Home LiteratureArticle Details
PMID: 15731082 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model.

Infection and immunity ·Vol. 73 ·No. 3 ·2005-03-00 ·Pages 1811-9

Fluckiger U, Ulrich M, Steinhuber A, Döring G, Mack D, Landmann R, Goerke C, Wolz C

Abstract

Biofilm formation of Staphylococcus epidermidis and S. aureus is mediated by the polysaccharide intercellular adhesin (PIA) encoded by the ica operon. We used a device-related animal model to investigate biofilm formation, PIA expression (immunofluorescence), and ica transcription (quantitative transcript analysis) throughout the course of infection by using two prototypic S. aureus strains and one S. epidermidis strain as well as corresponding ica mutants. During infection, the ica mutants were growth attenuated when inoculated in competition with the corresponding wild-type strains but not when grown singly. A typical biofilm was observed at the late course of infection. Only in S. aureus RN6390, not in S. aureus Newman, were PIA and ica-specific transcripts detectable after anaerobic growth in vitro. However, both S. aureus strains were PIA positive in vivo by day 8 of infection. ica transcription preceded PIA expression and biofilm formation in vivo. In S. epidermidis, both PIA and ica expression levels were elevated compared to those in the S. aureus strains in vitro as well as in vivo and were detectable throughout the course of infection. In conclusion, in S. aureus, PIA expression is dependent on the genetic background of the strain as well as on strong inducing conditions, such as those dominating in vivo. In S. epidermidis, PIA expression is elevated and less vulnerable to environmental conditions.

