Carbohydrate availability regulates virulence gene expression in Streptococcus suis

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Ferrando, M Laura ^a,b   Van Baarlen, Peter ^a   Orrù, Germano ^c   Piga, Rosaria ^a   Bongers, Roger S ^d   Wels, Michiel ^d   De Greeff, Astrid ^a   Smith, Hilde E ^a   Wells, Jerry M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF CAGLIARI   (Italy)

^d NIZO FOOD RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; GLUCOSE; PULLULAN; STARCH; BACTERIAL PROTEIN; GLUCAN; HEMOLYSIN; LACTOSE; MALTOTRIOSE; SUILYSIN; TRISACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APUA GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL INFECTION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CATABOLITE REPRESSION; CELL ADHESION; CELL INVASION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE REPRESSION; GLYCOGEN SYNTHESIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; SLY GENE; STREPTOCOCCUS SUIS; SWINE; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OROPHARYNX; PATHOGENICITY; SECRETION (PROCESS); STREPTOCOCCUS INFECTION; SWINE DISEASE; VETERINARY; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GLUCANS; GLUCOSE; HEMOLYSIN PROTEINS; HUMANS; LACTOSE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; OROPHARYNX; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS SUIS; SWINE; SWINE DISEASES; TRISACCHARIDES; VIRULENCE;

EID: 84898664681     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0089334     Document Type: Article

References (92)

1. Lun ZR, Wang QP, Chen XG, Li AX, Zhu XQ (2007) Streptococcus suis: an emerging zoonotic pathogen. Lancet Infect Dis 7:201-209.
2. Wertheim HF, Nghia HD, Taylor W, Schultsz C (2009) Streptococcus suis: an emerging human pathogen. Clin Infect Dis 48:617-625.
3. Gottschalk M, Segura M (2000) The pathogenesis of the meningitis caused by Streptococcus suis: the unresolved questions. Vet Microbiol 76:259-272.
4. Fittipaldi N, Segura M, Grenier D, Gottschalk M (2012) Virulence factors involved in the pathogenesis of the infection caused by the swine pathogen and zoonotic agent Streptococcus suis. Future Microbiol 7:259-279.
5. Meurman JH, Rytomaa I, Kari K, Laakso T, Murtomaa H (1987) Salivary pH and glucose after consuming various beverages, including sugar-containing drinks. Caries Res 21:353-359.
6. Gough H, Luke GA, Beeley JA, Geddes DA (1996) Human salivary glucose analysis by high-performance ion-exchange chromatography and pulsed amperometric detection. Arch Oral Biol 41:141-145.
7. Bakker GC, Dekker (Pubitemid 128523585)
8. Mormann JE, Muhlemann HR (1981) Oral starch degradation and its influence on acid production in human dental plaque. Caries Res 15:166-175. (Pubitemid 11169978)
9. Mormann JE, Amadò R, Neukom H (1982) Comparative Studies on the in vitro alpha-Amylolysis of Different Wheat Starch Products. Starch - Stärke 34:121-124.
10. Taravel FR, Datema R, Woloszczuk W, Marshall JJ, Whelan WJ (1983) Purification and characterization of a pig intestinal alpha-limit dextrinase. Eur J Biochem 130:147-153.
11. Shelburne SA, 3rd, Granville C, Tokuyama M, Sitkiewicz I, Patel P, et al. (2005) Growth characteristics of and virulence factor production by group A Streptococcus during cultivation in human saliva. Infect Immun 73:4723-4731. (Pubitemid 41105628)
12. Norton PM, Rolph C, Ward PN, Bentley RW, Leigh JA (1999) Epithelial invasion and cell lysis by virulent strains of Streptococcus suis is enhanced by the presence of suilysin. FEMS Immunol Med Microbiol 26:25-35. (Pubitemid 29475008)
13. Lalonde M, Segura M, Lacouture S, Gottschalk M (2000) Interactions between Streptococcus suis serotype 2 and different epithelial cell lines. Microbiology 146(Pt 8):1913-1921. (Pubitemid 30639266)
14. Walker GJ, Builder JE (1971) Metabolism of the reserve polysaccharide of Streptococcus mitis. Properties of branching enzyme, and its effect on the activity of glycogen synthetase. Eur J Biochem 20:14-21.
