Helicobacter pylori enter and survive within multivesicular vacuoles of epithelial cells

Cellular Microbiology

Volumn 4, Issue 10, 2002, Pages 677-690

  Amieva, Manuel R ^a   Salama, Nina R ^b   Tompkins, Lucy S ^a   Falkow, Stanley ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CYTOCHALASIN D; FLUORESCENT DYE; GENTAMICIN;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL REPRODUCTION; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CARCINOMA CELL; CELL INVASION; CELL LINE; CELL STRAIN CACO 2; CELL STRUCTURE; CELL VACUOLE; COLON ADENOCARCINOMA; CONTROLLED STUDY; CYTOSKELETON; ELECTRON MICROSCOPY; ENDOSOME; EPITHELIUM CELL; ERADICATION THERAPY; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; KIDNEY CELL; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; STOMACH ADENOCARCINOMA; TREATMENT FAILURE; VIDEORECORDING;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL LINE; CYTOCHALASIN D; CYTOSKELETON; ENDOCYTOSIS; EPITHELIAL CELLS; FLUORESCENT DYES; GENTAMICINS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; HYDROGEN-ION CONCENTRATION; MICROSCOPY, CONFOCAL; MICROSCOPY, VIDEO; TUMOR CELLS, CULTURED; VACUOLES;

ANIMALIA; BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI;

EID: 0036797045     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1462-5822.2002.00222.x     Document Type: Article

References (62)

