Colonization of the Mouse Gastrointestinal Tract Is Modulated by Wall Teichoic Acid, Capsule, and Surface Proteins

English version České info

Staphylococcus aureus persistently colonizes ~20% of the human population, and 40–60% of humans are intermittently colonized by this bacterium. The most common reservoir for S. aureus is the anterior nares, and the incidence of staphylococcal disease in higher in individuals who are colonized. Rectal colonization by S. aureus isolates, reflecting gastrointestinal (GI) carriage, has recently been recognized as an important reservoir from which person to person transmission occurs. We developed a murine model of S. aureus GI colonization to investigate bacterial factors that promote staphylococcal colonization of the gut. We identified several surface-associated S. aureus antigens that modulate colonization of the GI tract and identified a surface glycopolymer (cell wall teichoic acid) as critical for the early steps in colonization. The failure of the teichoic acid mutant to colonize the GI tract can be attributed to its defects in bacterial adherence and to its enhanced susceptibility to mammalian host defenses unique to the gastrointestinal tract. Efforts to develop antimicrobials that target WTA may lead to an overall reduction in asymptomatic colonization by antibiotic-resistant S. aureus and may impact the incidence of invasive disease.

Vyšlo v časopise: Colonization of the Mouse Gastrointestinal Tract Is Modulated by Wall Teichoic Acid, Capsule, and Surface Proteins. PLoS Pathog 11(7): e32767. doi:10.1371/journal.ppat.1005061
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005061

Souhrn

Zdroje

1. Archer GL (1998) Staphylococcus aureus: A well-armed pathogen. Clin Infect Dis 26: 1179–1181. 9597249

2. Creech CB 2nd, Talbot TR, Schaffner W (2006) Community-associated methicillin-resistant Staphylococcus aureus: the way to the wound is through the nose. J Infect Dis 193: 169–171. 16362879

3. Acton DS, Plat-Sinnige MJ, van Wamel W, de Groot N, van Belkum A (2009) Intestinal carriage of Staphylococcus aureus: how does its frequency compare with that of nasal carriage and what is its clinical impact? Eur J Clin Microbiol Infect Dis 28: 115–127. doi: 10.1007/s10096-008-0602-7 18688664

4. Boyce JM, Havill NL, Maria B (2005) Frequency and possible infection control implications of gastrointestinal colonization with methicillin-resistant Staphylococcus aureus. J Clin Microbiol 43: 5992–5995. 16333087

5. Ray AJ, Pultz NJ, Bhalla A, Aron DC, Donskey CJ (2003) Coexistence of vancomycin-resistant enterococci and Staphylococcus aureus in the intestinal tracts of hospitalized patients. Clin Infect Dis 37: 875–881. 13130397

6. Rimland D, Roberson B (1986) Gastrointestinal carriage of methicillin-resistant Staphylococcus aureus. J Clin Microbiol 24: 137–138. 3722359

7. Bhalla A, Aron DC, Donskey CJ (2007) Staphylococcus aureus intestinal colonization is associated with increased frequency of S. aureus on skin of hospitalized patients. BMC Infect Dis 7: 105. 17848192

8. Squier C, Rihs JD, Risa KJ, Sagnimeni A, Wagener MM, et al. (2002) Staphylococcus aureus rectal carriage and its association with infections in patients in a surgical intensive care unit and a liver transplant unit. Infect Control Hosp Epidemiol 23: 495–501. 12269445

9. Boyce JM, Havill NL, Otter JA, Adams NM (2007) Widespread environmental contamination associated with patients with diarrhea and methicillin-resistant Staphylococcus aureus colonization of the gastrointestinal tract. Infect Control Hosp Epidemiol 28: 1142–1147. 17828690

10. Faden H, Lesse AJ, Trask J, Hill JA, Hess DJ, et al. (2010) Importance of colonization site in the current epidemic of staphylococcal skin abscesses. Pediatrics 125: e618–624. doi: 10.1542/peds.2009-1523 20156893

11. Szumowski JD, Wener KM, Gold HS, Wong M, Venkataraman L, et al. (2009) Methicillin-resistant Staphylococcus aureus colonization, behavioral risk factors, and skin and soft-tissue infection at an ambulatory clinic serving a large population of HIV-infected men who have sex with men. Clin Infect Dis 49: 118–121. doi: 10.1086/599608 19480576

12. Schaffer AC, Solinga RM, Cocchiaro J, Portoles M, Kiser KB, et al. (2006) Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect Immun 74: 2145–2153. 16552044

13. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, et al. (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat Med 10: 243–245. 14758355

14. Wertheim HF, Walsh E, Choudhurry R, Melles DC, Boelens HA, et al. (2008) Key role for clumping factor B in Staphylococcus aureus nasal colonization of humans. PLoS Medicine 5: e17. doi: 10.1371/journal.pmed.0050017 18198942

