Helicobacter pylori: An invading microorganism? A review

FEMS Immunology and Medical Microbiology

Volumn 36, Issue 3, 2003, Pages 117-126

  Petersen, Andreas Munk ^a   Krogfelt, Karen Angeliki ^a  

^a STATENS SERUM INSTITUT   (Denmark)

Author keywords

Epithelial cell; Helicobacter pylori; Intracellular survival; Invasion

Indexed keywords

ACTIN; AMMONIUM CHLORIDE; CHLOROQUINE; CYTOCHALASIN B; CYTOCHALASIN D; CYTOTOXIN; DANSYLCADAVERINE; GENTAMICIN; HEAT SHOCK PROTEIN 60; HEMAGGLUTININ; METHYLAMINE; SUPEROXIDE DISMUTASE;

BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; CAMPYLOBACTER JEJUNI; CELL CULTURE; CELL DAMAGE; CELL DIVISION; CELL INVASION; CELL SURVIVAL; CELL VACUOLE; CHRONIC GASTRITIS; CONFERENCE PAPER; DISEASE ASSOCIATION; DUODENUM ULCER; EPITHELIUM CELL; ESCHERICHIA COLI; EXTRACELLULAR SPACE; FETAL CALF SERUM; FREQUENCY ANALYSIS; HELICOBACTER PYLORI; HEP 2 CELL; HUMAN; HYPOTHESIS; IMMUNOCOMPETENT CELL; IN VIVO STUDY; INTERNALIZATION; INTESTINE INFECTION; INTRACELLULAR SPACE; MICROORGANISM; NONHUMAN; PATHOGENESIS; PEPTIC ULCER; PHAGOCYTE; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHIGELLA FLEXNERI; STOMACH BIOPSY; STOMACH EPITHELIUM; STOMACH MUCUS; YERSINIA ENTEROCOLITICA;

EID: 0038061773     PISSN: 09288244     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0928-8244(03)00020-8     Document Type: Conference Paper

References (83)

