SalK/SalR, a two-component signal transduction system, is essential for full virulence of highly invasive Streptococcus suis serotype 2

PLoS ONE

Volumn 3, Issue 5, 2008, Pages

  Li, Ming ^a,b   Wang, Changjun ^b   Feng, Youjun ^c,e   Pan, Xiuzhen ^b   Cheng, Gong ^b   Wang, Jing ^b   Ge, Junchao ^b   Zheng, Feng ^b   Cao, Min ^b   Dong, Yaqing ^b   Liu, Di ^c   Wang, Jufang ^d   Lin, Ying ^d   Du, Hongli ^d   Gao, George F ^c   Wang, Xiaoning ^d   Hu, Fuquan ^a   Tang, Jiaqi ^a,b  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b Research Institute for Medicine of Nanjing Command   (China)

^c INSTITUTE OF MICROBIOLOGY   (China)

^d SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^e UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN HISTIDINE KINASE; BACTERIAL PROTEIN; VIRULENCE FACTOR;

ARTICLE; ASSAY; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATION; BACTERIUM MUTANT; BIOINFORMATICS; CHINA; CONTROLLED STUDY; DOWN REGULATION; EPIDEMIC; EVOLUTION; EXPERIMENTAL INFECTION; GENE CONTROL; GENETIC TRANSCRIPTION; LETHALITY; MICROARRAY ANALYSIS; NEUTROPHIL; NONHUMAN; ORTHOLOGY; PATHOGENESIS; PATHOGENICITY ISLAND; PIGLET; PREDICTION; SEROTYPE; SIGNAL TRANSDUCTION; STREPTOCOCCUS SALIVARIUS; STREPTOCOCCUS SUIS; VALIDITY; ANIMAL; ANIMAL DISEASE; CLASSIFICATION; DISEASE TRANSMISSION; GENE DELETION; GENETICS; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PROMOTER REGION; SEROTYPING; STREPTOCOCCUS INFECTION; SWINE; SWINE DISEASE; VIRULENCE;

STREPTOCOCCUS SALIVARIUS; STREPTOCOCCUS SUIS;

ANIMALS; BACTERIAL PROTEINS; GENE DELETION; PROMOTER REGIONS (GENETICS); SEROTYPING; SIGNAL TRANSDUCTION; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS SUIS; SWINE; SWINE DISEASES; TRANSCRIPTION, GENETIC; VIRULENCE; VIRULENCE FACTORS;

EID: 47749113315     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0002080     Document Type: Article

References (65)