15. Eisenberg RJ, Elchisak M, Lai C (1974) Glycogen accumulation by pleomorphic cells of Streptococcus sanguis. Biochem Biophys Res Commun 57:959-966.
16. Bongaerts RJ, Heinz HP, Hadding U, Zysk G (2000) Antigenicity, expression, and molecular characterization of surface-located pullulanase of Streptococcus pneumoniae. Infect Immun 68:7141-7143. (Pubitemid 32463431)
17. Shelburne SA, 3rd, Keith DB, Davenport MT, Horstmann N, Brennan RG, et al. (2008) Molecular characterization of group A Streptococcus maltodextrin catabolism and its role in pharyngitis. Mol Microbiol 69:436-452. (Pubitemid 351988014)
18. Abbott DW, Higgins MA, Hyrnuik S, Pluvinage B, Lammerts Van Bueren A, et al. (2010) The molecular basis of glycogen breakdown and transport in Streptococcus pneumoniae. Mol Microbiol 77:183-199.
19. Ferrando ML, Fuentes S, De Greeff A, Smith H, Wells JM (2010) ApuA, a multifunctional alpha-glucan-degrading enzyme of Streptococcus suis, mediates adhesion to porcine epithelium and mucus. Microbiology 156:2818-2828.
20. Moreno MS, Schneider BL, Maile RR, Weyler W, Saier MH, Jr. (2001) Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 39:1366-1381. (Pubitemid 32225145)
21. Deutscher J, Francke C, Postma PW (2006) How phosphotransferase systemrelated protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70:939-1031. (Pubitemid 44958262)
22. Vecht U, Arends JP, Van Der Molen EJ, Van Leengoed LA (1989) Differences in virulence between two strains of Streptococcus suis type II after experimentally induced infection of newborn germ-free pigs. Am J Vet Res 50:1037-1043.
23. Smith HE, Buijs H, Wisselink HJ, Stockhofe-Zurwieden N, Smits MA (2001) Selection of virulence-associated determinants of Streptococcus suis serotype 2 by in vivo complementation. Infect Immun 69:1961-1966. (Pubitemid 32187665)
24. De Greeff A, Wisselink HJ, De Bree FM, Schultsz C, Baums CG, et al. (2011) Genetic diversity of Streptococcus suis isolates as determined by comparative genome hybridization. BMC Microbiol 11:161.
25. Santi I, Pezzicoli A, Bosello M, Berti F, Mariani M, et al. (2008) Functional characterization of a newly identified group B Streptococcus pullulanase eliciting antibodies able to prevent alpha-glucans degradation. PLoS One 3:e3787.
26. Pfaffl MW (2001) A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29:e45.
27. Saulnier DM, Santos F, Roos S, Mistretta TA, Spinler JK, et al. (2011) Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PLoS One 6:e18783.
28. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, et al. (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30:e15.
29. Van Hijum SA, Garcia De La Nava J, Trelles O, Kok J, Kuipers OP (2003) MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics 2:241-244.
30. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, et al. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676. (Pubitemid 41264107)
31. Zdobnov EM, Apweiler R (2001) InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847-848. (Pubitemid 32970486)
32. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202-208.
33. Bailey TL, Gribskov M (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14:48-54. (Pubitemid 28395676)
34. Novichkov PS, Rodionov DA, Stavrovskaya ED, Novichkova ES, Kazakov AE, et al. (2010) RegPredict: an integrated system for regulon inference in prokaryotes by comparative genomics approach. Nucleic Acids Res 38:W299-307.
35. Chaptal V, Gueguen-Chaignon V, Poncet S, Lecampion C, Meyer P, et al. (2006) Structural analysis of B. subtilis CcpA effector binding site. Proteins 64:814-816. (Pubitemid 44100751)
36. Jacobs AA, Loeffen PL, Van Den Berg AJ, Storm PK (1994) Identification, purification, and characterization of a thiol-activated hemolysin (suilysin) of Streptococcus suis. Infect Immun 62:1742-1748. (Pubitemid 24136972)
37. Ferrari M, Losio MN, Bernori E, Lingeri R (1993) Established thyroid cell line of newborn pig (NPTh). New Microbiol 16:381-384.
38. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
39. Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28-36.
40. Miwa Y, Nakata A, Ogiwara A, Yamamoto M, Fujita Y (2000) Evaluation and characterization of catabolite-responsive elements (cre) of Bacillus subtilis. Nucleic Acids Res 28:1206-1210. (Pubitemid 30107692)
41. Lorca GL, Chung YJ, Barabote RD, Weyler W, Schilling CH, et al. (2005) Catabolite repression and activation in Bacillus subtilis: dependency on CcpA, HPr, and HprK. J Bacteriol 187:7826-7839. (Pubitemid 41587719)
42. Fujita Y (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci Biotechnol Biochem 73:245-259.
43. Willenborg J, Fulde M, De Greeff A, Rohde M, Smith HE, et al. (2011) Role of glucose and CcpA in capsule expression and virulence of Streptococcus suis. Microbiology 157:1823-1833.
44. Monedero V, Yebra MJ, Poncet S, Deutscher J (2008) Maltose transport in Lactobacillus casei and its regulation by inducer exclusion. Research in microbiology 159:94-102.
45. Schonert S, Seitz S, Krafft H, Feuerbaum EA, Andernach I, et al. (2006) Maltose and maltodextrin utilization by Bacillus subtilis. Journal of bacteriology 188:3911-3922. (Pubitemid 43825396)
46. Shim JH, Park JT, Hong JS, Kim KW, Kim MJ, et al. (2009) Role of maltogenic amylase and pullulanase in maltodextrin and glycogen metabolism of Bacillus subtilis 168. Journal of bacteriology 191:4835-4844.
47. Gopal S, Berg D, Hagen N, Schriefer EM, Stoll R, et al. (2010) Maltose and maltodextrin utilization by Listeria monocytogenes depend on an inducible ABC transporter which is repressed by glucose. PloS one 5:e10349.
48. Zhang X, Rogers M, Bierschenk D, Bonten MJ, Willems RJ, et al. (2013) A LacI-family regulator activates maltodextrin metabolism of Enterococcus faecium. PLoS One 8:e72285.
49. Benga L, Goethe R, Rohde M, Valentin-Weigand P (2004) Non-encapsulated strains reveal novel insights in invasion and survival of Streptococcus suis in epithelial cells. Cell Microbiol 6:867-881. (Pubitemid 39162628)
50. Iyer R, Baliga NS, Camilli A (2005) Catabolite control protein A (CcpA) contributes to virulence and regulation of sugar metabolism in Streptococcus pneumoniae. J Bacteriol 187:8340-8349. (Pubitemid 41780498)
51. Shelburne SA, 3rd, Keith D, Horstmann N, Sumby P, Davenport MT, et al. (2008) A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc Natl Acad Sci U S A 105:1698-1703. (Pubitemid 351346577)
52. Pan X, Ge J, Li M, Wu B, Wang C, et al. (2009) The orphan response regulator CovR: a globally negative modulator of virulence in Streptococcus suis serotype 2. J Bacteriol 191:2601-2612.
53. Seitz M, Baums CG, Neis C, Benga L, Fulde M, et al. (2013) Subcytolytic effects of suilysin on interaction of Streptococcus suis with epithelial cells. Vet Microbiol 167:584-591.
54. Vanier G, Segura M, Gottschalk M (2007) Characterization of the invasion of porcine endothelial cells by Streptococcus suis serotype 2. Can J Vet Res 71:81-89. (Pubitemid 46730813)
55. Charland N, Nizet V, Rubens CE, Kim KS, Lacouture S, et al. (2000) Streptococcus suis serotype 2 interactions with human brain microvascular endothelial cells. Infect Immun 68:637-643. (Pubitemid 30056517)
56. Lecours MP, Gottschalk M, Houde M, Lemire P, Fittipaldi N, et al. (2011) Critical role for Streptococcus suis cell wall modifications and suilysin in resistance to complement-dependent killing by dendritic cells. J Infect Dis 204:919-929.