1. Warren J.R., Marshall B.J. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet. 1:1983;1275.
2. Marshall B.J., Warren J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet. 1:1984;1311-1314.
3. Hopkins R.J., Girardi L.S., Turney E.A. Relationship between Helicobacter pylori eradication and reduced duodenal and gastric ulcer recurrence: a review. Gastroenterology. 110:1996;1244-1252.
4. Kreiss C., Blum A.L., Malfertheiner P. Peptic ulcer pathogenesis. Curr. Opin. Gastroenterol. 11:1995;25-31.
5. Forman D. Helicobacter pylori and gastric cancer. Scand. J. Gastroenterol. 31:1996;48-51.
6. Bayerdorffer E., Neubauer A., Rudolph B., Thiede C., Lehn N., Eidt S., Stolte M. Regression of primary gastric lymphoma of mucosa-associated lymphoid tissue type after cure of Helicobacter pylori infection. Lancet. 345:1995;1591-1594.
7. Logan R.P. Helicobacter pylori and gastric cancer. Lancet. 344:1994;1078-1079.
8. Parsonnet J. Helicobacter pylori. Infect. Dis. Clin. N. Am. 12:1998;185-197.
9. Labenz, J. and O'Morain, C. (1995) Eradication. In: The Year in Helicobacter pylori 1995 (Malfertheiner, P., Mégraud, F.M., Michetti, P. and Price, A., Eds.), pp. 47-51. Current Science, Philadelphia, PA.
10. Logan R.P. Adherence of Helicobacter pylori. Aliment. Pharmacol. Ther. 10:(Suppl. 1):1996;3-15.
11. Clyne M., Drumm B. Adherence of Helicobacter pylori to primary human gastrointestinal cells. Infect. Immun. 61:1993;4051-4057.
12. Segal E.D., Falkow S., Tompkins L.S. Helicobacter pylori attachment to gastric cells induces cytoskeletal rearrangements and tyrosine phosphorylation of host cell proteins. Proc. Natl. Acad. Sci. USA. 93:1996;1259-1264.
13. Smoot D.T., Resau J.H., Naab T., Desbordes B.C., Gilliam T., Bull-Henry K., Curry S.B., Nidiry J., Sewchand J., Mills-Robertson K. Adherence of Helicobacter pylori to cultured human gastric epithelial cells. Infect. Immun. 61:1993;350-355.
14. Dytoc M., Gold B., Louie M., Huesca M., Fedorko L., Crowe S., Lingwood C., Brunton J., Sherman P. Comparison of Helicobacter pylori and attaching-effacing Escherichia coli adhesion to eukaryotic cells. Infect. Immun. 61:1993;448-456.
15. Finlay B.B., Falkow S. Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61:1997;136-169.
16. Segal E.D. Consequences of attachment of Helicobacter pylori to gastric cells. Biomed. Pharmacother. 51:1997;5-12.
17. Noach L.A., Rolf T.M., Tytgat G.N. Electron microscopic study of association between Helicobacter pylori and gastric and duodenal mucosa. J. Clin. Pathol. 47:1994;699-704.
18. Wyle F.A., Tarnawski A., Schulman D., Dabros W. Evidence for gastric mucosal invasion by C. pylori: an ultrastructural study. J. Clin. Gastroenterol. 12:1990;S92-S98.
19. Bode G., Malfertheiner P., Ditschuneit H. Pathogenetic implications of ultrastructural findings in Campylobacter pylori related gastroduodenal disease. Scand. J. Gastroenterol. 142:(Suppl.):1988;25-39.
20. Bode G., Malfertheiner P., Ditschuneit H. Invasion of Campylobacter-like organisms in the duodenal mucosa in patients with active duodenal ulcer. Klin. Wochenschr. 65:1987;144-146.
21. Papadogiannakis N., Willén R., Carlén B., Sjöstedt S., Wadström T., Gad A. Modes of adherence of Helicobacter pylori to gastric surface epithelium in gastroduodenal disease: A possible sequence of events leading to internalisation. APMIS. 108:2000;439-447.
22. Ko G.H., Kang S.M., Kim Y.K., Lee J.H., Park C.K., Youn H.S., Baik S.C., Cho M.J., Lee W.K., Rhee K.H. Invasiveness of Helicobacter pylori into human gastric mucosa. Helicobacter. 4:1999;77-81.
23. Meyrick-Thomas J., Poynter D., Goodling C., Woodings D.F., Selway S., Cook A.R., et al. Gastric spiral bacteria. Lancet. ii:1984;100.
