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Infect Immun. Sep 1995; 63(9): 3722–3725.
PMCID: PMC173518

Inability of an isogenic urease-negative mutant stain of Helicobacter mustelae to colonize the ferret stomach.

Abstract

Eight ferrets specific-pathogen-free for Helicobacter mustelae were given, per dose, approximately 3.0 x 10(7) CFU of either the wild-type parent strain of H. mustelae (NCTC 12032) (two ferrets) the isogenic urease-negative mutant strain of H. mustelae (10::Tn3Km) (four ferrets), or sterile culture broth (two ferrets). Infection status was monitored by endoscopic gastric biopsy for urease activity, histopathology, and culture and by serology at 3, 6, 10, and 21 weeks. All ferrets were necropsied at 25 weeks. Both negative control ferrets remained uninfected, both ferrets receiving the H. mustelae wild-type parent strain became infected after two doses of the organism, and all four ferrets given two doses of the isogenic urease-negative mutant strain of H. mustelae remained uninfected throughout the 6-month study. Histopathology correlated with infection status. H. mustelae-infected ferrets exhibited diffuse mononuclear inflammation in the subglandular region and the lamina propria of the gastric mucosa, while uninfected ferrets showed no or minimal inflammation. These results suggest that urease activity is essential for colonization of the ferret stomach by H. mustelae.

