Antibiotic-driven dysbiosis mediates intraluminal agglutination and alternative segregation of enterococcus faecium from the intestinal epithelium

mBio

Volumn 6, Issue 6, 2015, Pages

  Hendrickx, Antoni P A ^a   Top, Janetta ^a   Bayjanov, Jumamurat R ^a   Kemperman, Hans ^a   Rogers, Malbert R C ^a   Paganelli, Fernanda L ^a   Bonten, Marc J M ^a   Willems, Rob J L ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CEPHALOSPORIN DERIVATIVE; IMMUNOGLOBULIN RECEPTOR; MUCIN 2; RECOMBINANT PROTEIN; SECRETORY IMMUNOGLOBULIN; UVOMORULIN; ANTIINFECTIVE AGENT; CADHERIN; CALCIUM; MUC2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL TRANSMISSION; CELL JUNCTION; COLON MUCOSA; CONTROLLED STUDY; DYSBIOSIS; ENTEROCOCCUS FAECIUM; EXTRACELLULAR MATRIX; FECES MICROFLORA; IN VITRO STUDY; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE WALL; MOUSE; MUCOSAL IMMUNITY; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; STOMACH MUCUS; ANIMAL; ANTIGEN ANTIBODY REACTION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FECES; FEMALE; GROWTH, DEVELOPMENT AND AGING; INTESTINE; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY;

AGGLUTINATION; ANIMALS; ANTI-BACTERIAL AGENTS; CADHERINS; CALCIUM; CEPHALOSPORINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; DYSBIOSIS; ENTEROCOCCUS FAECIUM; FECES; FEMALE; IMMUNOGLOBULIN A, SECRETORY; INTESTINAL MUCOSA; INTESTINES; MICE; MICROBIOTA; MUCIN-2;

EID: 84952845516     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01346-15     Document Type: Article

References (44)