24. Buck G.E., Gourley W.K., Lee W.K., Subramanyan K.A., Latimer J.M. Relation of Campylobacter pyloridis to gastritis and peptic ulcer. J. Infect. Dis. 153:1986;664-669.
25. Lee W.K., Gourley W.K., Buck G.E., Subramanyan K.A. A light and electron microscopic study of a Campylobacter-like bacteria inhabiting the human stomach. Gastroenterology. 88:1985;1470.
26. Tricottet V., Bruneval P., Vire O., Camilleri J.P. Campylobacter-like organisms and surface epithelium abnormalities in active, chronic gastritis in humans: an ultrastructural study. Ultrastruct. Pathol. 10:1986;113-122.
27. Kazi J.L., Sinniah R., Zaman V., Ng M.L., Jafarey N.A., Alam S.M., Zuberi S.J., Kazi A.M. Ultrastructural study of Helicobacter pylori-associated gastritis. J. Pathol. 161:1990;65-70.
28. Neri M., Susi D., Bovani I., Laterza F., Porreca E., Cuccurullo F. Gastric mucosal infiltration by Helicobacter pylori favours bacterial survival after treatment. Aliment. Pharmacol. Ther. 10:1996;181-185.
29. Neri M., Susi D., Bovani I., Laterza F., Mezzetti A., Cuccurullo F. Bacterial mucosal infiltration in Helicobacter pylori associated gastritis: histological and clinical consequences. Am. J. Gastroenterol. 89:1994;1801-1805.
30. Chan W.Y., Hui P.K., Leung K.M., Thomas T.M. Modes of Helicobacter colonization and gastric epithelial damage. Histopathology. 21:1992;521-528.
31. Engstrand L., Graham D., Scheynius A., Genta R.M., El-Zaatari F. Is the sanctuary where Helicobacter pylori avoids antibacterial treatment intracellular? Am. J. Clin. Pathol. 108:1997;504-509.
32. Kang J.K., Kim E., Kim K.H., Oh S.H. Association of Helicobacter pylori with gastritis and peptic ulcer diseases. Yonsei Med. J. 32:1991;157-168.
33. Jones, D.M. and Curry, A. (1992) The ultrastructure of Helicobacter pylori. In: Helicobacter pylori and Gastroduodenal Disease (Rathbone, B.J. and Heatley, R.V., Eds.), pp. 29-41. Blackwell Scientific, Oxford.
34. Hazell S.L., 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. 153:1986;658-663.
35. Thomsen L.L., Gavin J.B., Tasman-Jones C. Relation of Helicobacter pylori to the human gastric mucosa in chronic gastritis of the antrum. Gut. 31:1990;1230-1236.
36. Sirigu F., Capeccioni P.S., Dessi A., Usai P. Morphological study of the gastric antral mucosa colonized by Campylobacter pylori. Ital. J. Gastroenterol. 22:1990;22-23.
37. Hessey S.J., Spencer J., Wyatt J.I., Sobala G., Rathbone B.J., Axon A.T., Dixon M.F. Bacterial adhesion and disease activity in Helicobacter associated chronic gastritis. Gut. 31:1990;134-138.
38. Chen X.G., Correa P., Offerhaus J. Ultrastructure of the gastric mucosa harboring Campylobacter-like organisms. Am. J. Clin. Pathol. 86:1986;575-582.
39. Rollason T.P., Stone J., Rhodes J.M. Spiral organisms in endoscopic biopsies of the human stomach. J. Clin. Pathol. 37:1984;23-26.
40. Jiang S.J., Liu W.Z., Zhang D.Z. Campylobacter-like organisms in chronic gastritis, peptic ulcer, and gastric carcinoma. Scand. J. Gastroenterol. 22:1987;553-558.
41. Ogata T. Duodenal and gastric cell regenerating epithelia on margins of human duodenal ulcer and presence of H. pylori - an electron microscopic study. Histol. Histopathol. 12:1997;57-68.
42. Chlumska A., Sedlackova M. Ultrastructural findings in the gastric mucosa in children and adolescents with chronic Helicobacter pylori-positive gastritis. Cesk. Patol. 31:1995;119-121.
43. Taniguchi Y., Kimura K., Satoh K., Yoshida Y., Kihira K., Takimoto T., Saifuku K., Ido K., Ookawara S., Mato M. Helicobacter pylori detected deep in gastric glands: an ultrastructural quantitative study. J. Clin. Gastroenterol. 21:1995;S169-S173.