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Selected References

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  • Blaser MJ. Epidemiology and pathophysiology of Campylobacter pylori infections. Rev Infect Dis. 1990 Jan-Feb;12 (Suppl 1):S99–106. [PubMed]
  • Blaser MJ. Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation. Gastroenterology. 1992 Feb;102(2):720–727. [PubMed]
  • Chen XG, Correa P, Offerhaus J, Rodriguez E, Janney F, Hoffmann E, Fox J, Hunter F, Diavolitsis S. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am J Clin Pathol. 1986 Nov;86(5):575–582. [PubMed]
  • Correa P. Human gastric carcinogenesis: a multistep and multifactorial process--First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 1992 Dec 15;52(24):6735–6740. [PubMed]
  • Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, Massone A, Papini E, Xiang Z, Figura N, et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5791–5795. [PMC free article] [PubMed]
  • Cover TL, Blaser MJ. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem. 1992 May 25;267(15):10570–10575. [PubMed]
  • Crabtree JE, Figura N, Taylor JD, Bugnoli M, Armellini D, Tompkins DS. Expression of 120 kilodalton protein and cytotoxicity in Helicobacter pylori. J Clin Pathol. 1992 Aug;45(8):733–734. [PMC free article] [PubMed]
  • Crabtree JE, Taylor JD, Wyatt JI, Heatley RV, Shallcross TM, Tompkins DS, Rathbone BJ. Mucosal IgA recognition of Helicobacter pylori 120 kDa protein, peptic ulceration, and gastric pathology. Lancet. 1991 Aug 10;338(8763):332–335. [PubMed]
  • Doig P, Austin JW, Kostrzynska M, Trust TJ. Production of a conserved adhesin by the human gastroduodenal pathogen Helicobacter pylori. J Bacteriol. 1992 Apr;174(8):2539–2547. [PMC free article] [PubMed]
  • Dunn BE, Sung CC, Taylor NS, Fox JG. Purification and characterization of Helicobacter mustelae urease. Infect Immun. 1991 Sep;59(9):3343–3345. [PMC free article] [PubMed]
  • Eaton KA, Brooks CL, Morgan DR, Krakowka S. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect Immun. 1991 Jul;59(7):2470–2475. [PMC free article] [PubMed]
  • Eaton KA, Krakowka S. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect Immun. 1994 Sep;62(9):3604–3607. [PMC free article] [PubMed]
  • Eaton KA, Morgan DR, Krakowka S. Campylobacter pylori virulence factors in gnotobiotic piglets. Infect Immun. 1989 Apr;57(4):1119–1125. [PMC free article] [PubMed]
  • Evans DG, Evans DJ, Jr, Moulds JJ, Graham DY. N-acetylneuraminyllactose-binding fibrillar hemagglutinin of Campylobacter pylori: a putative colonization factor antigen. Infect Immun. 1988 Nov;56(11):2896–2906. [PMC free article] [PubMed]
  • Ferrero RL, Cussac V, Courcoux P, Labigne A. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol. 1992 Jul;174(13):4212–4217. [PMC free article] [PubMed]
  • Ferrero RL, Hazell SL, Lee A. The urease enzymes of Campylobacter pylori and a related bacterium. J Med Microbiol. 1988 Sep;27(1):33–40. [PubMed]
  • Figura N, Guglielmetti P, Rossolini A, Barberi A, Cusi G, Musmanno RA, Russi M, Quaranta S. Cytotoxin production by Campylobacter pylori strains isolated from patients with peptic ulcers and from patients with chronic gastritis only. J Clin Microbiol. 1989 Jan;27(1):225–226. [PMC free article] [PubMed]
  • Forman D, Sitas F, Newell DG, Stacey AR, Boreham J, Peto R, Campbell TC, Li J, Chen J. Geographic association of Helicobacter pylori antibody prevalence and gastric cancer mortality in rural China. Int J Cancer. 1990 Oct 15;46(4):608–611. [PubMed]
  • Fox JG, Cabot EB, Taylor NS, Laraway R. Gastric colonization by Campylobacter pylori subsp. mustelae in ferrets. Infect Immun. 1988 Nov;56(11):2994–2996. [PMC free article] [PubMed]
  • Fox JG, Correa P, Taylor NS, Lee A, Otto G, Murphy JC, Rose R. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenterology. 1990 Aug;99(2):352–361. [PubMed]
  • Fox JG, Correa P, Taylor NS, Zavala D, Fontham E, Janney F, Rodriguez E, Hunter F, Diavolitsis S. Campylobacter pylori-associated gastritis and immune response in a population at increased risk of gastric carcinoma. Am J Gastroenterol. 1989 Jul;84(7):775–781. [PubMed]
  • Fox JG, Edrise BM, Cabot EB, Beaucage C, Murphy JC, Prostak KS. Campylobacter-like organisms isolated from gastric mucosa of ferrets. Am J Vet Res. 1986 Feb;47(2):236–239. [PubMed]
  • Fox JG, Lee A. Gastric campylobacter-like organisms: their role in gastric disease of laboratory animals. Lab Anim Sci. 1989 Nov;39(6):543–553. [PubMed]
  • Fox JG, Otto G, Murphy JC, Taylor NS, Lee A. Gastric colonization of the ferret with Helicobacter species: natural and experimental infections. Rev Infect Dis. 1991 Jul-Aug;13 (Suppl 8):S671–S680. [PubMed]
  • Fox JG, Otto G, Taylor NS, Rosenblad W, Murphy JC. Helicobacter mustelae-induced gastritis and elevated gastric pH in the ferret (Mustela putorius furo). Infect Immun. 1991 Jun;59(6):1875–1880. [PMC free article] [PubMed]