MeSH Terms
Adhesins, Bacterial/genetics,metabolism Amidohydrolases/genetics,metabolism Animals Bacterial Proteins/genetics,metabolism Biofilms/growth & development Disease Models, Animal Guinea Pigs Humans Mice Operon Polysaccharides, Bacterial/genetics,metabolism Prosthesis-Related Infections/microbiology,physiopathology Staphylococcal Infections/microbiology,physiopathology Staphylococcus aureus/growth & development,pathogenicity Staphylococcus epidermidis/growth & development,pathogenicity Transcription, Genetic
Chemicals
Adhesins, Bacterial Bacterial Proteins Polysaccharides, Bacterial polysaccharide intercellular adhesin Amidohydrolases poly-N-acetylglucosamine deacetylase
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Fluckiger Ursula
Division of Infectious Diseases and Department of Research, University Hospital, Basel, Switzerland.
Ulrich Martina
Steinhuber Andrea
Döring Gerd
Mack Dietrich
Landmann Regine
Goerke Christiane
Wolz Christiane
References (57)
57 references, click to expand
  1. PCR-Based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains.
    J Clin Microbiol. 2000 Feb;38(2):877-80 PMID: 10655405
  2. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis.
    J Infect Dis. 2003 Sep 1;188(5):706-18 PMID: 12934187
  3. Identification of three essential regulatory gene loci governing expression of Staphylococcus epidermidis polysaccharide intercellular adhesin and biofilm formation.
    Infect Immun. 2000 Jul;68(7):3799-807 PMID: 10858187
  4. Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses.
    J Infect Dis. 2000 Jul;182(1):351-5 PMID: 10882623
  5. Alternative transcription factor sigma(B) is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate.
    J Bacteriol. 2000 Dec;182(23):6824-6 PMID: 11073930
  6. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model.
    J Infect Dis. 2001 Apr 1;183(7):1038-42 PMID: 11237828
  7. Quantification of bacterial transcripts during infection using competitive reverse transcription-PCR (RT-PCR) and LightCycler RT-PCR.
    Clin Diagn Lab Immunol. 2001 Mar;8(2):279-82 PMID: 11238208
  8. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress.
    J Bacteriol. 2001 Apr;183(8):2624-33 PMID: 11274123
  9. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis.
    Infect Immun. 2001 Jun;69(6):4079-85 PMID: 11349079
  10. Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections.
    J Clin Microbiol. 2001 Jun;39(6):2151-6 PMID: 11376050
  11. Detection of Staphylococcus aureus Clinical Isolates Harboring the ica Gene Cluster Needed for Biofilm Establishment.
    J Clin Microbiol. 2002 Apr;40(4):1569-70 PMID: 11923401
  12. Transcription of clumping factor A in attached and unattached Staphylococcus aureus in vitro and during device-related infection.
    Infect Immun. 2002 Jun;70(6):2758-62 PMID: 12010960
  13. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis.
    J Bacteriol. 2002 Aug;184(16):4400-8 PMID: 12142410
  14. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus.
    Infect Immun. 2002 Sep;70(9):4987-96 PMID: 12183545
  15. Biofilms: microbial life on surfaces.
    Emerg Infect Dis. 2002 Sep;8(9):881-90 PMID: 12194761
  16. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model.
    Microb Pathog. 2004 May;36(5):237-45 PMID: 15043859
  17. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces.
    Infect Immun. 1982 Jul;37(1):318-26 PMID: 6179880
  18. Pathogenesis of foreign body infection: description and characteristics of an animal model.
    J Infect Dis. 1982 Oct;146(4):487-97 PMID: 7119479
  19. Characterization of clinically significant strains of coagulase-negative staphylococci.
    J Clin Microbiol. 1983 Aug;18(2):258-69 PMID: 6311870
  20. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices.
    J Clin Microbiol. 1985 Dec;22(6):996-1006 PMID: 3905855
  21. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus.
    J Bacteriol. 1988 Sep;170(9):4365-72 PMID: 2457579
  22. Genetic systems in staphylococci.
    Methods Enzymol. 1991;204:587-636 PMID: 1658572
  23. Parallel induction by glucose of adherence and a polysaccharide antigen specific for plastic-adherent Staphylococcus epidermidis: evidence for functional relation to intercellular adhesion.
    Infect Immun. 1992 May;60(5):2048-57 PMID: 1314224
  24. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6462-6 PMID: 1321441
  25. Occurrence of capsular polysaccharide/adhesin among clinical isolates of coagulase-negative staphylococci.
    J Infect Dis. 1993 Nov;168(5):1211-8 PMID: 8228355
  26. Influence of some plasma proteins on in vitro bacterial adherence to PTFE and Dacron vascular prostheses.
    APMIS. 1993 Dec;101(12):926-32 PMID: 8110449
  27. Characterization of transposon mutants of biofilm-producing Staphylococcus epidermidis impaired in the accumulative phase of biofilm production: genetic identification of a hexosamine-containing polysaccharide intercellular adhesin.
    Infect Immun. 1994 Aug;62(8):3244-53 PMID: 8039894
  28. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis.
    J Bacteriol. 1996 Jan;178(1):175-83 PMID: 8550413
  29. Influence of strain, biomaterial, proteins, and oncostatic chemotherapy on Staphylococcus epidermidis adhesion to intravascular catheters in vitro.
    J Lab Clin Med. 1996 Jan;127(1):71-80 PMID: 8592099
  30. Infection after total hip arthroplasty. A study of the treatment of one hundred and six infections.
    J Bone Joint Surg Am. 1996 Apr;78(4):512-23 PMID: 8609130
  31. Influence of agr on fibrinogen binding in Staphylococcus aureus Newman.
    Infect Immun. 1996 Aug;64(8):3142-7 PMID: 8757845
  32. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis.
    Mol Microbiol. 1996 Jun;20(5):1083-91 PMID: 8809760
  33. Detection of the intercellular adhesion gene cluster (ica) and phase variation in Staphylococcus epidermidis blood culture strains and mucosal isolates.
    Infect Immun. 1997 Mar;65(3):890-6 PMID: 9038293
  34. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface.
    Mol Microbiol. 1997 Jun;24(5):1013-24 PMID: 9220008
  35. Characterization of a sar homolog of Staphylococcus epidermidis.
    Infect Immun. 1998 Jun;66(6):2871-8 PMID: 9596762
  36. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin.
    J Biol Chem. 1998 Jul 17;273(29):18586-93 PMID: 9660830
  37. Essential functional role of the polysaccharide intercellular adhesin of Staphylococcus epidermidis in hemagglutination.
    Infect Immun. 1999 Feb;67(2):1004-8 PMID: 9916125
  38. Surface protein adhesins of Staphylococcus aureus.
    Trends Microbiol. 1998 Dec;6(12):484-8 PMID: 10036727
  39. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model.
    Infect Immun. 1999 May;67(5):2627-32 PMID: 10225932
  40. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model.
    Infect Immun. 1999 May;67(5):2656-9 PMID: 10225938
  41. Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen.
    Science. 1999 May 28;284(5419):1523-7 PMID: 10348739
  42. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation.
    Infect Immun. 1999 Oct;67(10):5427-33 PMID: 10496925
  43. Staphylococcal coagulase; mode of action and antigenicity.
    J Gen Microbiol. 1952 Feb;6(1-2):95-107 PMID: 14927856
  44. The intercellular adhesin locus ica is present in clinical isolates of Staphylococcus aureus from bacteremic patients with infected and uninfected prosthetic joints.
    Med Microbiol Immunol. 2001 Apr;189(3):127-31 PMID: 11388609
  45. Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of alpha-toxin during device-related infection resolved by direct quantitative transcript analysis.
    Mol Microbiol. 2001 Jun;40(6):1439-47 PMID: 11442841
  46. Biofilm formation: a clinically relevant microbiological process.
    Clin Infect Dis. 2001 Oct 15;33(8):1387-92 PMID: 11565080
  47. Correlation of Staphylococcus aureus icaADBC genotype and biofilm expression phenotype.
    J Clin Microbiol. 2001 Dec;39(12):4595-6 PMID: 11797608
  48. The ica operon and biofilm production in coagulase-negative Staphylococci associated with carriage and disease in a neonatal intensive care unit.
    J Clin Microbiol. 2002 Feb;40(2):382-8 PMID: 11825946
  49. Evaluation of different detection methods of biofilm formation in Staphylococcus aureus.
    Med Microbiol Immunol. 2002 Oct;191(2):101-6 PMID: 12410349
  50. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis.
    FEMS Immunol Med Microbiol. 2003 Mar 20;35(2):135-40 PMID: 12628549
  51. Management of infection associated with prosthetic joints.
    Infection. 2003 Mar;31(2):99-108 PMID: 12682815
  52. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis.
    J Bacteriol. 2003 May;185(9):2879-86 PMID: 12700267
  53. Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR.
    Mol Microbiol. 2003 May;48(4):889-99 PMID: 12753184
  54. SarA and not sigmaB is essential for biofilm development by Staphylococcus aureus.
    Mol Microbiol. 2003 May;48(4):1075-87 PMID: 12753197
  55. Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model.
    J Infect Dis. 2003 Aug 1;188(3):414-23 PMID: 12870123
  56. Requirement of the Yersinia pseudotuberculosis effectors YopH and YopE in colonization and persistence in intestinal and lymph tissues.
    Infect Immun. 2003 Aug;71(8):4595-607 PMID: 12874339
  57. Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro.
    Infect Immun. 2000 Mar;68(3):1304-11 PMID: 10678942
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2005-03-00
Pages
1811-9
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC1064907
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com