57. Gottschalk M, Xu J, Calzas C, Segura M (2011) Streptococcus suis: a new emerging or an old neglected zoonotic pathogen? Future Microbiol 5:371-391.
58. Allen AG, Bolitho S, Lindsay H, Khan S, Bryant C, et al. (2001) Generation and characterization of a defined mutant of Streptococcus suis lacking suilysin. Infect Immun 69:2732-2735. (Pubitemid 32239752)
59. King SJ, Heath PJ, Luque I, Tarradas C, Dowson CG, et al. (2001) Distribution and genetic diversity of suilysin in Streptococcus suis isolated from different diseases of pigs and characterization of the genetic basis of suilysin absence. Infect Immun 69:7572-7582. (Pubitemid 33086584)
60. Bonafonte MA, Solano C, Sesma B, Alvarez M, Montuenga L, et al. (2000) The relationship between glycogen synthesis, biofilm formation and virulence in Salmonella enteritidis. FEMS Microbiol Lett 191:31-36.
61. Bourassa L, Camilli A (2009) Glycogen contributes to the environmental persistence and transmission of Vibrio cholerae. Mol Microbiol 72:124-138.
62. Chang DE, Smalley DJ, Tucker DL, Leatham MP, Norris WE, et al. (2004) Carbon nutrition of Escherichia coli in the mouse intestine. Proc Natl Acad Sci U S A 101:7427-7432. (Pubitemid 38638049)
63. Fabich AJ, Jones SA, Chowdhury FZ, Cernosek A, Anderson A, et al. (2008) Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine. Infect Immun 76:1143-1152. (Pubitemid 351428075)
64. Henrissat B, Deleury E, Coutinho PM (2002) Glycogen metabolism loss: a common marker of parasitic behaviour in bacteria? Trends Genet 18:437-440.
65. Jones SA, Jorgensen M, Chowdhury FZ, Rodgers R, Hartline J, et al. (2008) Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine. Infect Immun 76:2531-2540.
66. Sambou T, Dinadayala P, Stadthagen G, Barilone N, Bordat Y, et al. (2008) Capsular glucan and intracellular glycogen of Mycobacterium tuberculosis: biosynthesis and impact on the persistence in mice. Mol Microbiol 70:762-774.
67. Wilson WA, Roach PJ, Montero M, Baroja-Fernandez E, Munoz FJ, et al. (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952-985.
68. Pitsillides AA, Skerry TM, Edwards JC (1999) Joint immobilization reduces synovial fluid hyaluronan concentration and is accompanied by changes in the synovial intimal cell populations. Rheumatology (Oxford) 38:1108-1112. (Pubitemid 29537332)
69. Praest BM, Greiling H, Kock R (1997) Assay of synovial fluid parameters: hyaluronan concentration as a potential marker for joint diseases. Clin Chim Acta 266:117-128. (Pubitemid 28034191)
70. Hui AY, McCarty WJ, Masuda K, Firestein GS, Sah RL (2012) A systems biology approach to synovial joint lubrication in health, injury, and disease. Wiley Interdiscip Rev Syst Biol Med 4:15-37.
71. Smith HE, Damman M, Van Der Velde J, Wagenaar F, Wisselink HJ, et al. (1999) Identification and characterization of the cps locus of Streptococcus suis serotype 2: the capsule protects against phagocytosis and is an important virulence factor. Infect Immun 67:1750-1756. (Pubitemid 29144393)
72. 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.
73. Fittipaldi N, Sekizaki T, Takamatsu D, De La Cruz Dominguez-Punaro M, Harel J, et al. (2008) Significant contribution of the pgdA gene to the virulence of Streptococcus suis. Mol Microbiol 70:1120-1135.
74. Fittipaldi N, Sekizaki T, Takamatsu D, Harel J, Dominguez-Punaro Mde L, et al. (2008) D-alanylation of lipoteichoic acid contributes to the virulence of Streptococcus suis. Infect Immun 76:3587-3594.
