Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes

PLoS ONE

Volumn 4, Issue 1, 2009, Pages

  Courtney, Harry S ^a   Ofek, Itzhak ^a,b   Penfound, Thomas ^a   Nizet, Victor ^c   Pence, Morgan A ^c   Kreikemeyer, Bernd ^d   Podbielbski, Andreas ^d   Hasty, David L ^a   Dale, James B ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d ROSTOCK UNIVERSITY MEDICAL CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOTEICHOIC ACID; M PROTEIN; MULTIDRUG RESISTANCE PROTEIN; PROTEIN EMM; PROTEIN EMM1; PROTEIN ENN; PROTEIN SPA; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CARRIER PROTEIN; LIPOPOLYSACCHARIDE; OUTER MEMBRANE PROTEIN; STREPTOCOCCAL M PROTEIN; TEICHOIC ACID;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL METABOLISM; BACTERIAL MUTATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; COMPLEX FORMATION; CONTROLLED STUDY; CULTURE MEDIUM; GENE INACTIVATION; GENE OVEREXPRESSION; GENETIC VARIABILITY; HYDROPHOBICITY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SEROTYPE; STREPTOCOCCUS PYOGENES; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

STREPTOCOCCUS PYOGENES;

ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOFILMS; CARRIER PROTEINS; HYDROPHOBICITY; LIPOPOLYSACCHARIDES; STREPTOCOCCUS PYOGENES; TEICHOIC ACIDS;

EID: 58349111705     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004166     Document Type: Article

References (46)