44. el Shoura S.M. Helicobacter pylori: I. Ultrastructural sequences of adherence, attachment, and penetration into the gastric mucosa. Ultrastruct. Pathol. 19:1995;323-333.
45. Andersen L.P., Holck S. Possible evidence of invasiveness of Helicobacter pylori. Eur. J. Clin. Microbiol. Infect. Dis. 9:1990;135-138.
46. Mai U.E., Perez-Perez G.I., Allen J.B., Wahl S.M., Blaser M.J., Smith P.D. Surface proteins from Helicobacter pylori exhibit chemotactic activity for human leukocytes and are present in gastric mucosa. J. Exp. Med. 175:1992;517-525.
47. Morozov I.A. Possibility of Helicobacter pylori invasion into the lamina propria of the gastric mucosa. Arkh. Patol. 56:1994;19-22.
48. Price A.B. Histological aspects of Campylobacter pylori colonization and infection of gastric and duodenal mucosa. Scand. J. Gastroenterol. 23:1988;22-24.
49. Wyle F.A., Tarnawski A., Dabros W., Gergely H. Campylobacter pylori interactions with gastric cell tissue culture. J. Clin. Gastroenterol. 12:(suppl 1):1990;S99-S103.
50. Rautelin H., Kihlstrom E., Jurstrand M., Danielsson D. Adhesion to and invasion of HeLa cells by Helicobacter pylori. Int. J. Med. Microbiol. Virol. Parasitol. Infect. Dis. 282:1995;50-53.
51. Evans D.G., Evans D.J. Jr., Graham D.Y. Adherence and internalization of Helicobacter pylori by HEp-2 cells. Gastroenterology. 102:1992;1557-1567.
52. Birkness K.A., Gold B.D., White E.H., Bartlett J.H., Quinn F.D. In vitro models to study attacment and invasion of Helicobacter pylori. Ann. NY Acad. Sci. 797:1996;293-295.
53. Wilkinson S.M., Uhl J.R., Kline B.C., Cockerill F.R. Assessment of invasion frequencies of cultured HEp-2 cells by clinical isolates of Helicobacter pylori using an acridine orange assay. J. Clin. Pathol. 51:1998;127-133.
54. Petersen A.M., Blom J., Andersen L.P., Krogfelt K.A. Role of strain type, AGS cells and fetal calf serum in Helicobacter pylori adhesion and invasion assays. FEMS Immunol. Med. Microbiol. 29:2000;59-67.
55. Pucciarelli M.G., Finlay B.B. Polarized epithelial monolayers: Model systems to study bacterial interactions with host epithelial cells. Methods Enzymol. 236:1994;438-447.
56. Corthesy-Theulaz I., Porta N., Pringault E., Racine L., Bogdanova A., Kraehenbuhl J.P., Blum A.L., Michetti P. Adhesion of Helicobacter pylori to polarized T84 human intestinal cell monolayers is pH dependent. Infect. Immun. 64:1996;3827-3832.
57. Su B., Johansson S., Fallman M., Patarroyo M., Granstrom M., Normark S. Signal transduction-mediated adherence and entry of Helicobacter pylori into cultured cells. Gastroenterology. 117:1999;595-604.
58. Cooper J. Effects of cytochalasin and phalloidin on actin. J. Cell Biol. 105:1987;1473-1478.
59. Young V.B., Falkow S., Schoolnik G.K. The invasin proteins of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J. Cell Biol. 116:1992;197-207.
60. Finlay B.B., Ruschkowski S., Dedhar S. Cytoskeletal rearrangements accompanying Salmonella entry into epithelial cells. J. Cell Sci. 99:1991;283-296.
61. Small P.L.C., Isberg R.P., Falkow S. Comparison of the ablility of enteroinvasive Escherichia coli, Salmonella typhimurium, Yersinia pseudotuberculosis and Yersinia enterocolitica to enter and replicate within HEp-2 cells. Infect. Immun. 55:1987;1674-1679.
62. Konkel M.E., Joens L.A. Adhesion to and invasion of HEp-2 cells by Campylobacter spp. Infect. Immun. 57:1989;2984-2990.
63. Finlay, B.B. and Falkow, S. (1988) A comparison of microbial invasion strategies of Salmonella, Shigella and Yersinia species. In: Bacteria-Host Cell Interaction (Horwitz, M.A., Ed.), pp. 227-243. Liss, New York.
