Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis

Microbial Pathogenesis

Volumn 51, Issue 1-2, 2011, Pages 58-68

  Ogawa, Taiji ^a   Terao, Yutaka ^a   Okuni, Hisashi ^b   Ninomiya, Keiko ^c   Sakata, Hiroshi ^d   Ikebe, Kazunori ^a   Maeda, Yoshinobu ^a   Kawabata, Shigetada ^a  

^a OSAKA UNIVERSITY   (Japan)

^b Health Science Research Institute East Japan Co Ltd   (Japan)

^c Ninomiya Clinic for Children   (Japan)

^d Asahikawa City Hospital   (Japan)

Author keywords

Antimicrobial peptide; Biofilm; Internalization; PrtF1; Streptococcus pyogenes

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT;

ARTICLE; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; CONTROLLED STUDY; EPITHELIUM CELL; ERADICATION THERAPY; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GENOTYPE; INNATE IMMUNITY; INTERNALIZATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STREPTOCOCCAL PHARYNGITIS; STREPTOCOCCUS PYOGENES;

ADHESINS, BACTERIAL; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BIOFILMS; CARRIER PROTEINS; CELL LINE; CHILD; CHILD, PRESCHOOL; EPITHELIAL CELLS; GENOTYPE; HELA CELLS; HUMANS; MICROBIAL SENSITIVITY TESTS; NASOPHARYNX; PHARYNGITIS; STREPTOCOCCAL INFECTIONS; STREPTOCOCCUS PYOGENES; TREATMENT FAILURE;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PYOGENES;

EID: 79955589530     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2011.03.009     Document Type: Article

References (51)