1. Round JL, Mazmanian SK. 2009. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313-323. http://dx.doi.org/10.1038/nri2515.
2. Chu H, Mazmanian SK. 2013. Innate immune recognition of the microbiota promotes host-microbial symbiosis. Nat Immunol 14:668-675. http://dx.doi.org/10.1038/ni.2635.
3. Caballero S, Pamer EG. 2015. Microbiota-mediated inflammation and antimicrobial defense in the intestine. Annu Rev Immunol 33:227-256. http://dx.doi.org/10.1146/annurev-immunol-032713-120238.
4. Buffie CG, Pamer EG. 2013. Microbiota-mediated colonization resistance against intestinal pathogens. Nat Rev Immunol 13:790-801. http:// dx.doi.org/10.1038/nri3535.
5. Vaishnava S, Yamamoto M, Severson KM, Ruhn KA, Yu X, Koren O, Ley R, Wakeland EK, Hooper LV. 2011. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334:255-258. http://dx.doi.org/10.1126/ science.1209791.
6. Cash HL, Whitham CV, Behrendt CL, Hooper LV. 2006. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313: 1126-1130. http://dx.doi.org/10.1126/science.1127119.
7. Mathias A, Pais B, Favre L, Benyacoub J, Corthésy B. 2014. Role of secretory IgA in the mucosal sensing of commensal bacteria. Gut Microbes 5:688-695. http://dx.doi.org/10.4161/19490976.2014.983763.
8. Kaetzel CS. 2014. Cooperativity among secretory IgA, the polymeric immunoglobulin receptor, and the gut microbiota promotes host-microbial mutualism. Immunol Lett 162:10-21. http://dx.doi.org/10.1016/ j.imlet.2014.05.008.
9. Macpherson AJ, McCoy KD, Johansen F, Brandtzaeg P. 2008. The immune geography of IgA induction and function. Mucosal Immunol 1:11-22. http://dx.doi.org/10.1038/mi.2007.6.
10. Gallo RL, Hooper LV. 2012. Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12:503-516. http://dx.doi.org/10.1038/ nri3228.
11. Turner JR. 2009. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9:799-809. http://dx.doi.org/10.1038/nri2653.
12. Rodriguez-Boulan E, Macara IG. 2014. Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 15:225-242. http://dx.doi.org/10.1038/nrm3775.
13. Mehta S, Nijhuis A, Kumagai T, Lindsay J, Silver A. 2015. Defects in the adherens junction complex (E-cadherin/β-catenin) in inflammatory bowel disease. Cell Tissue Res 360:749-760. http://dx.doi.org/10.1007/ s00441-014-1994-6.
14. Ivanov AI, Naydenov NG. 2013. Dynamics and regulation of epithelial adherens junctions: recent discoveries and controversies. Int Rev Cell Mol Biol 303:27-99. http://dx.doi.org/10.1016/B978-0-12-407697-6.00002-7.
15. Johansson MEV, Sjövall H, Hansson GC. 2013. The gastrointestinal mucus system in health and disease. Nat Rev Gastroenterol Hepatol 10: 352-361. http://dx.doi.org/10.1038/nrgastro.2013.35.
16. McGuckin MA, Lindén SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265-278. http://dx.doi.org/ 10.1038/nrmicro2538.
17. Johansson MEV, Phillipson M, Petersson J, Velcich A, Holm L, Hansson GC. 2008. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc Natl Acad Sci U S A 105:15064-15069. http://dx.doi.org/10.1073/pnas.0803124105.
18. Johansson MEV, Larsson JMH, Hansson GC. 2011. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc Natl Acad Sci U S A 108(Suppl 1):4659-4665. http://dx.doi.org/10.1073/pnas.1006451107.
19. Cerutti A, Chen K, Chorny A. 2011. Immunoglobulin responses at the mucosal interface. Annu Rev Immunol 29:273-293. http://dx.doi.org/ 10.1146/annurev-immunol-031210-101317.
20. Sait LC, Galic M, Price JD, Simpfendorfer KR, Diavatopoulos DA, Uren TK, Janssen PH, Wijburg OLC, Strugnell RA. 2007. Secretory antibodies reduce systemic antibody responses against the gastrointestinal commensal flora. Int Immunol 19:257-265. http://dx.doi.org/10.1093/intimm/ dxl142.
21. Johansen F, Pekna M, Norderhaug IN, Haneberg B, Hietala MA, Krajci P, Betsholtz C, Brandtzaeg P. 1999. Absence of epithelial immunoglobulin A transport, with increased mucosal leakiness, in polymeric immu-noglobulin receptor/secretory component-deficient mice. J Exp Med 190: 915-922. http://dx.doi.org/10.1084/jem.190.7.915.
22. Brandtzaeg P. 1973. Two types of IgA immunocytes in man. Nat New Biol 243:142-143. http://dx.doi.org/10.1038/newbio243142a0.
23. Brandtzaeg P. 1974. Presence of J chain in human immunocytes containing various immunoglobulin classes. Nature 252:418-420. http:// dx.doi.org/10.1038/252418a0.
24. Brandtzaeg P, Prydz H. 1984. Direct evidence for an integrated function of J chain and secretory component in epithelial transport of immunoglobulins. Nature 311:71-73. http://dx.doi.org/10.1038/311071a0.
25. Sletten K, Christensen TB, Brandtzaeg P. 1975. Human secretory component-III. Carbohydrates, amino acids and N-terminal sequence. Immunochemistry 12:783-785. http://dx.doi.org/10.1016/0019-2791(75)90230-X.
