35206. doi:10.1371/journal.pone.0035206. PubMed: 22529992.
9. Glass JI, Assad-Garcia N, Alperovich N, Yooseph S, Lewis MR, et al. (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci U S A 103: 425-430. doi:10.1073/pnas.0510013103. PubMed: 16407165.
10. French CT, Lao P, Loraine AE, Matthews BT, Yu H, et al. (2008) Large-scale transposon mutagenesis of Mycoplasma pulmonis. Mol Microbiol 69: 67-76. doi:10.1111/j.1365-2958.2008.06262.x. PubMed: 18452587.
11. Song JH, Ko KS, Lee JY, Baek JY, Oh WS, et al. (2005) Identification of essential genes in Streptococcus pneumoniae by allelic replacement mutagenesis. Mol Cells 19: 365-374. PubMed: 15995353.
12. Oppenheimer-Shaanan Y, Wexselblatt E, Katzhendler J, Yavin E, Ben-Yehuda S, (2011) c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep 12: 594-601. doi:10.1038/embor.2011.77. PubMed: 21566650.
13. Luo Y, Helmann JD, (2012) Analysis of the role of Bacillus subtilis sigma(M) in beta-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol Microbiol 83: 623-639. doi:10.1111/j.1365-2958.2011.07953.x. PubMed: 22211522.
14. Hauser AR, Schlievert PM, (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. PubMed: 2198264.
15. Podbielski A, Woischnik M, Kreikemeyer B, Bettenbrock K, Buttaro BA, (1999) Cysteine protease SpeB expression in group A streptococci is influenced by the nutritional environment but SpeB does not contribute to obtaining essential nutrients. Med Microbiol Immunol (Berl) 188: 99-109. doi:10.1007/s004300050111.
16. Kapur V, Topouzis S, Majesky MW, Li LL, Hamrick MR, et al. (1993) A conserved Streptococcus pyogenes extracellular cysteine protease cleaves human fibronectin and degrades vitronectin. Microb Pathog 15: 327-346. doi:10.1006/mpat.1993.1083. PubMed: 7516997.
17. Burns EH Jr., Marciel AM, Musser JM, (1996) Activation of a 66-kilodalton human endothelial cell matrix metalloprotease by Streptococcus pyogenes extracellular cysteine protease. Infect Immun 64: 4744-4750. PubMed: 8890235.
18. Kapur V, Majesky MW, Li LL, Black RA, Musser JM, (1993) Cleavage of interleukin 1 beta (IL-1 beta) precursor to produce active IL-1 beta by a conserved extracellular cysteine protease from Streptococcus pyogenes. Proc Natl Acad Sci U S A 90: 7676-7680. doi:10.1073/pnas.90.16.7676. PubMed: 7689226.
19. Herwald H, Collin M, Müller-Esterl W, Björck L, (1996) Streptococcal cysteine proteinase releases kinins: a virulence mechanism. J Exp Med 184: 665-673. doi:10.1084/jem.184.2.665. PubMed: 8760820.
20. Rasmussen M, Björck L, (2002) Proteolysis and its regulation at the surface of Streptococcus pyogenes. Mol Microbiol 43: 537-544. doi:10.1046/j.1365-2958.2002.02766.x. PubMed: 11929513.
21. Olsen RJ, Musser JM, (2009) Molecular pathogenesis of necrotizing fasciitis. Annu Rev Pathol 5: 1-31. PubMed: 19737105.
22. Lyon WR, Caparon MG, (2003) Trigger factor-mediated prolyl isomerization influences maturation of the Streptococcus pyogenes cysteine protease. J Bacteriol 185: 3661-3667. doi:10.1128/JB.185.12.3661-3667.2003. PubMed: 12775704.
23. 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. PubMed: 9799235.
24. Ma Y, Bryant AE, Salmi DB, Hayes-Schroer SM, McIndoo E, et al. (2006) Identification and characterization of bicistronic speB and prsA gene expression in the group A Streptococcus. J Bacteriol 188: 7626-7634. doi:10.1128/JB.01059-06. PubMed: 16950917.
25. Cole JN, Aquilina JA, Hains PG, Henningham A, Sriprakash KS, et al. (2007) Role of group A Streptococcus HtrA in the maturation of SpeB protease. Proteomics 7: 4488-4498. doi:10.1002/pmic.200700626. PubMed: 18072207.
26. Lyon WR, Caparon MG, (2004) Role for serine protease HtrA (DegP) of Streptococcus pyogenes in the biogenesis of virulence factors SpeB and the hemolysin streptolysin S. Infect Immun 72: 1618-1625. doi:10.1128/IAI.72.3.1618-1625.2004. PubMed: 14977969.
27. Hanski E, Caparon M, (1992) Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcus Streptococcus pyogenes. Proc Natl Acad Sci U S A 89: 6172-6176. doi:10.1073/pnas.89.13.6172. PubMed: 1385871.