1. Staats JJ, Feder I, Okwumabua O, Chengappa MM (1997) Streptococcus suis: past and present. Vet Res Common 21: 381-407.
2. Lun ZR, Wang QP, Chen XG, Li AY, Zhu XQ (2007) Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7: 201-209.
3. Normile D (2005) Infectious diseases, WHO probes deadliness of China's pigborne disease. Science 309: 1308-1309.
4. Sriskandan S, Slater JD (2006) Invasive disease and toxic shock due to zoonotic Streptococcus suis: an emerging infection in the East? PLoS Med 3: e187.
5. Tang J, Wang C, Feng Y, Yang W, Song H, et al. (2006) Streptococcal toxic shock syndrome caused by Streptococcus suis serotype 2. PLoS Med 3: e151.
6. Chen C, Tang J, Dong W, Wang C, Feng Y, et al. (2007) A Glimpse of Streptococcal Toxic Shock Syndrome from Comparative Genomics of S. suis 2 Chinese Isolates. PLoS ONE 2: e315.
7. Lee CA (1996) Pathogenicity islands and the evolution of bacterial pathogens. Infect Agents Dis 5: 1-7.
8. Schmidt H, Hensel M (2004) Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17: 14-56.
9. Gal-Mor O, Finlay BB (2006) Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol 8: 1707-1719.
10. Brown JS, Gilliland SM, Holden DW (2001) A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol 40: 572-585.
11. Upton M, Tagg JR, Wescombe P, Jenkinson HF (2001) Intra- and interspecies signaling between Streptococcus salivarius and Streptococcus pyogenes mediated by SalA and SalA1 lantibiotic peptides. J Bacteriol 183: 3931-3938.
12. Shimizu T, Shima K, Yoshino K, Yonezawa K, Shimizu T, et al. (2002) Proteome and transcriptome analysis of the virulence genes regulated by the VirR/VirS system in Clostridium perfringens. J Bacteriol 184: 2587-2594.
13. McCluskey J, Hinds J, Husain S, Witney A, Mitchell TJ (2004) A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae. Mol Microbiol 51: 1661-1675.
14. Liang X, Zheng L, Landwehr C, Lunsford D, Holmes D, et al. (2005) Global regulation of gene expression by ArlRS, a two-component signal transduction regulatory system of Staphylococcus aureus. J Bacteriol 187: 5486-5492.
15. Ng WL, Tsui HC, Winkler ME (2005) Regulation of the pspA virulence factor and essential pcsB murein biosynthetic genes by the phosphorylated VicR (YycF) response regulator in Streptococcus pneumoniae. J Bacteriol 187: 7444-7459.
16. Sumby P, Whitney AR, Graviss EA, DeLeo FR, Musser JM (2006) Genomewide analysis of group a streptococci reveals a mutation that modulates global phenotype and disease specificity. PLoS Pathog 2: e5.
17. Lamy MC, Zouine M, Fert J, Vergassola M, Couve E, et al. (2004) CovS/ CovR of group B streptococcus: a two-component global regulatory system involved in virulence. Mol Microbiol 54: 1250-1268.
18. Beier D, Gross R (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9: 143-152.
19. 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 SA 99: 13855-13860.
20. Miller AA, Engleberg NC, DiRita VJ (2001) Repression of virulence genes by phosphorylation-dependent oligomerization of CsrR at target promoters in S. pyogenes. Mol Microbiol 40: 976-990.
21. Ba-Thein W, Lyristis M, Ohtani K, Nisbet IT, Hayashi H, et al. (1996) The virR/virS locus regulates the transcription of genes encoding extracellular toxin production in Clostridium perfringens. J Bacteriol 178: 2514-2520.
22. Banu S, Ohtani K, Yaguchi H, Swe T, Cole ST, et al. (2000) Identification of novel VirR/VirS-regulated genes in Clostridium perfringens. Mol Microbiol 35: 854-864.
23. Shimizu T, Ba-Thein W, Tamaki M, Hayashi H (1994) The virR gene, a member of a class of two-component response regulators, regulates the production of perfringolysin O, collagenase, and hemagglutinin in Clostridium perfringens. J Bacteriol 176: 1616-1623.
24. de Greeff A, Buys H, van Alphen L, Smith HE (2002) Response regulator important in pathogenesis of Streptococcus suis serotype 2. Microb Pathog 33: 185-192.
25. Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26: 71-112.
26. Whitehead NA, Barnard AM, Slater H, Simpson NJ, Salmond GP (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25: 365-404.
27. Yazaki K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Lett 580: 1183-1191.
28. Sipos G, Kuchler K (2006) Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr Drug Targets 7: 471-481.
29. Jones PM, George AM (2005) Multidrug resistance in parasites: ABC transporters, P-glycoproteins and molecular modelling. Int J Parasitol 35: 555-566.
30. Wolfger H, Mamnun YM, Kuchler K (2001) Fungal ABC proteins: pleiotropic drug resistance, stress response and cellular detoxification. Res Microbiol 152: 375-389.
31. Shin NR, Lee DY, Yoo HS (2007) Identification of quorum sensing-related regulons in Vibrio vulnificus by two-dimensional gel electrophoresis and differentially displayed reverse transcriptase PCR. FEMS Immunol Med Microbiol 50: 94-103.
32. Daigle F, Fairbrother JM, Harel J (1995) Identification of a mutation in the pst-phoU operon that reduces pathogenicity of an Eschcrichia coli strain causing septicemia in pigs. Infect Immun 63: 4924-4927.
33. Feng Y, Zheng F, Pan X, Sun W, Wang C, et al. (2007) Existence and characterization of allelic variants of Sao, a newly identified surface protein from Streptococcus suis. FEMS Microbiol Lett 275: 80-88.
34. Li Y, Martinez G, Gottschalk M, Lacouture S, Willson P, et al. (2006) Identification of a surface protein of Streptococcus suis and evaluation of its immunogenic and protective capacity in pigs. Infect Immun 74: 305-312.