64. Sansonetti P.J., Ryter A., Clerc P., Maurelli A.T., Mournier J. Multiplication of Shigella flexneri within HeLa cells: Lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun. 51:1986;461-469.
65. Barrow P.A., Lovell M.A. Invasion of Vero cells by Salmonella species. J. Med. Microbiol. 28:1989;59-67.
66. Petersen A.M., Sørensen K., Blom J., Krogfelt K.A. Reduced intracellular survival of H. pylori vacA mutants in comparison with their wild-types indicates the role of VacA in pathogenesis. FEMS Immunol. Med. Microbiol. 30:2001;103-108.
67. Petersen A.M., Fussing V., Colding H., Blom J., Nørgaard A., Andersen L.P., Krogfelt K.A. Phenotypic and genotypic characterization of Helicobacter pylori from patients with and without peptic ulcer disease. Scand. J. Gastroenterol. 35:2000;359-367.
68. Kenny B., Lai L.C., Finlay B.B., Donnenberg M.S. EspA, a protein secreted by enteropathogenic Escherichia coli, is required to induce signals in epithelial cells. Mol. Microbiol. 20:1996;313-323.
69. Riley L.W., Junio L.N., Schoolnik G.K. HeLa cell invasion by a strain of enteropathogenic Escherichia coli that lacks the O-antigenic polysaccharide. Mol. Microbiol. 4:1990;1661-1666.
70. Mauel J. Mechanisms of intracellular microbicide. Bull. Eur. Physiopathol. Respir. 19:1983;115-122.
71. Spiegelhalder C., Gerstenecker B., Kersten A., Schiltz E., Kist M. Purification of Helicobacter pylori superoxide dismutase and cloning and sequencing of the gene. Infect. Immun. 61:1993;5315-5325.
72. Pesci E.C., Cottle D.L., Pickett C.L. Genetic, enzymatic, and pathogenic studies of the iron superoxide dismutase of Campylobacter jejuni. Infect. Immun. 62:1994;2687-2694.
73. Papini E., de Bernard M., Milia E., Bugnoli M., Zerial M., Rappuoli R., Montecucco C. Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc. Natl. Acad. Sci. USA. 91:1994;9720-9724.
74. Bjorkholm B., Zhukhovitsky V., Lofman C., Hulten K., Enroth H., Block M., et al. Helicobacter pylori entry into human gastric epithelial cells: A potential determinant of virulence, persistence, and treatment failures. Helicobacter. 5:2000;148-154.
75. Andersen L.P., Blom J., Nielsen H. Survival and ultrastructural changes of Helicobacter pylori after phagocytosis by human polymorphnuclear leukocytes and monocytes. APMIS. 101:1993;61-72.
76. Peterson P.K., Verhoef J., Schmeling D., Quie P.G. Kinetics of phagocytosis and bacterial killing by human polymorphonuclear lecocytes and moncytes. J. Infect. Dis. 136:1977;502-509.
77. Allen L.A., Schlesinger L.S., Kang B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med. 191:2000;115-128.
78. Hultén K., Hjelm E., Cars O., Engstrand L. In vitro activity of azithromycin against intracellular Helicobacter pylori. J. Antimicrob. Chemother. 37:1996;483-489.
79. Odenbreit S., Gebert B., Puls J., Fischer W., Haas R. Interaction of Helicobacter pylori with professional phagocytes: role of the CAG pathogenecity island and translocation, phosphorylation and processing of CAG A. Cell Microbiol. 3:2001;21-31.
80. Gomez-Duarte O.G., Dehio M., Guzman C.A., Gursharan S.C., Dehio C., Meyer T.F. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect. Immun. 65:1997;3857-3866.
81. Duensing T.D., Van Putten J.P. Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect. Immun. 65:1997;964-970.
82. Cue D.R., Cleary P.P. High-frequency invasion of epithelial cells by Streptococcus pyogenes can be activated by fibrinogen and peptides containing the sequence RGD. Infect. Immun. 65:1997;2759-2764.
83. Duensing T.D., Wing J.S., Van Putten J.P. Sulfated polysaccharide-directed recruitment of mammalian host proteins: A novel strategy in microbial pathogenesis. Infect. Immun. 67:1999;4463-4468.