1. Allen, L.A. (1999) Intracellular niches for extracellular bacteria: lessons from Helicobacter pylori. J Leuko Biol 66: 753-756.
2. Allen, L.A., Schlesinger, L.S., and Kang, B. (2000) Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J Exp Med 191: 115-128.
3. Andersen, L.P., Blom, J., and Nielsen, H. (1993) Survival and ultrastructural changes of Helicobacter pylori after phagocytosis by human polymorphonuclear leukocytes and monocytes. Apmis 101: 61-72.
4. Arenas, G.N., Staskevich, A.S., Aballay, A., and Mayorga, L.S. (2000) Intracellular trafficking of Brucella abortus in J774 macrophages. Infect Immun 68: 4255-4263.
5. Axon, A.T. (1996) Eradication of Helicobacter pylori. Scand J Gastroenterol Suppl 214: 47-53; discussion 57-60.
6. Bjorkholm, B., Zhukhovitsky, V., Lofman, C., Hulten, K., Enroth, H., Block, M. et al. (2000) Helicobacter pylori entry into human gastric epithelial cells: a potential determinant of virulence, persistence, and treatment failures. Helicobacter 5: 148-154.
7. Bode, G., Malfertheiner, P., and Ditschuneit, H. (1988) Pathogenetic implications of ultrastructural findings in Campylobacter pylori related gastroduodenal disease. Scand J Gastroenterol Suppl 142: 25-39.
8. Bonamico, M., Mariani, P., Magliocca, F.M., Petrozza, V., Montuori, M., Pezzella, C. et al. (1997) Helicobacter pylori duodenal colonization in children. Acta Paediatr 86: 356-360.
9. Brenciaglia, M.I., Fornara, A.M., Scaltrito, M.M., Braga, P.C., and Dubini, F. (1996) Activity of amoxicillin, metronidazole, bismuth salicylate and six aminoglycosides against Helicobacter pylori. J Chemother 8: 52-54.
10. Catrenich, C.E., and Chestnut, M.H. (1992) Character and origin of vacuoles induced in mammalian cells by the cytotoxin of Helicobacter pylori. J Med Microbiol 37: 389-395.
11. Chan, W.Y., Hui, P.K., Leung, K.M., and Thomas, T.M. (1992) Modes of Helicobacter colonization and gastric epithelial damage. Histopathology 21: 521-528.
12. Chmiela, M., Paziak-Domanska, B., and Wadström, T. (1995) Attachment, ingestion and intracellular killing of Helicobacter pylori by human peripheral blood mononuclear leukocytes and mouse peritoneal inflammatory macrophages. FEMS Immunol Med Microbiol 10: 307-316.
13. Copass, M., Grandi, G., and Rappuoli, R. (1997) Introduction of unmarked mutations in the Helicobacter pylori vacA gene with a sucrose sensitivity marker. Infect Immun 65: 1949-1952.
14. Corthésy-Theulaz, I., Porta, N., Pringault, E., Racine, L., Bogdanova, A., Kraehenbuhl, J.P. et al. (1996) Adhesion of Helicobacter pylori to polarized T84 human intestinal cell monolayers is pH dependent. Infect Immun 64: 3827-3832.
15. Covacci, A., Censini, S., Bugnoli, M., Petracca, R., Burroni, D., Macchia, G. et al. (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.
16. Covacci, A., Falkow, S., Berg, D.E., and Rappuoli, R. (1997) Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori? Trends Microbiol 5: 205-208.
17. Crabtree, J.E., Xiang, Z., Lindley, I.J., Tompkins, D.S., Rappuoli, R., and Covacci, A. (1995a) Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori. J Clin Pathol 48: 967-969.
18. Crabtree, J.E., Covacci, A., Farmery, S.M., Xiang, Z., Tompkins, D.S., Perry, S. et al. (1995b) Helicobacter pylori induced interleukin-8 expression in gastric epithelial cells is associated with CagA positive phenotype. J Clin Pathol 48: 41-45.
19. Denzer, K., Kleijmeer, M.J., Heijnen, H.F., Stoorvogel, W., and Geuze, H.J. (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113: 3365-3374.
20. Dorn, B.R., Dunn, W.A. Jr and Progulske-Fox, A. (2001) Porphyromonas gingivalis traffics to autophagosomes in human coronary artery endothelial cells. Infect Immun 69: 5698-5708.
21. Dorn, B.R., Dunn, W.A., and Progulske-Fox, A. (2002) Bacterial interactions with the autophagic pathway. Cell Microbiol 4: 1-10.
22. Evans, D.G., Evans, D.J. Jr and Graham, D.Y. (1992) Adherence and internalization of Helicobacter pylori by HEp-2 cells. Gastroenterology 102: 1557-1567.
23. Figueroa-Arredondo, P., Heuser, J.E., Akopyants, N.S., Morisaki, J.H., Giono-Cerezo, S., Enriquez-Rincon, F., and Berg, D.E. (2001) Cell vacuolation caused by Vibrio cholerae hemolysin. Infect Immun 69: 1613-1624.
24. Foliguet, B., Vicari, F., Guedenet, J.C., De Korwin, J.D., and Marchal, L. (1989) Scanning electron microscopic study of Campylobacter pylori and associated gastroduodenal lesions. Gastroenterol Clin Biol 13: 65B-70B.
25. Goodman, K.J., and Correa, P. (2000) Transmission of Helicobacter pylori among siblings. Lancet 355: 358-362.
26. Han, S.R., Zschausch, H.C., Meyer, H.G., Schneider, T., Loos, M., Bhakdi, S., and Maeurer, M.J. (2000) Helicobacter pylori: clonal population structure and restricted transmission within families revealed by molecular typing. J Clin Microbiol 38: 3646-3651.
27. Hazell, S.L., Lee, A., Brady, L., and Hennessy, W. (1986) 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 153: 658-663.
28. Israel, D.A., Salama, N., Arnold, C.N., Moss, S.F., Ando, T., Wirth, H.P. et al. (2001) Helicobacter pylori strain-specific differences in genetic content, identified by microarray, influence host inflammatory responses. J Clin Invest 107: 611-620.
29. Kang, J.K., Kim, E., Kim, K.H., and Oh, S.H. (1991) Association of Helicobacter pylori with gastritis and peptic ulcer diseases. Yonsei Med J 32: 157-168.
30. Kazi, J.L., Sinniah, R., Zaman, V., Ng, M.L., Jafarey, N.A., Alam, S.M. et al. (1990) Ultrastructural study of Helicobacter pylori-associated gastritis. J Pathol 161: 65-70.
31. Ko, G.H., Kang, S.M., Kim, Y.K., Lee, J.H., Park, C.K., Youn, H.S. et al. (1999) Invasiveness of Helicobacter pylori into human gastric mucosa. Helicobacter 4: 77-81.
32. Kwok, T., Backert, S., Schwarz, H., Berger, J., and Meyer, T.F. (2002) Specific entry of Helicobacter pylori into cultured gastric epithelial cells via a zipper-like mechanism. Infect Immun 70: 2108-2120.
