The Expression of the fim Operon Is Crucial for the Survival of Streptococcus parasanguinis FW213 within Macrophages but Not Acid Tolerance

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Chen, Yi Ywan M ^a   Shieh, Hui Ru ^a   Chang, Ya Ching ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ACYLTRANSFERASE; ADHESIN; CHLORAMPHENICOL; CIS ACTING ELEMENT; DNA; FIMA PROTEIN; GENOMIC DNA; LIPOPROTEIN; METAL ION; PALINDROMIC DNA; UNCLASSIFIED DRUG; ACID; FIMBRIA PROTEIN;

ACID TOLERANCE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA FLANKING REGION; DNA SEQUENCE; ELECTROPHORESIS; ENDOCARDITIS; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; GENE FUNCTION; HEART; IN VITRO STUDY; IN VIVO STUDY; LIPID MONOLAYER; MACROPHAGE; NONHUMAN; OPERON; OXIDATIVE STRESS; PHAGOCYTE; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; STREPTOCOCCUS GORDONII; STREPTOCOCCUS PARASANGUINIS; WILD TYPE; ADAPTATION; GENETICS; MICROBIOLOGY; PHYSIOLOGY; STREPTOCOCCUS;

STREPTOCOCCUS GORDONII; STREPTOCOCCUS PARASANGUINIS;

ACIDS; ADAPTATION, PHYSIOLOGICAL; FIMBRIAE PROTEINS; MACROPHAGES; OPERON; OXIDATIVE STRESS; STREPTOCOCCUS;

EID: 84879146892     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066163     Document Type: Article

References (55)