28. Scott JR, (1974) A turbid plaque-forming mutant of phage P1 that cannot lysogenize Escherichia coli. Virology 62: 344-349. doi:10.1016/0042-6822(74)90397-3. PubMed: 4610991.
29. Caparon MG, Scott JR, (1991) Genetic manipulation of pathogenic streptococci. Methods Enzymol 204: 556-586. doi:10.1016/0076-6879(91)04028-M. PubMed: 1658571.
30. Brenot A, King KY, Caparon MG, (2005) The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol Microbiol 55: 221-234. PubMed: 15612930.
31. King KY, Horenstein JA, Caparon MG, (2000) Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J Bacteriol 182: 5290-5299. doi:10.1128/JB.182.19.5290-5299.2000. PubMed: 10986229.
32. Ghosh J, Caparon MG, (2006) Specificity of Streptococcus pyogenes NAD(+) glycohydrolase in cytolysin-mediated translocation. Mol Microbiol 62: 1203-1214. doi:10.1111/j.1365-2958.2006.05430.x. PubMed: 17042787.
33. Granok AB, Parsonage D, Ross RP, Caparon MG, (2000) The RofA binding site in Streptococcus pyogenes is utilized in multiple transcriptional pathways. J Bacteriol 182: 1529-1540. doi:10.1128/JB.182.6.1529-1540.2000. PubMed: 10692357.
34. Brenot A, King KY, Janowiak B, Griffith O, Caparon MG, (2004) Contribution of glutathione peroxidase to the virulence of Streptococcus pyogenes. Infect Immun 72: 408-413. doi:10.1128/IAI.72.1.408-413.2004. PubMed: 14688122.
35. Glantz S, (2002) Primer of Biostatistics. New York: McGraw-Hill Co.
36. Cho KH, Caparon MG, (2008) tRNA modification by GidA/MnmE is necessary for Streptococcus pyogenes virulence: a new strategy to make live attenuated strains. Infect Immun 76: 3176-3186. doi:10.1128/IAI.01721-07. PubMed: 18426891.
37. Hoffman DW, Cameron CS, Davies C, White SW, Ramakrishnan V, (1996) Ribosomal protein L9: a structure determination by the combined use of X-ray crystallography and NMR spectroscopy. J Mol Biol 264: 1058-1071. doi:10.1006/jmbi.1996.0696. PubMed: 9000630.
38. Yonath A, (2002) High-resolution structures of large ribosomal subunits from mesophilic eubacteria and halophilic archaea at various functional States. Curr Protein Pept Sci 3: 67-78. doi:10.2174/1389203023380828. PubMed: 12370012.
39. Herr AJ, Nelson CC, Wills NM, Gesteland RF, Atkins JF, (2001) Analysis of the roles of tRNA structure, ribosomal protein L9, and the bacteriophage T4 gene 60 bypassing signals during ribosome slippage on mRNA. J Mol Biol 309: 1029-1048. doi:10.1006/jmbi.2001.4717. PubMed: 11399077.
40. Song MS, Pham PT, Olson M, Carter JR, Franden MA, et al. (2001) The delta and delta ' subunits of the DNA polymerase III holoenzyme are essential for initiation complex formation and processive elongation. J Biol Chem 276: 35165-35175. doi:10.1074/jbc.M100389200. PubMed: 11432857.
41. Bustin M, Lin MC, Stein WH, Moore S, (1970) Activity of the reduced zymogen of streptococcal proteinase. J Biol Chem 245: 846-849. PubMed: 5416667.
42. Doran JD, Nomizu M, Takebe S, Ménard R, Griffith D, et al. (1999) Autocatalytic processing of the streptococcal cysteine protease zymogen: processing mechanism and characterization of the autoproteolytic cleavage sites. Eur J Biochem 263: 145-151. doi:10.1046/j.1432-1327.1999.00473.x. PubMed: 10429198.
43. Rosch J, Caparon M, (2004) A microdomain for protein secretion in Gram-positive bacteria. Science 304: 1513-1515. doi:10.1126/science.1097404. PubMed: 15178803.
44. Rosch JW, Hsu FF, Caparon MG, (2007) Anionic lipids enriched at the ExPortal of Streptococcus pyogenes. J Bacteriol 189: 801-806. doi:10.1128/JB.01549-06. PubMed: 17142392.
45. Kiefhaber T, Quaas R, Hahn U, Schmid FX, (1990) Folding of ribonuclease T1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29: 3061-3070. doi:10.1021/bi00464a024. PubMed: 2110824.
46. Meehl MA, Pinkner JS, Anderson PJ, Hultgren SJ, Caparon MG, (2005) A novel endogenous inhibitor of the secreted streptococcal NAD-glycohydrolase. PLOS Pathog 1: e35. doi:10.1371/journal.ppat.0010035. PubMed: 16333395.