Phase Variation of Poly-N-Acetylglucosamine Expression in

English version České info

Staphylococcal polysaccharide intercellular adhesin (PIA), also known as β-1-6-linked N-acetylglucosamine (PNAG) plays a role in immune evasion and biofilm formation. Evidence suggests that under certain circumstances PIA/PNAG production is beneficial, whereas at times, it may be advantageous for the bacteria to turn production off. In S. epidermidis, PIA/PNAG can be switched off when an insertion sequence recombines into the intercellular adhesin locus (ica). In this study, we have found a short tandem repeat sequence in the ica locus of S. aureus that can undergo expansion and contraction. The addition or subtraction of non-multiples of three of this repeat shifts the reading frame of the icaC gene, resulting in the complete loss of PIA/PNAG production. We hypothesize that certain conditions that make the PIA/PNAG-negative phenotype advantageous during infection, such as the development of an effective immune response to PIA/PNAG on the bacterial surface, would select for repeat mutants. In support of this hypothesis, we found clinical isolates with expansion and deletion of the repeat. These findings reveal a new on-off switch for the expression of PIA/PNAG.

Vyšlo v časopise: Phase Variation of Poly-N-Acetylglucosamine Expression in. PLoS Pathog 10(7): e32767. doi:10.1371/journal.ppat.1004292
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004292

Souhrn

Zdroje

1. LevinsonG, GutmanGA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4 : 203–221.

2. DeLeoFR, ChambersHF (2009) Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J Clin Invest 119 : 2464–2474.

3. CosP, ToteK, HoremansT, MaesL (2010) Biofilms: an extra hurdle for effective antimicrobial therapy. Curr Pharm Des 16 : 2279–2295.

4. StewartPS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Ijmm Int J Med Microbiol 292 : 107–113.

5. StewartPS, CostertonJW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358 : 135–138.

6. MackD, FischerW, KrokotschA, LeopoldK, HartmannR, et al. (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178 : 175–183.

7. Maira-LitránT, KropecA, AbeygunawardanaC, JoyceJ, MarkG3rd, et al. (2002) Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 70 : 4433–4440.

8. CercaN, JeffersonKK, Maira-LitránT, PierDB, Kelly-QuintosC, et al. (2007) Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1–6)-glucosamine. Infect Immun 75 : 3406–3413.

9. McKenneyD, HubnerJ, MullerE, WangY, GoldmannDA, et al. (1998) The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun 66 : 4711–4720.

10. Maira-LitránT, BentancorLV, Bozkurt-GuzelC, O'MalleyJM, Cywes-BentleyC, et al. (2012) Synthesis and evaluation of a conjugate vaccine composed of Staphylococcus aureus poly-N-acetyl-glucosamine and clumping factor A. PLoS One 7: e43813.

11. HeilmannC, SchweitzerO, GerkeC, VanittanakomN, MackD, et al. (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20 : 1083–1091.

12. CramtonSE, GerkeC, SchnellNF, NicholsWW, GötzF (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infection & Immunity 67 : 5427–5433.

13. GerkeC, KraftA, SussmuthR, SchweitzerO, GötzF (1998) Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem 273 : 18586–18593.

14. VuongC, KocianovaS, VoyichJM, YaoY, FischerER, et al. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279 : 54881–54886.

15. JeffersonKK, CramtonSE, GötzF, PierGB (2003) 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 48 : 889–899.

16. MajerczykCD, SadykovMR, LuongTT, LeeC, SomervilleGA, et al. (2008) Staphylococcus aureus CodY negatively regulates virulence gene expression. J Bacteriol 190 : 2257–2265.

17. ValleJ, Toledo-AranaA, BerasainC, GhigoJM, AmorenaB, et al. (2003) SarA and not sigma(B) is essential for biofilm development by Staphylococcus aureus. Mol Microbiol 48 : 1075–1087.

18. TamberS, CheungAL (2009) SarZ promotes the expression of virulence factors and represses biofilm formation by modulating SarA and agr in Staphylococcus aureus. Infect Immun 77 : 419–428.

19. ArcherNK, MazaitisMJ, CostertonJW, LeidJG, PowersME, et al. (2011) Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2 : 445–459.

20. McKenneyD, PouliotKL, WangY, MurthyV, UlrichM, et al. (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284 : 1523–1527.

21. PokrzywaR, PolanskiA (2010) BWtrs: A tool for searching for tandem repeats in DNA sequences based on the Burrows-Wheeler transform. Genomics 96 : 316–321.

22. Cywes-BentleyC, SkurnikD, ZaidiT, RouxD, DeoliveiraRB, et al. (2013) Antibody to a conserved antigenic target is protective against diverse prokaryotic and eukaryotic pathogens. Proc Natl Acad Sci U S A 110: E2209–2218.