1. Carlsson J, Grahnen H, Jonsson G, Wikner S, (1970) Establishment of Streptococcus sanguis in the mouths of infants. Arch Oral Biol 15: 1143-1148.
2. Jenkinson HF, Lamont RJ, (1997) Streptococcal adhesion and colonization. Crit Rev Oral Biol Med 8: 175-200.
3. Baddour LM, (1994) Virulence factors among gram-positive bacteria in experimental endocarditis. Infect Immun 62: 2143-2148.
4. van der Meer JT, van Vianen W, Hu E, van Leeuwen WB, Valkenburg HA, et al. (1991) Distribution, antibiotic susceptibility and tolerance of bacterial isolates in culture-positive cases of endocarditis in The Netherlands. Eur J Clin Microbiol Infect Dis 10: 728-734.
5. Oetjen J, Fives-Taylor P, Froeliger EH, (2002) The divergently transcribed Streptococcus parasanguis virulence-associated fimA operon encoding an Mn(2+)-responsive metal transporter and pepO encoding a zinc metallopeptidase are not coordinately regulated. Infect Immun 70: 5706-5714.
6. Burnette-Curley D, Wells V, Viscount H, Munro CL, Fenno JC, et al. (1995) FimA, a major virulence factor associated with Streptococcus parasanguis endocarditis. Infect Immun 63: 4669-4674.
7. Viscount HB, Munro CL, Burnette-Curley D, Peterson DL, Macrina FL, (1997) Immunization with FimA protects against Streptococcus parasanguis endocarditis in rats. Infect Immun 65: 994-1002.
8. Fenno JC, Shaikh A, Spatafora G, Fives-Taylor P, (1995) The fimA locus of Streptococcus parasanguis encodes an ATP-binding membrane transport system. Mol Microbiol 15: 849-863.
9. Spatafora G, Van Hoeven N, Wagner K, Fives-Taylor P, (2002) Evidence that ORF3 at the Streptococcus parasanguis fimA locus encodes a thiol-specific antioxidant. Microbiology 148: 755-762.
10. Das S, Kanamoto T, Ge X, Xu P, Unoki T, et al. (2009) Contribution of lipoproteins and lipoprotein processing to endocarditis virulence in Streptococcus sanguinis. J Bacteriol 191: 4166-4179.
11. Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF, (1998) The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J Bacteriol 180: 290-295.
12. McAllister LJ, Tseng HJ, Ogunniyi AD, Jennings MP, McEwan AG, et al. (2004) Molecular analysis of the psa permease complex of Streptococcus pneumoniae. Mol Microbiol 53: 889-901.
13. Paik S, Brown A, Munro CL, Cornelissen CN, Kitten T, (2003) The sloABCR operon of Streptococcus mutans encodes an Mn and Fe transport system required for endocarditis virulence and its Mn-dependent repressor. J Bacteriol 185: 5967-5975.
14. Jakubovics NS, Smith AW, Jenkinson HF, (2000) Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38: 140-153.
15. Kitten T, Munro CL, Michalek SM, Macrina FL, (2000) Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect Immun 68: 4441-4451.
16. Anderton JM, Rajam G, Romero-Steiner S, Summer S, Kowalczyk AP, et al. (2007) E-cadherin is a receptor for the common protein pneumococcal surface adhesin A (PsaA) of Streptococcus pneumoniae. Microb Pathog 42: 225-236.
17. Berry AM, Paton JC, (1996) Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae. Infect Immun 64: 5255-5262.
18. Ganeshkumar N, Hannam PM, Kolenbrander PE, McBride BC, (1991) Nucleotide sequence of a gene coding for a saliva-binding protein (SsaB) from Streptococcus sanguis 12 and possible role of the protein in coaggregation with actinomyces. Infect Immun 59: 1093-1099.
19. Kolenbrander PE, Andersen RN, Ganeshkumar N, (1994) Nucleotide sequence of the Streptococcus gordonii PK488 coaggregation adhesin gene, scaA, and ATP-binding cassette. Infect Immun 62: 4469-4480.
20. Marra A, Lawson S, Asundi JS, Brigham D, Hromockyj AE, (2002) In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection. Microbiology 148: 1483-1491.
21. Sampson JS, O'Connor SP, Stinson AR, Tharpe JA, Russell H, (1994) Cloning and nucleotide sequence analysis of psaA, the Streptococcus pneumoniae gene encoding a 37-kilodalton protein homologous to previously reported Streptococcus sp. adhesins. Infect Immun 62: 319-324.
22. Kloosterman TG, Witwicki RM, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP, (2008) Opposite effects of Mn2+ and Zn2+ on PsaR-mediated expression of the virulence genes pcpA, prtA, and psaBCA of Streptococcus pneumoniae. J Bacteriol 190: 5382-5393.
23. Rolerson E, Swick A, Newlon L, Palmer C, Pan Y, et al. (2006) The SloR/Dlg metalloregulator modulates Streptococcus mutans virulence gene expression. J Bacteriol 188: 5033-5044.
24. Tao X, Murphy JR, (1992) Binding of the metalloregulatory protein DtxR to the diphtheria tox operator requires a divalent heavy metal ion and protects the palindromic sequence from DNase I digestion. J Biol Chem 267: 21761-21764.
25. O'Rourke KP, Shaw JD, Pesesky MW, Cook BT, Roberts SM, et al. (2010) Genome-wide characterization of the SloR metalloregulome in Streptococcus mutans. J Bacteriol 192: 1433-1443.
