Helicobacter pylori induced gastric immunopathology is associated with distinct microbiota changes in the large intestines of long-term infected Mongolian gerbils

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Heimesaat, Markus M ^a   Fischer, André ^a   Plickert, Rita ^a   Wiedemann, Tobias ^b   Loddenkemper, Christoph ^a   Göbel, Ulf B ^a   Bereswill, Stefan ^a   Rieder, Gabriele ^c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c UNIVERSITY OF SALZBURG   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

AKKERMANSIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM MUTANT; BACTEROIDES; BIODEGRADATION; CECUM; CONTROLLED STUDY; DISEASE SEVERITY; ENTEROCOCCUS; ESCHERICHIA COLI; FEMALE; GASTRITIS; GERBIL; HELICOBACTER INFECTION; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOPATHOLOGY; INTESTINE FLORA; LARGE INTESTINE; MALIGNANT TRANSFORMATION; MOLECULAR GENETICS; MUCUS; NONHUMAN; PRECANCER; PREVOTELLA; STOMACH ATROPHY; STOMACH DISEASE; TYPE IV SECRETION SYSTEM; ACHLORHYDRIA; ANIMAL; BACTERIAL SECRETION SYSTEM; CHLAMYDIACEAE; COMPLICATION; HELICOBACTER PYLORI; IMMUNOLOGY; INNATE IMMUNITY; MICROBIOLOGY; MICROFLORA; PATHOGENICITY; PATHOLOGY; STOMACH;

ACHLORHYDRIA; ANIMALS; BACTERIAL SECRETION SYSTEMS; BACTEROIDES; CHLAMYDIACEAE; ESCHERICHIA COLI; FEMALE; GERBILLINAE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; IMMUNITY, INNATE; INTESTINE, LARGE; MICROBIOTA; PREVOTELLA; STOMACH;

EID: 84903397390     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100362     Document Type: Article

References (39)

