Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans

Journal of Clinical Investigation

Volumn 120, Issue 12, 2010, Pages 4332-4341

  Ubeda, Carles ^a   Taur, Ying ^a   Jenq, Robert R ^a   Equinda, Michele J ^a   Son, Tammy ^a   Samstein, Miriam ^a   Viale, Agnes ^a   Socci, Nicholas D ^a   Van Den Brink, Marcel R M ^a   Kamboj, Mini ^a   Pamer, Eric G ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; DNA 16S; METRONIDAZOLE; NEOMYCIN; VANCOMYCIN;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ARTICLE; BACTEREMIA; BACTERIAL COLONIZATION; BLOODSTREAM INFECTION; CECUM; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; ILEUM; INTESTINE FLORA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYROSEQUENCING; VANCOMYCIN RESISTANT ENTEROCOCCUS;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTEREMIA; BASE SEQUENCE; CROSS INFECTION; DNA, BACTERIAL; DNA, RIBOSOMAL; ENTEROCOCCUS; GRAM-POSITIVE BACTERIAL INFECTIONS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; INTESTINES; METAGENOME; MICE; MICE, INBRED C57BL; VANCOMYCIN RESISTANCE;

EID: 78649895980     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI43918     Document Type: Article

References (50)

1. Donskey CJ. Antibiotic regimens and intestinal colonization with antibiotic-resistant gram-negative bacilli. Clin Infect Dis. 2006;43(suppl 2):S62-S69.
2. Rice LB. Antimicrobial resistance in gram-positive bacteria. Am J Med. 2006;119(6 suppl 1):S11-S19.
3. Bartlett JG. Narrative review: the new epidemic of Clostridium difficile-associated enteric disease. Ann Intern Med. 2006;145(10):758-764.
4. Eckburg PB, et al. Diversity of the human intestinal microbial flora. Science. 2005;308(5728):1635-1638.
5. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI. Host-bacterial mutualism in the human intestine. Science. 2005;307(5717):1915-1920.
6. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006;124(4):837-848.
7. Versalovic J, Relman D. How bacterial communities expand functional repertoires. PLoS Biol. 2006;4(12):e430.
8. Dethlefsen L, Huse S, Sogin ML, Relman DA. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6(11):e280.
9. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444(7122):1022-1023. (Pubitemid 46018512)
10. Hooper LV, Midtvedt T, Gordon JI. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr. 2002;22:283-307.
11. Backhed F, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004;101(44):15718-15723.
12. Stappenbeck TS, Hooper LV, Gordon JI. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc Natl Acad Sci U S A. 2002;99(24):15451-15455.
13. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004;118(2):229-241.
14. Cebra JJ. Influences of microbiota on intestinal immune system development. Am J Clin Nutr. 1999;69(5):1046S-1051S.
15. Vollaard EJ, Clasener HA. Colonization resistance. Antimicrob Agents Chemother. 1994;38(3):409-414.
16. Pamer EG. Immune responses to commensal and environmental microbes. Nat Immunol. 2007;8(11):1173-1178. (Pubitemid 350011753)
17. Brandl K, et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature. 2008;455(7214):804-807.
18. Abreu MT, Thomas LS, Arnold ET, Lukasek K, Michelsen KS, Arditi M. TLR signaling at the intestinal epithelial interface. J Endotoxin Res. 2003;9(5):322-330.
19. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol. 2001;167(4):1882-1885.
20. Kobayashi KS, et al. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science. 2005;307(5710):731-734.
21. Rakoff-Nahoum S, Medzhitov R. Role of the innate immune system and host-commensal mutualism. Curr Top Microbiol Immunol. 2006;308:1-18. (Pubitemid 47400295)
22. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal alpha-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol. 2000;1(2):113-118.
23. Vora P, et al. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol. 2004;173(9):5398-5405.
24. Cash HL, Whitham CV, Behrendt CL, Hooper LV. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science. 2006;313(5790):1126- 1130.
25. Brandl K, Plitas G, Schnabl B, Dematteo RP, Pamer EG. MyD88-mediated signals induce the bactericidal lectin RegIII{gamma} and protect mice against intestinal Listeria monocytogenes infection. J Exp Med. 2007;204(8):1891-1900.
26. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A. 2008;105(52):20858-20863.
27. Kinnebrew MA, Ubeda C, Zenewicz LA, Smith N, Flavell RA, Pamer EG. Bacterial flagellin stimulates Toll-like receptor 5-dependent defense against vancomycin-resistant Enterococcus infection. J Infect Dis. 2010;201(4):534-543.
28. Sekirov I, et al. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun. 2008;76(10):4726-4736.
29. Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, Young VB. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect Immun. 2009;77(6):2367-2375.
30. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun. 2009;77(7):2741-2753.
31. Garner CD, et al. Perturbation of the small intestine microbial ecology by streptomycin alters pathology in a Salmonella enterica serovar typhimurium murine model of infection. Infect Immun. 2009;77(7):2691-2702.
32. Lawley TD, et al. Antibiotic treatment of clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun. 2009;77(9):3661-3669.
33. Hill DA, et al. Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunol. 2010;3(2):148-158.
34. Donskey CJ, Hanrahan JA, Hutton RA, Rice LB. Effect of parenteral antibiotic administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract. J Infect Dis. 1999;180(2):384-390.
35. Lozupone C, Hamady M, Knight R. UniFrac - an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics. 2006;7:371.
36. Weinstock DM, et al. Colonization, bloodstream infection, and mortality caused by vancomycin-resistant enterococcus early after allogeneic hematopoietic stem cell transplant. Biol Blood Marrow Transplant. 2007;13(5):615-621.
37. Zirakzadeh A, Gastineau DA, Mandrekar JN, Burke JP, Johnston PB, Patel R. Vancomycin-resistant enterococcal colonization appears associated with increased mortality among allogeneic hematopoietic stem cell transplant recipients. Bone Marrow Transplant. 2008;41(4):385-392. (Pubitemid 351330734)
38. Sonnenburg JL, Chen CT, Gordon JI. Genomic and metabolic studies of the impact of probiotics on a model gut symbiont and host. PLoS Biol. 2006;4(12):e413.
39. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature. 2008;453(7195):620-625.
40. van Baarlen P, et al. Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A. 2009;106(7):2371-2376.
41. Stecher B, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007;5(10):2177-2189.
42. Kingsley RA, van Amsterdam K, Kramer N, Baumler AJ. The shdA gene is restricted to serotypes of Salmonella enterica subspecies I and contributes to efficient and prolonged fecal shedding. Infect Immun. 2000;68(5):2720-2727.
43. Turnbaugh PJ, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457(7228):480-484.
44. Bik EM, et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci U S A. 2006;103(3):732-737.
45. Schloss PD, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75(23):7537-7541.
46. Pruesse E, et al. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007;35(21):7188-7196.
47. Sogin ML, et al. Microbial diversity in the deep sea and the underexplored "rare biosphere". Proc Natl Acad Sci U S A. 2006;103(32):12115-12120.
48. Wang Q, Garrity GM, Tiedje JM, Cole JR. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261-5267.
49. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 2009;26(7):1641-1650.
50. Robinson MD, Smyth GK. Moderated statistical tests for assessing differences in tag abundance. Bioinformatics. 2007;23(21):2881-2887.