33. Lin, H.J., Herman, P., Kang, J.S., and Lakowicz, J.R. (2001) Fluorescence lifetime characterization of novel low-pH probes. Anal Biochem 294: 118-125.
34. Malfertheiner, P., Bode, G., Stanescu, A., and Ditschuneit, H. (1989) Gastric metaplasia and Campylobacter pylori in duodenal ulcer disease: an ultrastructural analysis. Gastroenterol Clin Biol 13 (1): 71B-74B.
35. Martinez, J.J., Mulvey, M.A., Schilling, J.D., Pinkner, J.S., and Hultgren, S.J. (2000) Type 1 pilus-mediated bacterial invasion of bladder epithelial cells. EMBO J 19: 2803-2812.
36. Miyaji, H., Azuma, T., Ito, S., Abe, Y., Gejyo, F., Hashimoto, N. et al. (2000) Helicobacter pylori infection occurs via close contact with infected individuals in early childhood. J Gastroenterol Hepatol 15: 257-262.
37. Molinari, M., Galli, C., Norais, N., Telford, J.L., Rappuoli, R., Luzio, J.P., and Montecucco, C. (1997) Vacuoles induced by Helicobacter pylori toxin contain both late endosomal and lysosomal markers. J Biol Chem 272: 25339-25344.
38. Montecucco, C., De Bernard, M., Papini, E., and Zoratti, M. (2001) Helicobacter pylori vacuolating cytotoxin: cell intoxication and anion-specific channel activity. Current Topics Microbiol Immunol 257: 113-129.
39. Mulvey, M.A., Schilling, J.D., and Hultgren, S.J. (2001) Establishment of a persistent Escherichia coli reservoir during the acute phase of a bladder infection. Infect Immun 69: 4572-4579.
40. Neale, K.R., and Logan, R.P. (1995) The epidemiology and transmission of Helicobacter pylori infection in children. Alimentary Pharmacol Ther 9 (Suppl. 2): 77-84.
41. Noach, L.A., Rolf, T.M., and Tytgat, G.N. (1994) Electron microscopic study of association between Helicobacter pylori and gastric and duodenal mucosa. J Clin Pathol 47: 699-704.
42. Papadogiannakis, N., Willén, R., Carlén, B., Sjöstedt, S., Wadström, T., and Gad, A. (2000) Modes of adherence of Helicobacter pylori to gastric surface epithelium in gas-troduodenal disease: a possible sequence of events leading to internalization. Apmis 108: 439-447.
43. Papini, E., de Bernard, M., Milia, E., Bugnoli, M., Zerial, M., Rappuoli, R., and Montecucco, C. (1994) Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Natl Acad Sci USA 91: 9720-9724.
44. Pechere, J. (2001) New perspectives on macrolide antibiotics. Int J Antimicrob Agents 18: 93-97.
45. Peek, R.M. Jr (2001) IV. Helicobacter pylori strain-specific activation of signal transduction cascades related to gastric inflammation. Am J Physiol Gastrointest Liver Physiol 280: G525-G530.
46. Peek, R.M. Jr, Blaser, M.J., Mays, D.J., Forsyth, M.H., Cover, T.L., Song, S.Y. et al. (1999) Helicobacter pylori strain-specific genotypes and modulation of the gastric epithelial cell cycle. Cancer Res 59: 6124-6131.
47. Petersen, A.M., Sorensen, K., Blom, J., and Krogfelt, K.A. (2001) Reduced intracellular survival of Helicobacter pylori vacA mutants in comparison with their wild-types indicates the role of VacA in pathogenesis. FEMS Immunol Med Microbiol 30: 103-108.
48. Phadnis, S.H., Ilver, D., Janzon, L., Normark, S., and Westblom, T.U. (1994) Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. Infect Immun 62: 1557-1565.
49. Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J.L., and Gorvel, J.P. (1998) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387-2392.
50. Rothenbacher, D., Bode, G., Berg, G., Knayer, U., Gonser, T., Adler, G., and Brenner, H. (1999) Helicobacter pylori among preschool children and their parents: evidence of parent-child transmission. J Infect Dis 179: 398-402.
51. Salama, N.R., Otto, G., Tompkins, L., and Falkow, S. (2001) Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect Immun 69: 730-736.
52. Segal, E.D., Lange, C., Covacci, A., Tompkins, L.S., and Falkow, S. (1997) Induction of host signal transduction pathways by Helicobacter pylori. Proc Natl Acad Sci USA 94: 7595-7599.
53. el-Shoura, S.M. (1995) Helicobacter pylori. I. Ultrastructural sequences of adherence, attachment, and penetration into the gastric mucosa. Ultrastruct Pathol 19: 323-333.
54. Sommi, P., Ricci, V., Fiocca, R., Romano, M., Ivey, K.J., Cova, E. et al, (1996) Significance of ammonia in the genesis of gastric epithelial lesions induced by Helicobacter pylori: an in vitro study with different bacterial strains and urea concentrations. Digestion 57: 299-304.
55. Steer, H.W. (1984) Surface morphology of the gastroduodenal mucosa in duodenal ulceration. Gut 25: 1203-1210.
56. Su, B., Johansson, S., Fällman, M., Patarroyo, M., Granström, M., and Normark, S. (1999) Signal transduction-mediated adherence and entry of Helicobacter pylori into cultured cells. Gastroenterology 117: 595-604.
57. Sung, J.J. (2000) Where are we with current therapy? Helicobacter 5 (Suppl. 1): S17-S21; discussion S27-31.
58. Wang, Y., and Taylor, D.E. (1990) Chloramphenicol resistance in Campylobacter coli: nucleotide sequence, expression, and cloning vector construction. Gene 94: 23-28.
59. Wilkinson, S.M., Uhl, J.R., Kline, B.C., Cockerill, F.R., 3rd (1998) Assessment of invasion frequencies of cultured HEp-2 cells by clinical isolates of Helicobacter pylori using an acridine orange assay. J Clin Pathol 51: 127-133.
60. Wyle, F.A., Tarnawski, A., Schulman, D., and Dabros, W. (1990) Evidence for gastric mucosal cell invasion by C. pylori: an ultrastructural study. J Clin Gastroenterol 12: S92-S98.
61. Xiang, Z., Censini, S., Bayeli, P.F., Telford, J.L., Figura, N., Rappuoli, R., and Covacci, A. (1995) Analysis of expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two major types and that CagA is not necessary for expression of the vacuolating cytotoxin. Infect Immun 63: 94-98.
62. Yamashiro, Y., Oguchi, S., Otsuka, Y., Nagata, S., Shioya, T., and Shimizu, T. (1994) Helicobacter pylori colonization in children with gastritis and peptic ulcer. II. Ultrastructural change of the gastric mucosa. Acta Paediatr Jpn 36: 171-175.