75. 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. (Pubitemid 34163407)
76. Esgleas M, Li Y, Hancock MA, Harel J, Dubreuil JD, et al. (2008) Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154:2668-2679.
77. Brassard J, Gottschalk M, Quessy S (2004) Cloning and purification of the Streptococcus suis serotype 2 glyceraldehyde-3-phosphate dehydrogenase and its involvement as an adhesin. Vet Microbiol 102:87-94. (Pubitemid 39037377)
78. Ge J, Feng Y, Ji H, Zhang H, Zheng F, et al. (2009) Inactivation of dipeptidyl peptidase IV attenuates the virulence of Streptococcus suis serotype 2 that causes streptococcal toxic shock syndrome. Curr Microbiol 59:248-255.
79. Jobin MC, Grenier D (2003) Identification and characterization of four proteases produced by Streptococcus suis. FEMS Microbiol Lett 220:113-119. (Pubitemid 36324329)
80. Tan C, Fu S, Liu M, Jin M, Liu J, et al. (2008) Cloning, expression and characterization of a cell wall surface protein, 6-phosphogluconate- dehydrogenase, of Streptococcus suis serotype 2. Vet Microbiol 130:363-370.
81. Si Y, Yuan F, Chang H, Liu X, Li H, et al. (2009) Contribution of glutamine synthetase to the virulence of Streptococcus suis serotype 2. Vet Microbiol 139:80-88.
82. Kouki A, Haataja S, Loimaranta V, Pulliainen AT, Nilsson UJ, et al. (2011) Identification of a novel streptococcal adhesin P (SadP) protein recognizing galactosyl-alpha1-4-galactose-containing glycoconjugates: convergent evolution of bacterial pathogens to binding of the same host receptor. J Biol Chem 286:38854-38864.
83. Winterhoff N, Goethe R, Gruening P, Rohde M, Kalisz H, et al. (2002) Identification and characterization of two temperature-induced surface-associated proteins of Streptococcus suis with high homologies to members of the Arginine Deiminase system of Streptococcus pyogenes. J Bacteriol 184:6768-6776. (Pubitemid 36356111)
84. Fontaine MC, Perez-Casal J, Willson PJ (2004) Investigation of a novel DNase of Streptococcus suis serotype 2. Infect Immun 72:774-781. (Pubitemid 38166655)
85. Bonifait L, Vaillancourt K, Gottschalk M, Frenette M, Grenier D (2010) Purification and characterization of the subtilisin-like protease of Streptococcus suis that contributes to its virulence. Vet Microbiol 148:333-340.
86. Zhang A, Mu X, Chen B, Han L, Chen H, et al. (2010) IgA1 protease contributes to the virulence of Streptococcus suis. Vet Microbiol 148:436-439.
87. Allen AG, Lindsay H, Seilly D, Bolitho S, Peters SE, et al. (2004) Identification and characterisation of hyaluronate lyase from Streptococcus suis. Microb Pathog 36:327-335. (Pubitemid 38543060)
88. Tonnaer EL, Hafmans TG, Van Kuppevelt TH, Sanders EA, Verweij PE, et al. (2006) Involvement of glycosaminoglycans in the attachment of pneumococci to nasopharyngeal epithelial cells. Microbes Infect 8:316-322. (Pubitemid 43216261)
89. Vanier G, Sekizaki T, Dominguez-Punaro MC, Esgleas M, Osaki M, et al. (2007) Disruption of srtA gene in Streptococcus suis results in decreased interactions with endothelial cells and extracellular matrix proteins. Vet Microbiol.
90. Baums CG, Kaim U, Fulde M, Ramachandran G, Goethe R, et al. (2006) Identification of a novel virulence determinant with serum opacification activity in Streptococcus suis. Infect Immun 74:6154-6162. (Pubitemid 44657394)
91. Wen ZT, Burne RA (2002) Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl Environ Microbiol 68:1196-1203. (Pubitemid 34205358)
92. 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. (Pubitemid 26318177)