1. Doyle RJ, Rosenberg M (1990) Microbial Cell Surface Hydrophobicity. Washington, DC: American Society for Microbiology. 425 p.
2. Courtney HS, Hasty DL, Ofek I (1990) Hydrophobicity of Group A Streptococci and Its Relationship to Adhesion of Streptococci to Host Cells. In: Doyle RJ, Rosenberg M, eds (1990) Microbial Cell Surface Hydrophobicity. Washington, DC: American Society for Microbiology. pp 361-386.
3. Fedtke I, Mader D, Kohler T, Moll H, Nicholson G, et al. (2007) A Staphylococcus aureus ypfP mutant with strongly reduced lipoteichoic acid (LTA) content: LTA governs bacterial surface properties and autolysin activity. Mol Microbiol 65: 1078-1091.
4. Miorner H, Johansson G, Kronvall G (1983) Lipoteichoic acid is the major cell wall component responsible for surface hydrophobicity of group A streptococci. Infect Immun 39: 336-343.
5. Fischer W (1988) Physiology of lipoteichoic acids in bacteria. Adv Microb Physiol 29: 233-302.
6. Neuhaus FC, Baddiley J (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67: 686-723.
7. Ginsburg I (2002) Role of lipoteichoic acid in infection and inflammation. Lancet Infect Dis 2: 171-179.
8. Hasty DL, Meron-Sudai S, Cox KH, Nagorna T, Ruiz-Bustos E, et al. (2006) Monocyte and macrophage activation by lipoteichoic acid is independent of alanine and is potentiated by hemoglobin. J Immunol 176: 5567-5576.
9. Morath S, Stadelmaier A, Geyer A, Schmidt RR, Hartung T (2002) Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 195: 1635-1640.
10. Grundling A, Schneewind O (2007) Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci U S A 104: 8478-8483.
11. Hasty DL, Ofek I, Courtney HS, Doyle RJ (1992) Multiple adhesins of streptococci. Infect Immun 60: 2147-2152.
12. Ofek I, Whitnack E, Beachey EH (1983) Hydrophobic interactions of group A streptococci with hexadecane droplets. J Bacteriol 154: 139-145.
13. Courtney HS, Simpson WA, Beachey EH (1983) Binding of streptococcal lipoteichoic acid to fatty acid-binding sites on human plasma fibronectin. J Bacteriol 153: 763-770.
14. Kalia A, Bessen DE (2004) Natural selection and evolution of streptococcal virulence genes involved in tissue-specific adaptations. J Bacteriol 186: 110-121.
15. Bessen DE, Sotir CM, Readdy TL, Hollingshead SK (1996) Genetic correlates of throat and skin isolates of group A streptococci. J Infect Dis 173: 896-900.
16. Bessen DE, Izzo MW, McCabe EJ, Sotir CM (1997) Two-domain motif for IgG-binding activity by group A streptococcal emm gene products. Gene 196: 75-82.
17. Ofek I, Simpson WA, Beachey EH (1982) Formation of molecular complexes between a structurally defined M protein and acylated or deacylated lipoteichoic acid of Streptococcus pyogenes. J Bacteriol 149: 426-433.
18. McLellan DG, Chiang EY, Courtney HS, Hasty DL, Wei SC, et al. (2001) Spa contributes to the virulence of type 18 group A streptococci. Infect Immun 69: 2943-2949.
19. Dale JB, Chiang EY, Liu S, Courtney HS, Hasty DL (1999) New protective antigen of group A streptococci. J Clin Invest 103: 1261-1268.
20. Maguin E, Prevost H, Ehrlich SD, Gruss A (1996) Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol 178: 931-935.
21. Lancefield RC (1928) The antigenic complex of Streptococcus hemolyticus, I Demonstration of a type-specific substance in extracts of Streptococcus hemolyticus. J Exp Med 47: 9-10.
22. Chaffin DO, Rubens CE (1998) Blue/white screening of recombinant plasmids in Gram-positive bacteria by interruption of alkaline phosphatase gene (phoZ) expression. Gene 219: 91-99.
23. Jeng A, Sakota V, Li Z, Datta V, Beall B, et al. (2003) Molecular genetic analysis of a group A Streptococcus operon encoding serum opacity factor and a novel fibronectin-binding protein, SfbX. J Bacteriol 185: 1208-1217.
24. Kraus W, Haanes-Fritz E, Cleary PP, Seyer JM, Dale JB, et al. (1987) Sequence and type-specific immunogenicity of the amino-terminal region of type 1 streptococcal M protein. J Immunol 139: 3084-3090.
25. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, et al. (1985) Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 22: 996-1006.
26. Lembke C, Podbielski A, Hidalgo-Grass C, Jonas L, Hanski E, et al. (2006) Characterization of biofilm formation by clinically relevant serotypes of group A streptococci. Appl Environ Microbiol 72: 2864-2875.
27. Baldassarri L, Creti R, Recchia S, Imperi M, Facinelli B, et al. (2006) Therapeutic failures of antibiotics used to treat macrolide-susceptible Streptococcus pyogenes infections may be due to biofilm formation. J Clin Microbiol 44: 2721-2727.
28. Ofek I, Beachey EH, Jefferson W, Campbell GL (1975) Cell membrane-binding properties of group A streptococcal lipoteichoic acid. J Exp Med 141: 990-1003.
29. Hogg SD, Old LA (1993) The wall associated lipoteichoic acid of Streptococcus sanguis. Antonie Van Leeuwenhoek 63: 29-34.
30. Morath S, Geyer A, Spreitzer I, Hermann C, Hartung T (2002) Structural decomposition and heterogeneity of commercial lipoteichoic Acid preparations. Infect Immun 70: 938-944.
31. Slade HD (1957) Studies on Streptococcus pyogenes. III. The effect of trypsin and a cationic detergent on the structure, permeability, and metabolism of the cell. J Gen Physiol 41: 63-76.
32. Carlsson F, Stalhammar-Carlemalm M, Flardh K, Sandin C, Carlemalm E, et al. (2006) Signal sequence directs localized secretion of bacterial surface proteins. Nature 442: 943-946.
33. Courtney HS, Podbielski A (2004) Group A Streptococcal Invasion of Host Cells. In: Lamont RJ, ed (2004) Bacterial Invasion of Host Cells. Cambridge: Cambridge University Press. pp 239-273.
34. Courtney HS, Hasty DL, Dale JB (2002) Molecular mechanisms of adhesion, colonization, and invasion of group A streptococci. Ann Med 34: 77-87.
35. Podbielski A, Schnitzler N, Beyhs P, Boyle MD (1996) M-related protein (Mrp) contributes to group A streptococcal resistance to phagocytosis by human granulocytes. Mol Microbiol 19: 429-441.
36. Courtney HS, Hasty DL, Dale JB (2006) Anti-phagocytic mechanisms of Streptococcus pyogenes: binding of fibrinogen to M-related protein. Mol Microbiol 59: 936-947.
37. Perez-Caballero D, Garcia-Laorden I, Cortes G, Wessels MR, de Cordoba SR, et al. (2004) Interaction between complement regulators and Streptococcus pyogenes: binding of C4b-binding protein and factor H/ factor H-like protein 1 to M18 strains involves two different cell surface molecules. J Immunol 173: 6899-6904.
38. Cho KH, Caparon MG (2005) Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Mol Microbiol 57: 1545-1556.
39. Manetti AG, Zingaretti C, Falugi F, Capo S, Bombaci M, et al. (2007) Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 64: 968-983.
40. Eran Y, Getter Y, Baruch M, Belotserkovsky I, Padalon G, et al. (2007) Transcriptional regulation of the sil locus by the SilCR signalling peptide and its implications on group A streptococcus virulence. Mol Microbiol 63: 1209-1222.
41. Podbielski A, Flosdorff A, Weber-Heynemann J (1995) The group A streptococcal virR49 gene controls expression of four structural vir regulon genes. Infect Immun 63: 9-20.
42. Frick IM, Morgelin M, Bjorck L (2000) Virulent aggregates of Streptococcus pyogenes are generated by homophilic protein-protein interactions. Mol Microbiol 37: 1232-1247.
43. Cunningham MW (2000) Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13: 470-511.
44. Kansal RG, McGeer A, Low DE, Norrby-Teglund A, Kotb M (2000) Inverse relation between disease severity and expression of the streptococcal cysteine protease, SpeB, among clonal M1T1 isolates recovered from invasive group A streptococcal infection cases. Infect Immun 68: 6362-6369.
45. Norgren M, Caparon MG, Scott JR (1989) A method for allelic replacement that uses the conjugative transposon Tn916: deletion of the emm6.1 allele in Streptococcus pyogenes JRS4. Infect Immun 57: 3846-3850.
46. Courtney HS, Bronze MS, Dale JB, Hasty DL (1994) Analysis of the role of M24 protein in group A streptococcal adhesion and colonization by use of omega-interposon mutagenesis. Infect Immun 62: 4868-4873.