1. Cunningham M.W. Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 2000, 13:470-511.
2. Bisno A.L., Gerber M.A., Gwaltney J.M., Kaplan E.L., Schwartz R.H. Practice guidelines for the diagnosis and management of group A streptococcal pharyngitis. Infectious Diseases Society of America. Clin Infect Dis 2002, 35:113-125. Infectious Diseases Society of America.
3. Dajani A., Taubert K., Ferrieri P., Peter G., Shulman S. Treatment of acute streptococcal pharyngitis and prevention of rheumatic fever: a statement for health professionals. Committee on rheumatic fever, endocarditis, and kawasaki disease of council on cardiovascular disease in the young, the American Heart Association. Pediatrics 1995, 96:758-764.
4. Kuhn S.M., Preiksaitis J., Tyrrel G.J., Jadavji T., Church D., Davies H.D. Evaluation of potential factors contributing to microbiological treatment failure in Streptococcus pyogenes pharyngitis. Can J Infect Dis 2001, 12:33-39.
5. Macris M.H., Hartman N., Murray B., Klein R.F., Roberts R.B., Kaplan E.L., et al. Studies of the continuing susceptibility of group A streptococcal strains to penicillin during eight decades. Pediatr Infect Dis J 1998, 17:377-381.
6. Brook I. Penicillin failure and copathogenicity in streptococcal pharyngotonsillitis. J Fam Pract 1994, 38:175-179.
7. Neeman R., Keller N., Barzilai A., Korenman Z., Sela S. Prevalence of internalisation-associated gene, prtF1, among persisting group-a streptococcus strains isolated from asymptomatic carriers. Lancet 1998, 352:1974-1977.
8. Baldassarri L., Creti R., Recchia S., Imperi M., Facinelli B., Giovanetti E., et al. Therapeutic failures of antibiotics used to treat macrolide-susceptible Streptococcus pyogenes infections may be due to biofilm formation. J Clin Microbiol 2006, 44:2721-2727.
9. Hall-Stoodley L., Stoodley P. Evolving concepts in biofilm infections. Cell Microbiol 2009, 11:1034-1043.
10. Hoyle B.D., Costerton J.W. Bacterial resistance to antibiotics: the role of biofilms. Prog Drug Res 1991, 37:91-105.
11. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284:1318-1322.
12. Hutchison M.L., Govan J.R. Pathogenicity of microbes associated with cystic fibrosis. Microbes Infect 1999, 12:1005-1014.
13. Overhage J., Campisano A., Bains M., Torfs E.C., Rehm B.H., Hancock R.E. Human host defense peptide LL-37 p.events bacterial biofilm formation. Infect Immun 2008, 76:4176-4182.
14. Terao Y., Okamoto S., Kataoka K., Hamada S., Kawabata S. Protective immunity against Streptococcus pyogenes challenge in mice after immunization with fibronectin-binding protein. J Infect Dis 2005, 192:2081-2091.
15. Molinari G., Talay S.R., Valentin-Weigand P., Rohde M., Chhatwal G.S. The fibronectin-binding protein of Streptococcus pyogenes, SfbI, is involved in the internalization of group A streptococci by epithelial cells. Infect Immun 1997, 65:1357-1363.
16. Terao Y., Kawabata S., Kunitomo E., Murakami J., Nakagawa I., Hamada S. Fba, a novel fibronectin-binding protein from Streptococcus pyogenes, promotes bacterial entry into epithelial cells, and the fba gene is positively transcribed under the Mga regulator. Mol Microbiol 2001, 42:75-86.
17. Michos A.G., Bakoula C.G., Braoudaki M., Koutouzi F.I., Roma E.S., Pangalis A., et al. Macrolide resistance in Streptococcus pyogenes: prevalence, resistance determinants, and emm types. Diagn Microbiol Infect Dis 2009, 64:295-299.
18. Murakami J., Kawabata S., Terao Y., Kikuchi K., Totsuka K., Tamaru A., et al. Distribution of emm genotypes and superantigen genes of Streptococcus pyogenes isolated in Japan, 1994-9. Epidemiol Infect 2002, 128:397-404.
19. Courtney H.S., Ofek I., Penfound T., Nizet V., Pence M.A., Kreikemeyer B., et al. Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes. PLoS One 2009, 4:e4166.
20. Köller T., Manetti A.G., Kreikemeyer B., Lembke C., Margarit I., Grandi G., et al. Typing of the pilus-protein-encoding FCT region and biofilm formation as novel parameters in epidemiological investigations of Streptococcus pyogenes isolates from various infection sites. J Med Microbiol 2010, 59:442-452.
21. Manetti A.G., Köller T., Becherelli M., Buccato S., Kreikemeyer B., Podbielski A., et al. Environmental acidification drives S. pyogenes pilus expression and microcolony formation on epithelial cells in a FCT-dependent manner. PLoS One 2010, 5:e13864.
22. Bagge N., Hentzer M., Andersen J.B., Ciofu O., Givskov M., Høiby N. Dynamics and spatial distribution of beta-lactamase expression in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2004, 48:1168-1174.
23. Lenz A.P., Williamson K.S., Pitts B., Stewart P.S., Franklin M.J. Localized gene expression in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 2008, 74:4463-4471.