15. Savage DC, Dubos R, Schaedler RW (1968) The gastrointestinal epithelium and its autochthonous bacterial flora. J Exp Med 127: 67–76. 4169441

16. Saha S, Jing X, Park SY, Wang S, Li X, et al. (2010) Peptidoglycan recognition proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-gamma. Cell Host Microbe 8: 147–162. doi: 10.1016/j.chom.2010.07.005 20709292

17. Kiser KB, Cantey-Kiser JM, Lee JC (1999) Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect Immun 67: 5001–5006. 10496870

18. Weidenmaier C, Kokai-Kun JF, Kulauzovic E, Kohler T, Thumm G, et al. (2008) Differential roles of sortase-anchored surface proteins and wall teichoic acid in Staphylococcus aureus nasal colonization. Int J Med Microbiol 298: 505–513. doi: 10.1016/j.ijmm.2007.11.006 18221914

19. Pierce JV, Kumamoto CA (2012) Variation in Candida albicans EFG1 expression enables host-dependent changes in colonizing fungal populations. MBio 3: e00117–00112. doi: 10.1128/mBio.00117-12 22829676

20. Skurnik D, Roux D, Cattoir V, Danilchanka O, Lu X, et al. (2013) Enhanced in vivo fitness of carbapenem-resistant oprD mutants of Pseudomonas aeruginosa revealed through high-throughput sequencing. Proc Natl Acad Sci U S A 110: 20747–20752. doi: 10.1073/pnas.1221552110 24248354

21. Coyne MJ, Chatzidaki-Livanis M, Paoletti LC, Comstock LE (2008) Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc Natl Acad Sci U S A 105: 13099–13104. doi: 10.1073/pnas.0804220105 18723678

22. Weidenmaier C, McLoughlin RM, Lee JC (2010) The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4+ T-cell-dependent mechanism. PLoS One 5: e13227. doi: 10.1371/journal.pone.0013227 20949105

23. Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, et al. (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191: 1771–1777. 15838806

24. Risley AL, Loughman A, Cywes-Bentley C, Foster TJ, Lee JC (2007) Capsular polysaccharide masks clumping factor A-mediated adherence of Staphylococcus aureus to fibrinogen and platelets. J Infect Dis 196: 919–927. 17703424

25. Pohlmann-Dietze P, Ulrich M, Kiser KB, Doring G, Lee JC, et al. (2000) Adherence of Staphylococcus aureus to endothelial cells: influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect Immun 68: 4865–4871. 10948098

26. Begley M, Gahan CG, Hill C (2005) The interaction between bacteria and bile. FEMS Microbiol Rev 29: 625–651. 16102595

27. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, et al. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76–83. doi: 10.1038/ni.1825 19855381

28. Ghosh D, Porter E, Shen B, Lee SK, Wilk D, et al. (2002) Paneth cell trypsin is the processing enzyme for human defensin-5. Nat Immunol 3: 583–590. 12021776

29. Koprivnjak T, Weidenmaier C, Peschel A, Weiss JP (2008) Wall teichoic acid deficiency in Staphylococcus aureus confers selective resistance to mammalian group IIA phospholipase A(2) and human beta-defensin 3. Infect Immun 76: 2169–2176. doi: 10.1128/IAI.01705-07 18347049

30. Mani N, Tobin P, Jayaswal RK (1993) Isolation and characterization of autolysis-defective mutants of Staphylococcus aureus created by Tn917-lacZ mutagenesis. J Bacteriol 175: 1493–1499. 8095258

31. Atilano ML, Pereira PM, Yates J, Reed P, Veiga H, et al. (2010) Teichoic acids are temporal and spatial regulators of peptidoglycan cross-linking in Staphylococcus aureus. Proc Natl Acad Sci U S A 107: 18991–18996. doi: 10.1073/pnas.1004304107 20944066

32. Kernbauer E, Maurer K, Torres VJ, Shopsin B, Cadwell K (2015) Gastrointestinal dissemination and transmission of Staphylococcus aureus following bacteremia. Infect Immun 83: 372–378. doi: 10.1128/IAI.02272-14 25385792

33. Baur S, Rautenberg M, Faulstich M, Grau T, Severin Y, et al. (2014) A nasal epithelial receptor for Staphylococcus aureus WTA governs adhesion to epithelial cells and modulates nasal colonization. PLoS Pathog 10: e1004089. doi: 10.1371/journal.ppat.1004089 24788600

34. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, et al. (2000) Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113–118. 11248802

35. Schlag M, Biswas R, Krismer B, Kohler T, Zoll S, et al. (2010) Role of staphylococcal wall teichoic acid in targeting the major autolysin Atl. Mol Microbiol 75: 864–873. doi: 10.1111/j.1365-2958.2009.07007.x 20105277

36. Kohler T, Weidenmaier C, Peschel A (2009) Wall teichoic acid protects Staphylococcus aureus against antimicrobial fatty acids from human skin. J Bacteriol 191: 4482–4484. doi: 10.1128/JB.00221-09 19429623

