Experimental infection of Mongolian gerbils with wild-type and mutant Helicobacter pylori strains

Infection and Immunity

Volumn 66, Issue 10, 1998, Pages 4856-4866

  Wirth, Hans Peter ^a,c   Beins, Michael H ^a   Yang, Manqiao ^a,c   Tham, Kyi T ^a,b   Blaser, Martin J ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL INFECTION; BACTERIUM CULTURE; BACTERIUM ISOLATION; BACTERIUM MUTANT; CONTROLLED STUDY; EXPERIMENTAL INFECTION; GASTRITIS; GERBIL; HELICOBACTER PYLORI; HISTOPATHOLOGY; INFECTION RATE; NONHUMAN; PRIORITY JOURNAL;

EID: 0031664438     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.66.10.4856-4866.1998     Document Type: Article

References (61)

1. Abraham, D., D. J. Weiner, and J. P. Farrell. 1986. Cellular and humoral immune responses of jirds resistant to Dipetalonema viteae infection. Infect. Immun. 52:742-747.
2. Akopyanz, N., N. O. Bukanov, T. U. Westblom, S. Kresovich, and D. E. Berg. 1992. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 20:5137-5142.
3. Andrutis, K. A., J. G. Fox, D. B. Schauer, R. P. Marini, J. C. Murphy, L. Yan, and J. V. Solnick. 1995. Inability of an isogenic urease-negative mutant strain of Helicobacter mustelae to colonize the ferret stomach. Infect. Immun. 63:3722-3725.
4. Andrutis, K. A., J. G. Fox, D. B. Schauer, R. P. Marini, X. Li, L. Yan, C. Josenhans, and S. Suerbaum. 1997. Infection of the ferret stomach by isogenic flagellar mutant strains of Helicobacter mustelae. Infect. Immun. 65:1962-1966.
5. Bartizal, K. F., B. S. Wostmann, and M. Wagner. 1984. Distribution and effects of a defined six-member murine-derived microflora in gnotobiotic gerbils. Appl. Environ. Microbiol. 47:746-751.
6. Bingel, S. A. 1995. Pathologic findings in an aging Mongolian gerbil (Meriones unguiculatus) colony. Lab. Anim. Sci. 45:597-600.
7. Blaser, M. J. 1996. Role of vacA and the cagA locus of Helicobacter pylori in human disease. Aliment. Pharmacol. Ther. 10(Suppl. 1):73-77.
8. Censini, S., C. Lange, Z. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
9. Cheal, M. L. 1986. The gerbil: a unique model for research on aging. Exp. Aging Res. 12:3-21.
10. Chen, X. G., P. Correa, J. Offerhaus, E. Rodriguez, F. Janney, E. Hoffmann, J. Fox, F. Hunter, and S. Diavolitsis. 1986. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am. J. Clin. Pathol. 86:575-582.
11. Covacci, A., S. Censini, M. Bugnoli, R. Petracca, D. Burroni, G. Macchia, A. Massone, E. Papini, Z. Xiang, N. Figura, and R. Rappuoli. 1993. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc. Natl. Acad. Sci. USA 90:5791-5795.
12. Cover, T. L., M. K. R. Tummuru, P. Cao, S. A. Thompson, and M. J. Blaser. 1994. Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J. Biol. Chem. 269:10566-10573.
13. Cover, T. L., and M. J. Blaser. 1996. Helicobacter pylori, a paradigm for chronic mucosal inflammation: pathogenesis and implications for eradication and prevention. Adv. Intern. Med. 41:85-117.
14. Dubois, A., N. Fiala, L. M. Heman-Ackah, E. S. Drazek, A. Tarnawski, W. N. Fishbein, G. I. Perez-Perez, and M. J. Blaser. 1994. Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology 106:1405-1417.
15. Dubois, A., D. E. Berg, E. T. Incecik, N. Fiala, L. M. Heman-Ackah, G. I. Perez-Perez, and M. J. Blaser. 1996. Transient and persistent experimental infection of nonhuman primates with Helicobacter pylori: implications for human disease. Infect. Immun. 64:2885-2891.
16. Eaton, K. A., C. L. Brooks, D. R. Morgan, and S. Krakowka. 1991. Essential role of urease in pathogenesis of gastritis induced by Helicobacter pylori in gnotobiotic piglets. Infect. Immun. 59:2470-2475.
17. Eaton, K. A., T. L. Cover, M. K. R. Tummuru, M. J. Blaser, and S. Krakowka. 1947. Role of vacuolating cytotoxin in gastritis due to Helicobacter pylori in gnotobiotic piglets. Infect. Immun. 65:3462-3464.
18. Eaton, K. A., and S. Krakowka. 1994. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect. Immun. 62:3604-3607.