24. Wood D.N., Chaussee M.A., Chaussee M.S., Buttaro B.A. Persistence of Streptococcus pyogenes in stationary-phase cultures. J Bacteriol 2005, 187:3319-3328.
25. Zhang L., Mah T.F. Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 2008, 190:4447-4452.
26. Leid J.G., Shirtliff M.E., Costerton J.W., Stoodley P. Human leukocytes adhere, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 2002, 70:6339-6345.
27. Bjarnsholt T., Jensen P.Ø., Burmølle M., Hentzer M., Haagensen J.A., Hougen H.P., et al. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 2005, 151:373-383.
28. Turner J., Cho Y., Dinh N.N., Waring A.J., Lehrer R.I. Activities of LL-37, a cathelin-associated antimicrobial peptide of human neutrophils. Antimicrob Agents Chemother 1998, 42:2206-2214.
29. Harder J., Bartels J., Christophers E., Schroder J.M. Isolation and characterization of human betadefensin-3, a novel human inducible peptide antibiotic. J Biol Chem 2001, 276:5707-5713.
30. Bals R., Weiner D.J., Meegalla R.L., Wilson J.M. Transfer of a cathelicidin peptide antibiotic gene restores bacterial killing in a cystic fibrosis xenograft model. J Clin Invest 1999, 103:1113-1117.
31. Bowdish D.M., Davidson D.J., Lau Y.E., Lee K., Scott M.G., Hancock R.E. Impact of LL-37 on anti-infective immunity. J Leukoc Biol 2005, 77:451-459.
32. Vuong C., Voyich J.M., Fischer E.R., Braughton K.R., Whitney A.R., DeLeo F.R., et al. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell Microbiol 2004, 6:269-275.
33. Fernie-King B.A., Seilly D.J., Lachmann P.J. The interaction of streptococcal inhibitor of complement (SIC) and its proteolytic fragments with the human beta defensins. Immunology 2004, 111:444-452.
34. Frick I.M., Akesson P., Rasmussen M., Schmidtchen A., Björck L. SIC, a secreted protein of Streptococcus pyogenes that inactivates antibacterial peptides. J Biol Chem 2003, 278:16561-16566.
35. Akesson P., Sjöholm A.G., Björck L. Protein SIC, a novel extracellular protein of Streptococcus pyogenes interfering with complement function. J Biol Chem 1996, 271:1081-1088.
36. Tjelle T.E., Lovdal T., Berg T. Phagosome dynamics and function. Bioessays 2000, 22:255-263.
37. Molinari G., Rohde M., Guzmán C.A., Chhatwal G.S. Two distinct pathways for the invasion of Streptococcus pyogenes in non-phagocytic cells. Cell Microbiol 2000, 2:145-154.
38. Rosenberger C.M., Finlay B.B. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 2003, 4:385-396.
39. Ogawa M., Yoshimori T., Suzuki T., Sagara H., Mizushima N., Sasakawa C. Escape of intracellular Shigella from autophagy. Science 2005, 307:727-731.
40. Hernandez L.D., Pypaert M., Flavell R.A., Galán J.E. A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 2003, 163:1123-1131.
41. Nakagawa I., Amano A., Mizushima N., Yamamoto A., Yamaguchi H., Kamimoto T., et al. Autophagy defends cells against invading group A Streptococcus. Science 2004, 306:1037-1040.
42. Olsen R.J., Shelburne S.A., Musser J.M. Molecular mechanisms underlying group A streptococcal pathogenesis. Cell Microbiol 2009, 11:1-12.
43. Natanson S., Sela S., Moses A.E., Musser J.M., Caparon M.G., Hanski E. Distribution of fibronectin-binding proteins among group A streptococci of different M types. J Infect Dis 1995, 171:871-878.
44. Courtney H.S., Li Y., Dale J.B., Hasty D.L. Cloning, sequencing, and expression of a fibronectin/fibrinogen-binding protein from group A streptococci. Infect Immun 1994, 62:3937-3946.
45. Jaffe J., Natanson-Yaron S., Caparon M.G., Hanski E. Protein F2, a novel fibronectin-binding protein from Streptococcus pyogenes, possesses two binding domains. Mol Microbiol 1996, 21:373-384.
46. Kreikemeyer B., Talay S.R., Chhatwal G.S. Characterization of a novel fibronectin-binding surface protein in group A streptococci. Mol Microbiol 1995, 17:137-145.
47. Rocha C.L., Fischetti V.A. Identification and characterization of a novel fibronectin-binding protein on the surface of group A streptococci. Infect Immun 1999, 67:2720-2728.
48. Wang B., Dileepan T., Briscoe S., Hyland K.A., Kang J., Khoruts A., et al. Induction of TGF-β1 and TGF-β1-dependent predominant Th17 differentiation by group A streptococcal infection. Proc Natl Acad Sci U S A 2010, 107:5937-5942.
49. Kotb M., Norrby-Teglund A., McGeer A., El-Sherbini H., Dorak M.T., Khurshid A., et al. An immunogenetic and molecular basis for differences in outcomes of invasive group A streptococcal infections. Nat Med 2002, 12:1398-1404.
50. Manetti A.G., Zingaretti C., Falugi F., Capo S., Bombaci M., Bagnoli F., et al. Streptococcus pyogenes pili promote pharyngeal cell adhesion and biofilm formation. Mol Microbiol 2007, 64:968-983.
51. Terao Y., Kawabata S., Nakata M., Nakagawa I., Hamada S. Molecular characterization of a novel fibronectin-binding protein of Streptococcus pyogenes strains isolated from toxic shock-like syndrome patients. J Biol Chem 2002, 277:47428-47435.