26. Jacobsen FE, Kazmierczak KM, Lisher JP, Winkler ME, Giedroc DP, (2011) Interplay between manganese and zinc homeostasis in the human pathogen Streptococcus pneumoniae. Metallomics 3: 38-41.
27. Stoll KE, Draper WE, Kliegman JI, Golynskiy MV, Brew-Appiah RA, et al. (2009) Characterization and structure of the manganese-responsive transcriptional regulator ScaR. Biochemistry 48: 10308-10320.
28. Geng J, Chiu CH, Tang P, Chen Y, Shieh HR, et al. (2012) Complete genome and transcriptomes of Streptococcus parasanguinis FW213: phylogenic relations and potential virulence mechanisms. PLoS One 7: e34769.
29. Pennella MA, Giedroc DP, (2005) Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators. Biometals 18: 413-428.
30. LeBlanc DJ, Lee LN, Inamine JM, (1991) Cloning and nucleotide base sequence analysis of a spectinomycin adenyltransferase AAD(9) determinant from Enterococcus faecalis. Antimicrob Agents Chemother 35: 1804-1810.
31. Fenno JC, Shaikh A, Fives-Taylor P, (1993) Characterization of allelic replacement in Streptococcus parasanguis: transformation and homologous recombination in a 'nontransformable' streptococcus. Gene 130: 81-90.
32. Kim JS, Sung MH, Kho DH, Lee JK, (2005) Induction of manganese-containing superoxide dismutase is required for acid tolerance in Vibrio vulnificus. J Bacteriol 187: 5984-5995.
33. Martin-Galiano AJ, Overweg K, Ferrandiz MJ, Reuter M, Wells JM, et al. (2005) Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae. Microbiology 151: 3935-3946.
34. Wen ZT, Burne RA, (2004) LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. J Bacteriol 186: 2682-2691.
35. Bruno-Barcena JM, Azcarate-Peril MA, Hassan HM, (2010) Role of antioxidant enzymes in bacterial resistance to organic acids. Appl Environ Microbiol 76: 2747-2753.
36. Hanks TS, Liu M, McClure MJ, Fukumura M, Duffy A, et al. (2006) Differential regulation of iron- and manganese-specific MtsABC and heme-specific HtsABC transporters by the metalloregulator MtsR of group A Streptococcus. Infect Immun 74: 5132-5139.
37. Janulczyk R, Pallon J, Bjorck L, (1999) Identification and characterization of a Streptococcus pyogenes ABC transporter with multiple specificity for metal cations. Mol Microbiol 34: 596-606.
38. Ricci S, Janulczyk R, Bjorck L, (2002) The regulator PerR is involved in oxidative stress response and iron homeostasis and is necessary for full virulence of Streptococcus pyogenes. Infect Immun 70: 4968-4976.
39. Brenot A, King KY, Caparon MG, (2005) The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol Microbiol 55: 221-234.
40. Kinkel TL, McIver KS, (2008) CcpA-mediated repression of streptolysin S expression and virulence in the group A streptococcus. Infect Immun 76: 3451-3463.
41. Gaudu P, Lamberet G, Poncet S, Gruss A, (2003) CcpA regulation of aerobic and respiration growth in Lactococcus lactis. Mol Microbiol 50: 183-192.
42. Reyes-Caballero H, Guerra AJ, Jacobsen FE, Kazmierczak KM, Cowart D, et al. (2010) The metalloregulatory zinc site in Streptococcus pneumoniae AdcR, a zinc-activated MarR family repressor. J Mol Biol 403: 197-216.
43. Forbes JR, Gros P, (2001) Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 9: 397-403.
44. Papp-Wallace KM, Maguire ME, (2006) Manganese transport and the role of manganese in virulence. Annu Rev Microbiol 60: 187-209.
45. Cole RM, Calandra GB, Huff E, Nugent KM, (1976) Attributes of potential utility in differentiating among "group H" streptococci or Streptococcus sanguis. J Dent Res 55: A142-153.
46. Terleckyj B, Willett NP, Shockman GD, (1975) Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun 11: 649-655.
47. Chen YY, Clancy KA, Burne RA, (1996) Streptococcus salivarius urease: genetic and biochemical characterization and expression in a dental plaque streptococcus. Infect Immun 64: 585-592.
48. Chen YY, Weaver CA, Mendelsohn DR, Burne RA, (1998) Transcriptional regulation of the Streptococcus salivarius 57.I urease operon. J Bacteriol 180: 5769-5775.
49. Anderson DG, McKay LL, (1983) Simple and rapid method for isolating large plasmid DNA from lactic streptococci. Appl Environ Microbiol 46: 549-552.
50. Horinouchi S, Weisblum B, (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150: 815-825.
51. Bartolome B, Jubete Y, Martinez E, de la Cruz F, (1991) Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene 102: 75-78.
52. Dunny GM, Lee LN, LeBlanc DJ, (1991) Improved electroporation and cloning vector system for gram-positive bacteria. Appl Environ Microbiol 57: 1194-1201.
53. Chen YY, Betzenhauser MJ, Burne RA, (2002) cis-Acting elements that regulate the low-pH-inducible urease operon of Streptococcus salivarius. Microbiology 148: 3599-3608.
54. Shaw WV, (1975) Chloramphenicol acetyltransferase from chloramphenicol-resistant bacteria. Methods Enzymol 43: 737-755.
55. Grainger DC, Overton TW, Reppas N, Wade JT, Tamai E, et al. (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186: 6938-6943.