19. Engstrand, L. 1995. Potential animal models of Helicobacter pylori infection in immunological and vaccine research. FEMS immunol. Med. Microbiol. 10:265-270.
20. Fox, J. G., P. Correa, N. S. Taylor, A. Lee. G. Otto, J. C. Murphy, and R. Rose. 1990. Helicobacter mustelae-associated gastritis in ferrets. An animal model of Helicobacter pylori gastritis in humans. Gastroenteroloyy 99:352-361.
21. Fox, J. G., M. Batchelder, R. Marini, L. Yan, L. Handt, X. Li, B. Shames, A. Hayward, J. Campbell, and J. C. Murphy. 1995. Helicobacter pylori-induced gastritis in the domestic cat. Infect. Immun. 63:2674-2681.
22. Fox, J. G., and A. Lee. 1997. The role of Helicobacter species in newly recognized gastrointestinal tract diseases of animals. Lab. Anim. Sci. 47:222-255.
23. Ghiara, P., M. Marchetti, M. J. Blaser, M. K. R. Tummuru, T. L. Cover, E. D. Segal, L. S. Tompkins, and R. Rappuoli. 1995. Role of the Helicobacter pylori virulence factors vacuolnting cytotoxin, CagA, and urease in a mouse model of disease. Infect. Immun. 63:4154-4160.
24. Ghoshal, N. G., and H. S. Bal. 1984. Comparative morphology of the stomach of some laboratory mammals. Lab. Anim. 23:21-29.
25. Gorenflot, A., E. Precigout, G. Bissuel, O. Lecointre, P. Brasseur, E. Vidor, M. L'Hostis, and J. Schrevel. 1990. Identification of major Babesia divergent polypeptides that induce protection against homologous challenge in gerbils. Infect. Immun. 58:4076-4082.
26. Harlan Sprague-Dawley, Inc. 1997. Personal communication.
27. Hazell, S. L., T. J. Borody, A. Gal, and A. Lee. 1987. Campylobacter pyloridis gastritis I: detection of urease as a marker of bacterial colonization and gastritis. Am. J. Gastroenterol. 82:292-296.
28. Hirata, I., T. Itoh, K. Suzuki, Y. Irikura, S. Kaneko, S. Takahashi. 1993. Colonization of urease positive and negative strains of Helicobacter pylori in gastric mucosa of cynomolgus monkeys. Acta Gastroenterol. Belg. 56(Suppl.):112.
29. Hirayama, F., S. Takagi, Y. Yokoyama, E. Iwao, and Y. Ikeda. 1996. Establishment of gastric Helicobacter pylori infection in Mongolian gerbils. J. Gastroenterol. 31(Suppl. IX):24-28.
30. Hirayama, F., S. Takagi, H. Kusuhara, E. Iwao, Y. Yokoyama, and Y. Ikeda. 1996. Induction of gastric ulcer and intestinal metaplasia in Mongolian gerbils infected with Helicobacter pylori. J. Gastroenterol. 31:755-757.
31. Karita, M., T. Kouchiyama, K. Okita, and T. Nakazawa. 1991. New small animal model for human gastric Helicobacter pylori infection: success in both nude and euthymic mice. Am. J. Gastroenterol. 86:1596-1603.
32. Karita, M., Q. Li, D. Cantero, and K. Okita. 1994. Establishment of a small animal model for human Helicobacter pylori infection using germ-free mouse. Am. J. Gastroenterol. 89:208-213.
33. Karita, M., M. K. R. Tummuru, H. P. Wirth, and M. J. Blaser. 1996. Effect of growth phase and acid shock on Helicobacter pylori cagA expression. Infect. Immun. 64:4598-4605.
34. Kariwa, H., J. Arikawa, I. Takashima, and N. Hashimoto. 1992. Development and application of protein G antibody assay for the detection of antibody to hantavirus. J. Virol. Methods 37:345-354.
35. Krakowka, S., D. R. Morgan, W. G. Kraft, and R. D. Leunk. 1987. Establishment of gastric Campylobacter pylori infection in the neonatal gnotobiotic piglet. Infect. Immun. 55:2789-2796.
36. Krakowka, S., K. A. Eaton, and D. M. Rings. 1995. Occurrence of gastric ulcers in gnotobiotic piglets colonized by Helicobacter pylori. Infect. Immun. 63:2352-2355.
37. Lambert, J. K., M. Borromeo, K. J. Pinkard, H. Turner, C. B. Chapman, and M. L. Smith. 1987. Colonization of gnotobiotic piglets with Campylobacter pyloridis - an animal model? J. Infect. Dis. 155:1344-1348.
38. Lee, A., J. G. Fox, G. Otto, and J. C. Murphy. 1990. A small animal model of human Helicobacter pylori active chronic gastritis. Gastroenterology 99:1315-1323.
39. Lee, A., J. O'Rourke, M. Coruzon de Ungria, B. Robertson, G. Daskalopoulos, and M. F. Dixon. 1997. A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112:1386-1397.