26. Brandtzaeg P, Fjellanger I, Gjeruldsen ST. 1970. Human secretory immunoglobulins. I. Salivary secretions from individuals with normal or low levels of serum immunoglobulins. Scand J Haematol Suppl 12:3-83.
27. Brandtzaeg P, Kiyono H, Pabst R, Russell MW. 2008. Terminology: nomenclature of mucosa-associated lymphoid tissue. Mucosal Immunol 1:31-37. http://dx.doi.org/10.1038/mi.2007.9.
28. Corthésy B. 2010. Role of secretory immunoglobulin A and secretory component in the protection of mucosal surfaces. Future Microbiol 5:817-829. http://dx.doi.org/10.2217/fmb.10.39.
29. Hendrickx AP, van Schaik W, Willems RJ. 2013. The cell wall architecture of Enterococcus faecium: from resistance to pathogenesis. Future Microbiol 8:993-1010. http://dx.doi.org/10.2217/fmb.13.66.
30. Ruiz-Garbajosa P, de Regt M, Bonten M, Baquero F, Coque TM, Cantón R, Harmsen HJ, Willems RJL. 2012. High-density fecal Enterococcus faecium colonization in hospitalized patients is associated with the presence of the polyclonal subcluster CC17. Eur J Clin Microbiol Infect Dis 31:519-522. http://dx.doi.org/10.1007/s10096-011-1342-7.
31. Ubeda C, Taur Y, Jenq RR, Equinda MJ, Son T, Samstein M, Viale A, Socci ND, van den Brink MRM, Kamboj M, Pamer EG. 2010. Vancomycin-resistant enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. J Clin Invest 120:4332-4341. http://dx.doi.org/ 10.1172/JCI43918.
32. Brandl K, Plitas G, Mihu CN, Ubeda C, Jia T, Fleisher M, Schnabl B, DeMatteo RP, Pamer EG. 2008. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 455:804-807. http://dx.doi.org/10.1038/nature07250.
33. Keeney KM, Yurist-Doutsch S, Arrieta M, Finlay BB. 2014. Effects of antibiotics on human microbiota and subsequent disease. Annu Rev Microbiol 68:217-235. http://dx.doi.org/10.1146/annurev-micro-091313-103456.
34. Stecher B, Maier L, HardtW. 2013. "Blooming" in the gut: how dysbiosis might contribute to pathogen evolution. Nat Rev Microbiol 11:277-284. http://dx.doi.org/10.1038/nrmicro2989.
35. Britton RA, Young VB. 2014. Role of the intestinal microbiota in resistance to colonization by Clostridium difficile. Gastroenterology 146: 1547-1553. http://dx.doi.org/10.1053/j.gastro.2014.01.059.
36. Wlodarska M, Willing B, Keeney KM, Menendez A, Bergstrom KS, Gill N, Russell SL, Vallance BA, Finlay BB. 2011. Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis. Infect Immun 79:1536-1545. http:// dx.doi.org/10.1128/IAI.01104-10.
37. Brandtzaeg P. 2013. Secretory IgA: designed for anti-microbial defense. Front Immunol 4:222. http://dx.doi.org/10.3389/fimmu.2013.00222.
38. Ito K, Okamoto I, Araki N, Kawano Y, Nakao M, Fujiyama S, Tomita K, Mimori T, Saya H. 1999. Calcium influx triggers the sequential proteolysis of extracellular and cytoplasmic domains of E-cadherin, leading to loss of beta-catenin from cell-cell contacts. Oncogene 18:7080-7090. http://dx.doi.org/10.1038/sj.onc.1203191.
39. van der Heijden KM, van der Heijden IM, Galvao FH, Lopes CG, Costa SF, Abdala E, D'Albuquerque LA, Levin AS. 2014. Intestinal translocation of clinical isolates of vancomycin-resistant Enterococcus faecalis and ESBL-producing Escherichia coli in a rat model of bacterial colonization and liver ischemia/reperfusion injury. PLoS One 9:e108453. http:// dx.doi.org/10.1371/journal.pone.0108453.
40. Rigottier-Gois L, Madec C, Navickas A, Matos RC, Akary-Lepage E, Mistou M, Serror P. 2015. The surface rhamnopolysaccharide Epa of Enterococcus faecalis is a key determinant of intestinal colonization. J Infect Dis 211:62-71. http://dx.doi.org/10.1093/infdis/jiu402.
41. Steck N, Hoffmann M, Sava IG, Kim SC, Hahne H, Tonkonogy SL, Mair K, Krueger D, Pruteanu M, Shanahan F, Vogelmann R, Schemann M, Kuster B, Sartor RB, Haller D. 2011. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology 141:959-971. http://dx.doi.org/10.1053/ j.gastro.2011.05.035.
42. Repetto O, De Paoli P, De Re V, Canzonieri V, Cannizzaro R. 2014. Levels of soluble E-cadherin in breast, gastric, and colorectal cancers. Biomed Res Int 2014:408047. http://dx.doi.org/10.1155/2014/408047.
43. De Wever O, Derycke L, Hendrix A, De Meerleer G, Godeau F, Depypere H, Bracke M. 2007. Soluble cadherins as cancer biomarkers. Clin Exp Metastasis 24:685-697. http://dx.doi.org/10.1007/s10585-007-9104-8.
44. Jump RLP, Polinkovsky A, Hurless K, Sitzlar B, Eckart K, Tomas M, Deshpande A, Nerandzic MM, Donskey CJ. 2014. Metabolomics analysis identifies intestinal microbiota-derived biomarkers of colonization resistance in clindamycin-treated mice. PLoS One 9:e101267. http:// dx.doi.org/10.1371/journal.pone.0101267.