35. Staats JJ, Plattner BL, Stewart GC, Changappa MM (1999) Presence of the Streptococcus suis suilysin gene and expression of MRP and EF correlates with high virulence in Streptococcus suis type 2 isolates. Vet Microbiol 70: 201-211.
36. Jonsson IM, Mazmanian SK, Schneewind O, Verdrengh M, Bremell T, et al. (2002) On the role of Staphylococcus aureus sortase and sortase-catalyzed surface protein anchoring in murine septic arthritis. J Infect Dis 185: 1417-1424.
37. Berthelot-Herault F, Morvan H, Keribin AM, Gottschalk M, Kobisch M (2000) Production of muraminidase-released protein (MRP), extracellular factor (EF) and suilysin by field isolates of Streptococcus suis capsular types 2, 1/2, 9, 7 and 3 isolated from swine in France. Vet Res 31: 473-479.
38. Herwald H, Cramer H, Morgelin M, Russell W, Sollenberg U, et al. (2004) M protein, a classical bacterial virulence determinant, forms complexes with fibrinogen that induce vascular leakage. Cell 116: 367-379.
39. Smith HE, Vecht U, Gielkens AL, Smits MA (1992) Cloning and nucleotide sequence of the gene encoding the 136-kilodalton surface protein (muramidase-released protein) of Streptococcus suis type 2. Infect Immun 60: 2361-2367.
40. Smith HE, de Vries R, van't Slot R, Smits MA (2000) The cps locus of Streptococcus suis serotype 2: genetic determinant for the synthesis of sialic acid. Microb Pathog 29: 127-134.
41. Charland N, Harel J, Kobisch M, Lacasse S, Gottschalk M (1998) Streptococcus suis serotype 2 mutants deficient in capsular expression. Microbiology 144 (Pt 2): 325-332.
42. Tarradas C, Borge C, Arenas A, Maldonado A, Astorga R, et al. (2001) Suilysin production by Streptococcus suis strains isolated from diseased and healthy carrier pigs in Spain. Vet Rec 148: 183-184.
43. Takamatsu D, Osaki M, Sekizaki T (2002) Evidence for lateral transfer of the Suilysin gene region of Streptococcus suis. J Bacteriol 184: 2050-2057.
44. Lun S, Perez-Gasal J, Connor W, Willson Pj (2003) Role of suilysin in pathogenesis of Streptococcus suis capsular serotype 2. Microb Pathog 34: 27-37.
45. Roberts AP, Mullany P (2006) Genetic basis of horizontal gene transfer among oral bacteria. Periodontol 2000 42: 36-46.
46. Kurland CG, Canback B, Berg OG (2003) Horizontal gene transfer: a critical view. Proc Natl Acad Sci U S A 100: 9658-9662.
47. Jain R, Rivera MC, Moore JE, Lake JA (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61: 489-495.
48. Kehoe MA, Kapur V, Whatmore AM, Musser JM (1996) Horizontal gene transfer among group A streptococci: implications for pathogenesis and epidemiology. Trends Microbiol 4: 436-443.
49. Sanders IR (2006) Rapid disease emergence through horizontal gene transfer between eukaryotes. Trends Ecol Evol 21: 656-658.
50. Mahan MJ, Slauch JM, Mekalanos JJ (1993) Selection of bacterial virulence genes that are specifically induced in host tissues. Science 259: 686-688.
51. Vecht U, Wisselink HJ, van Dijk JE, Smith HE (1992) Virulence of Streptococcus suis type 2 strains in newborn germfree pigs depends on phenotype. Infect Immun 60: 550-556.
52. Throup JP, Koretke KK, Bryant AP, Ingraham KA, Chalker AF, et al. (2000) A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol Microbiol 35: 566-576.
53. Smith HE, Vecht U, Wisselink HJ, Stockhofe-Zurwieden N, Biermann Y, et al. (1996) Mutants of Streptococcus suis types 1 and 2 impaired in expression of muramidase-released protein and extracellular protein induce disease in newborn germfree pigs. Infect Immun 64: 4409-4412.
54. Gottschalk M, Lebrun A, Wisselink H, Dubreuil JD, Smith H, et al. (1998) Production of virulence related-proteins by Canadian strains of Streptococcus suis capsular type 2. Can J Vet Res 62: 75-79.
55. Gottschalk M, Higgins R, Quessy S (1999) Dilemma of the virulence of Strptococcus suis strains. J Clin Microbiol 37: 4202-4203.
56. Berthelot-Herault F, Gottschalk M, Morvan H, Kobisch M (2005) Dilemma of virulence of Streptococcus suis: Canadian isolate 89-1591 characterized as a virulent strain using a standardized experimental model in pigs. Can J Vet Res 69: 236-240.
57. Smith HE, Wisselink HJ, Vecht U, Gielkens AL, Smits MA (1995) High-efficiency transformation and gene inactivation in Streptococcus suis type 2. Microbiology 141: 181-188.
58. de Greeff A, Buys H, Verhaar R, Dijkstra J, van Alphen L, et al. (2002) Contribution of fibronectin-binding protein to pathogenesis of Streptococcus suis serotype 2. Infect Immun 70: 1319-1325.
59. Baltimore RS, Kasper DL, Baker CJ, Goroff DK (1977) Antigenic specificity of opsonophagocytic antibodies in rabbit anti-sera to group B streptococci. J Immunol 118: 673-678.
60. Kobayashi SD, Braughton KR, Whitney AR, Voyich JM, Schwan TG, et al. (2003) Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proc Natl Acad Sci U S A 100: 10948-10953.
61. Voyich JM, Sturdevant DE, Braughton KR, Kobayashi SD, Lei B, et al. (2003) Genome-wide protective response used by group A Streptococcus to evade destruction by human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A 100: 1996-2001.
62. de Saizieu A, Gardes C, Flint N, Wagner C, Kamber M, et al. (2000) Microarray-based identification of a novel Streptococcus pneumoniae regulon controlled by an autoinduced peptide. J Bacteriol 182: 4696-4703.
63. Schmittgen TD, Zakrajsek BA (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46: 69-81.
64. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta CM) Method. Methods 25: 402-408.
65. Takamatsu D, Osaki M, Sekizaki T (2001) Construction and characterization of Streptococcus suis-Escherichia coli shuttle cloning vectors. Plasmid 45: 101-113.