1. Dooley CP, Cohen H, Fitzgibbons PL, Bauer M, Appleman MD, et al. (1989) Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons. N Engl J Med 321: 1562-1566. (Pubitemid 20008234)
2. Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G, et al. (1995) Long-term sequelae of Helicobacter pylori gastritis. Lancet 345: 1525-1528.
3. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347: 1175-1186.
4. International Agency for Research on Cancer (1994) Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr Eval Carcinog Risks Hum 61: 1-241.
5. Wessler S, Backert S (2008) Molecular mechanisms of epithelial-barrier disruption by Helicobacter pylori. Trends Microbiol 16: 397-405.
6. Poppe M, Feller SM, Romer G, Wessler S (2007) Phosphorylation of Helicobacter pylori CagA by c-Abl leads to cell motility. Oncogene 26: 3462-3472. (Pubitemid 46816757)
7. Sewald X, Gebert-Vogl B, Prassl S, Barwig I, Weiss E, et al. (2008) Integrin subunit CD18 Is the T-lymphocyte receptor for the Helicobacter pylori vacuolating cytotoxin. Cell Host Microbe 3: 20-29.
8. Hatakeyama M (2006) The role of Helicobacter pylori CagA in gastric carcinogenesis. Int J Hematol 84: 301-308.
9. Wiedemann T, Loell E, Mueller S, Stoeckelhuber M, Stolte M, et al. (2009) Helicobacter pylori cag-Pathogenicity island-dependent early immunological response triggers later precancerous gastric changes in Mongolian gerbils. PLoS One 4: e4754.
10. Rieder G, Merchant JL, Haas R (2005) Helicobacter pylori cag-type IV secretion system facilitates corpus colonization to induce precancerous conditions in Mongolian gerbils. Gastroenterology 128: 1229-1242. (Pubitemid 40712175)
11. Hirayama F, Takagi S, Yokoyama Y, Iwao E, Ikeda Y (1996) Establishment of gastric Helicobacter pylori infection in Mongolian gerbils. J Gastroenterol 31 Suppl 9: 24-28. (Pubitemid 27026292)
12. Hirayama F, Takagi S, Kusuhara H, Iwao E, Yokoyama Y, et al. (1996) Induction of gastric ulcer and intestinal metaplasia in mongolian gerbils infected with Helicobacter pylori . J Gastroenterol 31: 755-757. (Pubitemid 26345549)
13. Tsukamoto T, Toyoda T, Mizoshita T, Tatematsu M (2013) Helicobacter pylori infection and gastric carcinogenesis in rodent models. Semin Immunopathol 35: 177-190.
14. Zhang S, Moss SF (2012) Rodent models of Helicobacter infection, inflammation, and disease. Methods Mol Biol 921: 89-98.
15. Aebischer T, Fischer A, Walduck A, Schlotelburg C, Lindig M, et al. (2006) Vaccination prevents Helicobacter pylori-induced alterations of the gastric flora in mice. FEMS Immunol Med Microbiol 46: 221-229.
16. Yin YN, Wang CL, Liu XW, Cui Y, Xie N, et al. (2011) Gastric and duodenum microflora analysis after long-term Helicobacter pylori infection in Mongolian Gerbils. Helicobacter 16: 389-397.
17. Osaki T, Matsuki T, Asahara T, Zaman C, Hanawa T, et al. (2012) Comparative analysis of gastric bacterial microbiota in Mongolian gerbils after long-term infection with Helicobacter pylori . Microb Pathog 53: 12-18.
18. Zaman C, Osaki T, Hanawa T, Yonezawa H, Kurata S, et al. (2010) Analysis of the microflora in the stomach of Mongolian gerbils infected with Helicobacter pylori. J Gastroenterol Hepatol 25 Suppl 1: S11-14.
19. Haag LM, Fischer A, Otto B, Plickert R, Kuhl AA, et al. (2012) Intestinal microbiota shifts towards elevated commensal Escherichia coli loads abrogate colonization resistance against Campylobacter jejuni in mice. PLoS One 7: e35988.
20. 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. (Pubitemid 44893845)
21. 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. (Pubitemid 46999077)
22. 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.
23. 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.
24. Saha A, Hammond CE, Beeson C, Peek RM, Jr., Smolka AJ (2010) Helicobacter pylori represses proton pump expression and inhibits acid secretion in human gastric mucosa. Gut 59: 874-881.
25. Saha A, Backert S, Hammond CE, Gooz M, Smolka AJ (2010) Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase alpha subunit. Gastroenterology 139: 239-248.
26. Smolka AJ, Backert S (2012) How Helicobacter pylori infection controls gastric acid secretion. J Gastroenterol 47: 609-618.
27. Gaddy JA, Radin JN, Loh JT, Zhang F, Washington MK, et al. (2013) High dietary salt intake exacerbates Helicobacter pylori-induced gastric carcinogenesis. Infect Immun 81: 2258-2267.
28. Sun YQ, Monstein HJ, Nilsson LE, Petersson F, Borch K (2003) Profiling and identification of eubacteria in the stomach of Mongolian gerbils with and without Helicobacter pylori infection. Helicobacter 8: 149-157. (Pubitemid 36522919)
29. Jiang W, Ghosh SK, Flyckt R, Kalinowska M, Starks D, et al. (2012) Bacterial colonization and beta defensins in the female genital tract in HIV infection. Curr HIV Res 10: 504-512.
30. Valeur N, Engel P, Carbajal N, Connolly E, Ladefoged K (2004) Colonization and immunomodulation by Lactobacillus reuteri ATCC 55730 in the human gastrointestinal tract. Appl Environ Microbiol 70: 1176-1181. (Pubitemid 38568246)
31. Derrien M, Vaughan EE, Plugge CM, de Vos WM (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54: 1469-1476. (Pubitemid 39359958)
32. Selgrad M, Bornschein J, Rokkas T, Malfertheiner P (2012) Helicobacter pylori: gastric cancer and extragastric intestinal malignancies. Helicobacter 17 Suppl 1: 30-35.
33. Chu S, Schubert ML (2013) Gastric secretion. Curr Opin Gastroenterol 29: 636-641.
34. Huseby ES, White J, Crawford F, Vass T, Becker D, et al. (2005) How the T cell repertoire becomes peptide and MHC specific. Cell 122: 247-260. (Pubitemid 41032988)
35. Yakoob J, Abbas Z, Naz S, Islam M, Jafri W (2012) Virulence markers of Helicobacter pylori in patients with diarrhoea-dominant irritable bowel syndrome. Br J Biomed Sci 69: 6-10.
36. Farnbacher M, Jahns T, Willrodt D, Daniel R, Haas R, et al. (2010) Sequencing, annotation, and comparative genome analysis of the gerbil-adapted Helicobacter pylori strain B8. BMC Genomics 11: 335.
37. Kavermann H, Burns BP, Angermuller K, Odenbreit S, Fischer W, et al. (2003) Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J Exp Med 197: 813-822. (Pubitemid 36437859)
38. 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.
39. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73: 127-141. (Pubitemid 28209906)