  • Fox JG, Wishnok JS, Murphy JC, Tannenbaum SR, Correa P. MNNG-induced gastric carcinoma in ferrets infected with Helicobacter mustelae. Carcinogenesis. 1993 Sep;14(9):1957–1961. [PubMed]
  • Goodwin CS, Armstrong JA, Marshall BJ. Campylobacter pyloridis, gastritis, and peptic ulceration. J Clin Pathol. 1986 Apr;39(4):353–365. [PMC free article] [PubMed]
  • Gottfried MR, Washington K, Harrell LJ. Helicobacter pylori-like microorganisms and chronic active gastritis in ferrets. Am J Gastroenterol. 1990 Jul;85(7):813–818. [PubMed]
  • Hazell SL, Borody TJ, Gal A, Lee A. Campylobacter pyloridis gastritis I: Detection of urease as a marker of bacterial colonization and gastritis. Am J Gastroenterol. 1987 Apr;82(4):292–296. [PubMed]
  • Hazell SL, Lee A. Campylobacter pyloridis, urease, hydrogen ion back diffusion, and gastric ulcers. Lancet. 1986 Jul 5;2(8497):15–17. [PubMed]
  • Hazell SL, Lee A, Brady L, Hennessy W. Campylobacter pyloridis and gastritis: association with intercellular spaces and adaptation to an environment of mucus as important factors in colonization of the gastric epithelium. J Infect Dis. 1986 Apr;153(4):658–663. [PubMed]
  • Kostrzynska M, Betts JD, Austin JW, Trust TJ. Identification, characterization, and spatial localization of two flagellin species in Helicobacter pylori flagella. J Bacteriol. 1991 Feb;173(3):937–946. [PMC free article] [PubMed]
  • Krakowka S, Morgan DR, Kraft WG, Leunk RD. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect Immun. 1987 Nov;55(11):2789–2796. [PMC free article] [PubMed]
  • Lee A, Fox J, Hazell S. Pathogenicity of Helicobacter pylori: a perspective. Infect Immun. 1993 May;61(5):1601–1610. [PMC free article] [PubMed]
  • Leunk RD, Ferguson MA, Morgan DR, Low DE, Simor AE. Antibody to cytotoxin in infection by Helicobacter pylori. J Clin Microbiol. 1990 Jun;28(6):1181–1184. [PMC free article] [PubMed]
  • Leunk RD, Johnson PT, David BC, Kraft WG, Morgan DR. Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J Med Microbiol. 1988 Jun;26(2):93–99. [PubMed]
  • Nomura A, Stemmermann GN, Chyou PH, Kato I, Perez-Perez GI, Blaser MJ. Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med. 1991 Oct 17;325(16):1132–1136. [PubMed]
  • O'Rourke J, Lee A, Fox JG. An ultrastructural study of Helicobacter mustelae and evidence of a specific association with gastric mucosa. J Med Microbiol. 1992 Jun;36(6):420–427. [PubMed]
  • Otto G, Fox JG, Wu PY, Taylor NS. Eradication of Helicobacter mustelae from the ferret stomach: an animal model of Helicobacter (Campylobacter) pylori chemotherapy. Antimicrob Agents Chemother. 1990 Jun;34(6):1232–1236. [PMC free article] [PubMed]
  • Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med. 1991 Oct 17;325(16):1127–1131. [PubMed]
  • Peterson WL. Helicobacter pylori and peptic ulcer disease. N Engl J Med. 1991 Apr 11;324(15):1043–1048. [PubMed]
  • Phadnis SH, Ilver D, Janzon L, Normark S, Westblom TU. Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. Infect Immun. 1994 May;62(5):1557–1565. [PMC free article] [PubMed]
  • Rabeneck L, Ransohoff DF. Is Helicobacter pylori a cause of duodenal ulcer? A methodologic critique of current evidence. Am J Med. 1991 Dec;91(6):566–572. [PubMed]
  • Rautelin H, Kosunen TU. Helicobacter pylori and associated gastroduodenal diseases. Review article. APMIS. 1991 Aug;99(8):677–695. [PubMed]
  • Solnick JV, Josenhans C, Suerbaum S, Tompkins LS, Labigne A. Construction and characterization of an isogenic urease-negative mutant of Helicobacter mustelae. Infect Immun. 1995 Sep;63(9):3718–3721. [PMC free article] [PubMed]
  • Suerbaum S, Josenhans C, Labigne A. Cloning and genetic characterization of the Helicobacter pylori and Helicobacter mustelae flaB flagellin genes and construction of H. pylori flaA- and flaB-negative mutants by electroporation-mediated allelic exchange. J Bacteriol. 1993 Jun;175(11):3278–3288. [PMC free article] [PubMed]
  • Tompkins DS, Wyatt JI, Rathbone BJ, West AP. The characterization and pathological significance of gastric Campylobacter-like organisms in the ferret: a model for chronic gastritis? Epidemiol Infect. 1988 Oct;101(2):269–278. [PMC free article] [PubMed]
  • Tsuda M, Karita M, Morshed MG, Okita K, Nakazawa T. A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect Immun. 1994 Aug;62(8):3586–3589. [PMC free article] [PubMed]
  • Tummuru MK, Cover TL, Blaser MJ. Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect Immun. 1993 May;61(5):1799–1809. [PMC free article] [PubMed]
  • Tummuru MK, Cover TL, Blaser MJ. Mutation of the cytotoxin-associated cagA gene does not affect the vacuolating cytotoxin activity of Helicobacter pylori. Infect Immun. 1994 Jun;62(6):2609–2613. [PMC free article] [PubMed]
  • Wallace JL. Possible mechanisms and mediators of gastritis associated with Helicobacter pylori infection. Scand J Gastroenterol Suppl. 1991;187:65–70. [PubMed]

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