23. Martin-LopezJV, Perez-RothE, Claverie-MartinF, Diez GilO, BatistaN, et al. (2002) Detection of Staphylococcus aureus Clinical Isolates Harboring the ica Gene Cluster Needed for Biofilm Establishment. J Clin Microbiol 40 : 1569–1570.

24. Juarez-VerdayesMA, Ramon-PerezML, Flores-PaezLA, Camarillo-MarquezO, ZentenoJC, et al. (2013) Staphylococcus epidermidis with the icaA-/icaD-/IS256 -⁠ genotype and protein or protein/extracellular-DNA biofilm is frequent in ocular infections. J Med Microbiol 62(Pt 10): 1579–87.

25. ZiebuhrW, KrimmerV, RachidS, LossnerI, GötzF, et al. (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32 : 345–356.

26. KiemS, OhWS, PeckKR, LeeNY, LeeJY, et al. (2004) Phase variation of biofilm formation in Staphylococcus aureus by IS 256 insertion and its impact on the capacity adhering to polyurethane surface. J Korean Med Sci 19 : 779–782.

27. CramtonSE, UlrichM, GötzF, DoringG (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun 69 : 4079–4085.

28. RogersKL, RuppME, FeyPD (2008) The presence of icaADBC is detrimental to the colonization of human skin by Staphylococcus epidermidis. Appl Environ Microbiol 74 : 6155–6157.

29. PeacockSJ, MooreCE, JusticeA, KantzanouM, StoryL, et al. (2002) Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70 : 4987–4996.

30. MachucaMA, SosaLM, GonzalezCI (2013) Molecular typing and virulence characteristic of methicillin-resistant Staphylococcus aureus isolates from pediatric patients in bucaramanga, Colombia. PLoS One 8: e73434.

31. Maira-LitránT, KropecA, GoldmannDA, PierGB (2005) Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated Staphylococcal Poly-N-acetyl-beta-(1–6)-glucosamine. Infect Immun 73 : 6752–6762.

32. SchlievertPM, BlomsterDA (1983) Production of staphylococcal pyrogenic exotoxin type C: influence of physical and chemical factors. J Infect Dis 147 : 236–242.

33. ArnaudM, ChastanetA, DébarbouilléM (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70 : 6887–6891.

34. LuongTT, LeeCY (2006) The arl locus positively regulates Staphylococcus aureus type 5 capsule via an mgrA-dependent pathway. Microbiology 152 : 3123–3131.

35. LeeJC (1995) Electrotransformation of Staphylococci. Methods Mol Biol 47 : 209–216.

36. SanderP, SpringerB, PrammanananT, SturmfelsA, KapplerM, et al. (2002) Fitness cost of chromosomal drug resistance-conferring mutations. Antimicrob Agents Chemother 46 : 1204–1211.

37. ChristensenGD, SimpsonWA, YoungerJJ, BaddourLM, BarrettFF, 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.

38. SkinnerME, UzilovAV, SteinLD, MungallCJ, HolmesIH (2009) JBrowse: a next-generation genome browser. Genome Res 19 : 1630–1638.

39. HoldenMT, LindsayJA, CortonC, QuailMA, CockfieldJD, et al. (2010) Genome sequence of a recently emerged, highly transmissible, multi-antibiotic -⁠ and antiseptic-resistant variant of methicillin-resistant Staphylococcus aureus, sequence type 239 (TW). J Bacteriol 192 : 888–892.

40. Costa MO, Beltrame CO, Ferreira FA, Botelho AM, Lima NC, et al.. (2013) Complete Genome Sequence of a Variant of the Methicillin-Resistant Staphylococcus aureus ST239 Lineage, Strain BMB9393, Displaying Superior Ability To Accumulate ica-Independent Biofilm. Genome Announc 1: pii: e00576–13

41. Chen FJ, Lauderdale TL, Wang LS, Huang IW (2013) Complete Genome Sequence of Staphylococcus aureus Z172, a Vancomycin-Intermediate and Daptomycin-Nonsusceptible Methicillin-Resistant Strain Isolated in Taiwan. Genome Announc 1: pii: e01011–13

42. LiY, CaoB, ZhangY, ZhouJ, YangB, et al. (2011) Complete genome sequence of Staphylococcus aureus T0131, an ST239-MRSA-SCCmec type III clone isolated in China. J Bacteriol 193 : 3411–3412.

43. HowdenBP, SeemannT, HarrisonPF, McEvoyCR, StantonJA, et al. (2010) Complete genome sequence of Staphylococcus aureus strain JKD6008, an ST239 clone of methicillin-resistant Staphylococcus aureus with intermediate-level vancomycin resistance. J Bacteriol 192 : 5848–5849.