Intestinal microbiota shifts towards elevated commensal escherichia coli loads abrogate colonization resistance against campylobacter jejuni in mice

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Haag, Lea Maxie ^a   Fischer, André ^a   Otto, Bettina ^a   Plickert, Rita ^a   Kühl, Anja A ^a   Göbel, Ulf B ^a   Bereswill, Stefan ^a   Heimesaat, Markus M ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; INTERLEUKIN 10;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BLOOD; CAMPYLOBACTER ENTERITIS; CAMPYLOBACTER JEJUNI; CAMPYLOBACTERIOSIS; COLITIS; COMMENSAL ESCHERICHIA COLI; CONTROLLED STUDY; ENTEROCOLITIS; FEMALE; ILEITIS; IMMUNE RESPONSE; INTESTINE FLORA; KIDNEY; LIVER; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; SPLEEN; TOXOPLASMA GONDII; ANIMAL; BACTERIAL TRANSLOCATION; C57BL MOUSE; COLON; ESCHERICHIA COLI; FECES; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INTESTINE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; MOUSE STRAIN; PHYSIOLOGY; TIME; TOXOPLASMOSIS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; MURINAE; MUS; TOXOPLASMA GONDII;

ANIMALS; BACTERIAL TRANSLOCATION; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; COLITIS; COLON; ESCHERICHIA COLI; FECES; HOST-PATHOGEN INTERACTIONS; HUMANS; ILEITIS; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; INTERLEUKIN-10; INTESTINES; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; TIME FACTORS; TOXOPLASMOSIS, ANIMAL; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84860437657     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035988     Document Type: Article

References (50)

1. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, et al. (2012) Poultry as a Host for the Zoonotic Pathogen Campylobacter jejuni. Vector Borne Zoonotic Dis 12: 89-98.
2. Man SM, (2011) The clinical importance of emerging Campylobacter species. Nat Rev Gastroenterol Hepatol 8: 669-685.
3. Lane JA, Mehra RK, Carrington SD, Hickey RM, (2010) The food glycome: a source of protection against pathogen colonization in the gastrointestinal tract. Int J Food Microbiol 142: 1-13.
4. Guerry P, Szymanski CM, (2008) Campylobacter sugars sticking out. Trends Microbiol 16: 428-435.
5. Young KT, Davis LM, Dirita VJ, (2007) Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 5: 665-679.
6. Kist M, Bereswill S, (2001) Campylobacter jejuni. Contrib Microbiol 8: 150-165.
7. van Spreeuwel JP, Duursma GC, Meijer CJ, Bax R, Rosekrans PC, et al. (1985) Campylobacter colitis: histological immunohistochemical and ultrastructural findings. Gut 26: 945-951.
8. Walker RI, Caldwell MB, Lee EC, Guerry P, Trust TJ, et al. (1986) Pathophysiology of Campylobacter enteritis. Microbiol Rev 50: 81-94.
9. Ketley JM, (1997) Pathogenesis of enteric infection by Campylobacter. Microbiology 143 (Pt 1): 5-21.
10. Allos BM, (1997) Association between Campylobacter infection and Guillain-Barre syndrome. J Infect Dis 176 (Suppl 2): S125-128.
11. Butzler JP, (2004) Campylobacter, from obscurity to celebrity. Clin Microbiol Infect 10: 868-876.
12. Dorrell N, Wren BW, (2007) The second century of Campylobacter research: recent advances, new opportunities and old problems. Curr Opin Infect Dis 20: 514-518.
13. Dasti JI, Tareen AM, Lugert R, Zautner AE, Gross U, (2010) Campylobacter jejuni: a brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int J Med Microbiol 300: 205-211.
14. Yrios JW, Balish E, (1986) Immune response of athymic and euthymic germfree mice to Campylobacter spp. Infect Immun 54: 339-346.
15. Yrios JW, Balish E, (1986) Colonization and infection of athymic and euthymic germfree mice by Campylobacter jejuni and Campylobacter fetus subsp. fetus. Infect Immun 53: 378-383.
16. Yrios JW, Balish E, (1986) Pathogenesis of Campylobacter spp. in athymic and euthymic germfree mice. Infect Immun 53: 384-392.
17. Bereswill S, Fischer A, Plickert R, Haag LM, Otto B, et al. (2011) Novel Murine Infection Models Provide Deep Insights into the "Menage a Trois" of Campylobacter jejuni, Microbiota and Host Innate Immunity. PLoS One 6: e20953.
18. Bereswill S, Plickert R, Fischer A, Kühl AA, Loddenkemper C, et al. (2011) What you eat is what you get: Novel Campylobacter models in the quadrangle relationship between nutrition, obesity, microbiota and susceptibiliy to infection. Eur J Microbiol Immunol 1: 237-248.
19. Stecher B, Hardt WD, (2011) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 14: 82-91.
20. Stecher B, Robbiani R, Walker AW, Westendorf AM, Barthel M, et al. (2007) Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5: 2177-2189.
21. Stecher B, Chaffron S, Kappeli R, Hapfelmeier S, Freedrich S, et al. (2010) Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6: e1000711.
22. Heimesaat MM, Bereswill S, Fischer A, Fuchs D, Struck D, et al. (2006) Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J Immunol 177: 8785-8795.
23. Heimesaat MM, Fischer A, Jahn HK, Niebergall J, Freudenberg M, et al. (2007) Exacerbation of murine ileitis by Toll-like receptor 4 mediated sensing of lipopolysaccharide from commensal Escherichia coli. Gut 56: 941-948.
24. Heimesaat MM, Fischer A, Siegmund B, Kupz A, Niebergall J, et al. (2007) Shift towards pro-inflammatory intestinal bacteria aggravates acute murine colitis via Toll-like receptors 2 and 4. PLoS One 2: e662.
25. Erridge C, Duncan SH, Bereswill S, Heimesaat MM, (2010) The induction of colitis and ileitis in mice is associated with marked increases in intestinal concentrations of stimulants of TLRs 2, 4, and 5. PLoS One 5: e9125.
26. Kalischuk LD, Buret AG, (2010) A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am J Physiol Gastrointest Liver Physiol 298: G1-9.
27. Jess T, Simonsen J, Nielsen NM, Jorgensen KT, Bager P, et al. (2011) Enteric Salmonella or Campylobacter infections and the risk of inflammatory bowel disease. Gut 60: 318-324.
28. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, et al. (2002) Mucosal flora in inflammatory bowel disease. Gastroenterology 122: 44-54.
29. Swidsinski A, Weber J, Loening-Baucke V, Hale LP, Lochs H, (2005) Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol 43: 3380-3389.
30. Man SM, Kaakoush NO, Mitchell HM, (2011) The role of bacteria and pattern-recognition receptors in Crohn's disease. Nat Rev Gastroenterol Hepatol 8: 152-168.
31. Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B, et al. (2009) Increased short- and long-term risk of inflammatory bowel disease after salmonella or campylobacter gastroenteritis. Gastroenterology 137: 495-501.
32. Helms M, Simonsen J, Molbak K, (2006) Foodborne bacterial infection and hospitalization: a registry-based study. Clin Infect Dis 42: 498-506.
33. Garcia Rodriguez LA, Ruigomez A, Panes J, (2006) Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 130: 1588-1594.
34. Wohlgemuth S, Keller S, Kertscher R, Stadion M, Haller D, et al. (2011) Intestinal steroid profiles and microbiota composition in colitic mice. Gut Microbes 2: 159-166.
35. Diker KS, Hascelik G, Diker S, (1992) Colonization of infant mice with flagellar variants of Campylobacter jejuni. Acta Microbiol Hung 39: 133-136.
36. Hanninen ML, (1989) Effect of endotoxin on colonisation of Campylobacter jejuni in infant mice. J Med Microbiol 30: 199-206.
37. Hanninen ML, (1990) Bismuth subsalicylate in the prevention of colonization of infant mice with Campylobacter jejuni. Epidemiol Infect 104: 397-404.
38. Abimiku AG, Dolby JM, (1987) The mechanism of protection of infant mice from intestinal colonisation with Campylobacter jejuni. J Med Microbiol 23: 339-344.
39. Field LH, Headley VL, Payne SM, Berry LJ, (1986) Influence of iron on growth, morphology, outer membrane protein composition, and synthesis of siderophores in Campylobacter jejuni. Infect Immun 54: 126-132.
40. Haag LM, Fischer A, Otto B, Grundmann U, Kühl AA, et al. (2012) Campylobacter jejuni infection of infant mice: acute enterocolitis is followed by asymptomatic intestinal and extra-intestinal immune response. Eur J Microbiol Immunol 2: 2-11.
41. Mansfield LS, Bell JA, Wilson DL, Murphy AJ, Elsheikha HM, et al. (2007) C57BL/6 and congenic interleukin-10-deficient mice can serve as models of Campylobacter jejuni colonization and enteritis. Infect Immun 75: 1099-1115.
42. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, et al. (2007) Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2: 204.
43. Man SM, Zhang L, Day AS, Leach ST, Lemberg DA, et al. (2010) Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn's disease. Inflamm Bowel Dis 16: 1008-1016.
44. Mahendran V, Riordan SM, Grimm MC, Tran TA, Major J, et al. (2011) Prevalence of Campylobacter species in adult Crohn's disease and the preferential colonization sites of Campylobacter species in the human intestine. PLoS One 6: e25417.
45. Marshall JK, Thabane M, Garg AX, Clark WF, Salvadori M, et al. (2006) Incidence and epidemiology of irritable bowel syndrome after a large waterborne outbreak of bacterial dysentery. Gastroenterology 131: 445-450.
46. Field LH, Underwood JL, Pope LM, Berry LJ, (1981) Intestinal colonization of neonatal animals by Campylobacter fetus subsp. jejuni. Infect Immun 33: 884-892.
47. Siegmund B, Fantuzzi G, Rieder F, Gamboni-Robertson F, Lehr HA, et al. (2001) Neutralization of interleukin-18 reduces severity in murine colitis and intestinal IFN-gamma and TNF-alpha production. Am J Physiol Regul Integr Comp Physiol 281: R1264-1273.
48. Bereswill S, Munoz M, Fischer A, Plickert R, Haag LM, et al. (2010) Anti-inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation. PLoS One 5: e15099.
49. Munoz M, Heimesaat MM, Danker K, Struck D, Lohmann U, et al. (2009) Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J Exp Med 206: 3047-3059.
50. Heimesaat MM, Nogai A, Bereswill S, Plickert R, Fischer A, et al. (2010) MyD88/TLR9 mediated immunopathology and gut microbiota dynamics in a novel murine model of intestinal graft-versus-host disease. Gut 59: 1079-1087.