37. Bera A, Biswas R, Herbert S, Kulauzovic E, Weidenmaier C, et al. (2007) Influence of wall teichoic acid on lysozyme resistance in Staphylococcus aureus. J Bacteriol 189: 280–283. 17085565

38. Chung H, Pamp SJ, Hill JA, Surana NK, Edelman SM, et al. (2012) Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149: 1578–1593. doi: 10.1016/j.cell.2012.04.037 22726443

39. Suzuki T, Swoboda JG, Campbell J, Walker S, Gilmore MS (2011) In vitro antimicrobial activity of wall teichoic acid biosynthesis inhibitors against Staphylococcus aureus isolates. Antimicrob Agents Chemother 55: 767–774. doi: 10.1128/AAC.00879-10 21098254

40. Suzuki T, Campbell J, Swoboda JG, Walker S, Gilmore MS (2011) Role of wall teichoic acids in Staphylococcus aureus endophthalmitis. Invest Ophthalmol Vis Sci 52: 3187–3192. doi: 10.1167/iovs.10-6558 21345983

41. Sewell EW, Brown ED (2014) Taking aim at wall teichoic acid synthesis: new biology and new leads for antibiotics. J Antibiot (Tokyo) 67: 43–51.

42. Cramton SE, Gerke C, Schnell NF, Nichols WW, Gotz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67: 5427–5433. 10496925

43. Foster SJ (1995) Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177: 5723–5725. 7559367

44. Mempel M, Schmidt T, Weidinger S, Schnopp C, Foster T, et al. (1998) Role of Staphylococcus aureus surface-associated proteins in the attachment to cultured HaCaT keratinocytes in a new adhesion assay. J Invest Dermatol 111: 452–456. 9740240

45. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, et al. (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197: 1523–1530. doi: 10.1086/587907 18700257

46. Lencer WI, Moe S, Rufo PA, Madara JL (1995) Transcytosis of cholera toxin subunits across model human intestinal epithelia. Proc Natl Acad Sci U S A 92: 10094–10098. 7479732

47. Saslowsky DE, Lencer WI (2008) Conversion of apical plasma membrane sphingomyelin to ceramide attenuates the intoxication of host cells by cholera toxin. Cell Microbiol 10: 67–80. 18052945

48. Bayer AS, Sullam PM, Ramos M, Li C, Cheung AL, et al. (1995) Staphylococcus aureus induces platelet aggregation via a fibrinogen- dependent mechanism which is independent of principal platelet glycoprotein IIb/IIIa fibrinogen-binding domains. Infect Immun 63: 3634–3641. 7642301

49. Shaw LN, Golonka E, Szmyd G, Foster SJ, Travis J, et al. (2005) Cytoplasmic control of premature activation of a secreted protease zymogen: deletion of staphostatin B (SspC) in Staphylococcus aureus 8325–4 yields a profound pleiotropic phenotype. J Bacteriol 187: 1751–1762. 15716447

50. Groicher KH, Firek BA, Fujimoto DF, Bayles KW (2000) The Staphylococcus aureus lrgAB operon modulates murein hydrolase activity and penicillin tolerance. J Bacteriol 182: 1794–1801. 10714982

51. Qoronfleh MW, Wilkinson BJ (1986) Effects of growth of methicillin-resistant and-susceptible Staphylococcus aureus in the presence of beta-lactams on peptidoglycan structure and susceptibility to lytic enzymes. Antimicrob Agents Chemother 29: 250–257. 2872855

52. McDevitt D, Francois P, Vaudaux P, Foster TJ (1994) Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Mol Microbiol 11: 237–248. 8170386

53. Kneidinger B, O'Riordan K, Li J, Brisson JR, Lee JC, et al. (2003) Three highly conserved proteins catalyze the conversion of UDP-N-acetyl-D-glucosamine to precursors for the biosynthesis of O antigen in Pseudomonas aeruginosa O11 and capsule in Staphylococcus aureus type 5. Implications for the UDP-N-acetyl-L-fucosamine biosynthetic pathway. J Biol Chem 278: 3615–3627. 12464616

54. Novick R (1967) Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33: 155–166. 4227577

55. Bramley AJ, Patel AH, O'Reilly M, Foster R, Foster TJ (1989) Roles of alpha-toxin and beta-toxin in virulence of Staphylococcus aureus for the mouse mammary gland. Infect Immun 57: 2489–2494. 2744856

56. Brown S, Xia G, Luhachack LG, Campbell J, Meredith TC, et al. (2012) Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc Natl Acad Sci U S A 109: 18909–18914. doi: 10.1073/pnas.1209126109 23027967

57. Iordanescu S, Surdeanu M (1976) Two restriction and modification systems in Staphylococcus aureus NCTC8325. J Gen Microbiol 96: 277–281.

58. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, et al. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405–8410. 10085071