40. Marchetti, M., B. Aricò, D. Burroni, N. Figura, R. Rappuoli, and P. Ghiara. 1995. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 267:1655-1658.
41. Matsumoto, S., Y. Washizuka, Y. Matsumoto, S. Tawara, F. Ikeda, Y. Yokota, and M. Karita. 1997. Induction of ulceration and severe gastritis in Mongolian gerbil by Helicobacter pylori infection. J. Med. Microbiol. 46:391-397.
42. McColm, A. A., J. Bagshaw, C. O'Malley, et al. 1995. Development of a mouse model of gastric colonisation with Helicobacter pylori. Gut 37(Suppl. 1):A50.
43. Mohammadi, M., R. Redline, J. Nedrud, and S. Czinn. 1996. Role of the host in pathogenesis of Helicobacter-associated gastritis: H. felis infection of inbred and congenic mouse strains. Infect. Immun. 64:238-245.
44. Morris, A. J., M. R. Ali, G. I. Nicholson, G. I. Perez-Perez, and M. J. Blaser. 1941. Long-term follow-up of voluntary ingestion of Helicobacter pylori. Ann. Intern. Med. 114:662-663.
45. Newell, D. G. 1987. Human antibody responses to the surface protein antigens of Camphylobacter pyloridis. Serodiagn. Immunother. 1:209-217.
46. Radin, M. J., K. A. Eaton, S. Krakowa, D. R. Morgan, A. Lee, G. Otto, and J. Fox. 1990. Helicobacter pylori gastric infection in gnotobiotic beagle dogs. Infect. Immun. 58:2606-2612.
47. Shuto, R., T. Fujioka, T. Kubota, and M. Nasu. 1993. Experimental gastritis induced by Helicobacter pylori in Japanese monkeys. Infect. Immun. 61:933-939.
48. Soong, C. G., B. E. Torian, M. D. Abd-Alla, T. F. Jackson, V. Gatharim, and J. I. Ravdin. 1995. Protection of gerbils from amebic liver ascess by immunization with recombinant Entamboeba histolytica 29-kilodalton antigen. Infect. Immun. 63:472-477.
49. Tham, K. T. Unpublished data.
50. Tomb, J.-F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
51. Tsuda, M., M. Karita, M. G. Morshed, K. Okita, and T. Nakazawa. 1994. A urease-negative mutant of Helicobacter pylori constructed by allelic exchange mutagenesis lacks the ability to colonize the nude mouse stomach. Infect. Immun. 62:3586-3589.
52. Tummuru, M. K. R., T. L. Cover, and M. J. Blaser. 1993. Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect. Immun. 61:1799-1809.
53. Winger, C. M., E. U. Canning, and J. D. Culverhouse. 1987. Induction of protective immunity to Babesia divergens in Mongolian gerbils, Meriones unguiculatus, using culture-derived immunogens. Vet. Parasitol. 26:43-53.
54. Wirth, H. P. Unpublished data.
55. Wirth, H. P., M. Yang, M. Karita, and M. J. Blaser. 1996. Expression of the human cell surface glycoconjugates Lewis X and Lewis Y by Helicobacter pylori isolates is related to cagA status. Infect. Immun. 64:4598-4605.
56. Wirth, H. P., M. Yang, R. M. Peek, K. T. Tham, and M. J. Blaser. 1997. Helicobacter pylori Lewis expression is related to the host Lewis phenotype. Gastroenterology 113:1091-1098.
57. Worthington, J. M., and R. S. Fulghum. 1988. Cecal and fecal bacterial flora of the Mongolian gerbil and the chinchilla. Appl. Environ. Microbiol. 54:1210-1215.
58. Yates, J. A., E. K. Saliba, K. L. Yates, K. Schmitz, M. Othman, and G. I. Higashi. 1989. Course of infection and humoral response to Leishmania major in inbred Meriones unguiculatits, J. Parasitol. 75:942-945.
59. Yokota, K., Y. Kurebayashi, Y. Takayama, S. Hayashi, H. Isogai, E. Isogai, K. Imai, T. Yabana, A. Yachi, and K. Oguma. 1991. Colonization of Helicobacter pylori in the gastric mucosa of Mongolian gerbils. Microbiol. Immunol. 35:475-480.
60. Zhang, H. M., N. Wakisaka, O. Maeda, and T. Yamamoto. 1997. Vitamin C inhibits the growth of a bacterial risk factor for gastric adenocarcinoma: Helicobacter pylori. Cancer 80:1897-1903.
61. Zhang, T., and S. L. Stanley, Jr. 1996. Oral immunization with an attenuated vaccine strain of Salmonella typhimurium expressing the serine-rich Entabmoeba histolytica protein induces an antiamebic immune response and protects gerbils from amebic liver abscess. Infect. Immun. 64:1526-1531.