Helicobacter pylori: Focus on CagA and VacA major virulence factors

Salud Publica de Mexico

Volumn 46, Issue 6, 2004, Pages 538-548

  Castillo Rojas, Gonzalo ^a   Mazarí Hiriart, Marisa ^b   López Vidal, Yolanda ^a,c  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO DE ECOLOGÍA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Helicobocter pylori; Pathogenesis; Virulence factors

Indexed keywords

CAGA PROTEIN; VACUOLATING TOXIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL INFECTION; BACTERIAL VIRULENCE; HELICOBACTER PYLORI; HUMAN; NONHUMAN; PATHOGENESIS; PEPTIC ULCER; STOMACH ULCER;

EID: 11844273886     PISSN: 00363634     EISSN: None     Source Type: Journal    
DOI: 10.1590/S0036-36342004000600010     Document Type: Article

References (90)

1. Warren R. Discovery and Pathology of Helicobacter pylori. Xth International Workshop on Gastroduodenal Pathology and Helicobacter pylori; 1997 September 12-14; Lisboa, Portugal.
2. th World Congress of Gastroenterology; 1994 October 2-7; Los Angeles, California.
3. Mobley HLT. Defining Helicobacter pylori as a Pathogen: Strain heterogeneity and virulence. Am J Med 1996; 100:S2-S11.
4. Jerris RC, Helicobacter. En: Murray PR, Barron JE, Pfaller MA, Tenover FC, Yolken RH, ed. Manual of clinical microbiology. 6th Edition. Washington, DC:ASM Press; 1995:492-498,
5. Group 2. Aerobic/microaerophilic, motile, helical/vibrioid Gram-negative bacteria. Genus helicobacter. En: Holt JG, Krieg NR, Sneath PHA, Staley JT. Williams ST, ed. Bergey's manual of determinative Bacteriology, Ninth Edition. Baltimore (MD): Williams and Wilkins. 1994:42-43,62.
6. Cave DR. Epidemiology and transmission of Helicobacter pylori infection. How is Helicobacter pylori transmitted? Gastroenterology 1997;113;S9-S14.
7. Everhart JE, Kruszon-Moran D, Pérez-Pérez GJ, Tralka TS, McQuillan G. Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis 2000;181:1359-1363.
8. Torres J, Leal-Herrera Y, Pérez-Pérez G, Gómez A, Camorlinga-Ponce M, Cedillo-Rivera R et et al. A community-based seroepidemiologic study of Helicobacter pylori infection in Mexico. J Infect Dis 1998;178: 1089-1094.
9. Dubois A, Berg DE, Incecik ET, Fiala N, Heman-Ackah LM, Pérez-Pérez GI et al. Transient and persistent infection of nonhuman primates with Helicobacter pylori: Implications for human disease. Infect Immun 1996;64:2885-2891.
10. Mitchell HM. Epidemiology of infection. En: Mobley HLT, Méndez GL, Hazell SL, ed. Helicobacter pylori: Physiology and genetics. Washington, DC:ASM Press; 2001:7-18.
11. Mazari-Hiriart M, López-Vidal Y, Calva JJ. Helicobacter pylori in water systems for human use in Mexico City. Water Sci Technol 2001;43: 93-98.
12. Mazari-Hiriart M, López-Vidal Y, Castillo-Rojas G, Ponce de León S, Cravioto A. Helicobacter pylori and other enteric bacteria in freshwater environments in Mexico City. Arch Med Res 2001;32:458-467.
13. Hegarty JP, Dowd MT, Baker KH. Occurrence of Helicobacter pylori in surface water in the United States. J Appl Microbiol 1999;87:697-701.
14. Klein PD, Gastrointestinal Physiology Working Group, Graham DY, Gaillour A, Opekun AR, Smith EO. Water source as risk for Helicobacter pylori infection in Peruvian children. Lancet 1991;337:1503-1506.
15. Hulten K, Han SW, Enroth H, Klein PD, Opekun AR, Gilman RH et al. Helicobacter pylori in drinking water in Peru. Gastroenterol 1996;110:1031-1035.
16. Goodman KJ, Correa P, Tengana-Aux HJ, Ramírez H, DeLany JP, Guerrero Pepinosa O et al. Helicobocter pylori infection in the Colombian Andes:A population-based study of transmission pathways. Am J Epidemiol 1996;144:290-299.
17. Hopkins RJ, Vial PA, Ferreccio C, Ovalle J, Prado P, Sotomayor V et al. Seroprevalence of Helicobacter pylori in Chile: Vegetables may serve as one route of transmission. J Infect Dis 1993; 168:222-226.
18. Hultén K, Enroth H, Nyström T, Engstrand L. Presence of Helicobacter species DNA in Swedish water. J Appl Microbiol 1998;85:282-286.
19. Mazari-Hiriart M, López-Vidal Y, Ponce de León S, Calva-Mercado JJ, Rojo-Callejas F. Significance of water quality indicators: A case study in Mexico City. Proceedings of the International Conference: Water and Wastewater, Perspectives of Developing Countries. New Delhi, India: Indian Institute of Technology Delhi-International Water Association; 2002:407-416.
20. Cover T, Blaser JM. Helicobacter pylori: A bacteria cause of gastritis, peptic ulcer disease and gastric cancer. ASM News 1995;61:21-26.
21. Atherton JC, Tham KT, Peek RM, Cover TI, Blaser MJ. Density of Helicobacter pylori infection in vivo as assessed by quantitative culture and histology. J Infect Dis 1996;174:552-556.
22. Blaser MJ, Pérez-Pérez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH et al. Infection with Helicobacter pylori strains possessing CagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 1995;55:2111-2115.
23. Parkin DM, Bray FI, Devesa SS. Cancer burden in the year 2000: The global picture. Eur J Cancer 2002;37:S4-S66.
24. Guarner J, Mohar A, Parsonnet J, Halperin D. The association of Helicobacter pylori with gastric cancer and pre-neoplastic gastric lesions in Chiapas, Mexico. Cancer 1993;71:297-301.
25. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001;345:784-789.
26. Dunn BE, Campbell GP, Pérez-Pérez GI, Blazer MJ. Purification and characterization of urease from Helicobacter pylori. J Biol Chem 1990;265:9464-9469.
27. Austin JW, Doig P, Stewart M. Trust TJ. Macromolecular structure and aggregation state of Helicobacter pylori urease. J Bacteriol 1991;173:5663-5667.
28. Labigne A, Cussac V, Courcoux P. Shuttle cloning and nucleotide sequences of Helicobacter pylori genes responsible for urease activity. J Bacteriol 1991;173:1920-1931.
29. Ferrero RL, Cussac V, Courcoux P, Labigne A. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol 1992;174:4212-4217.
30. 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;62:3586-3589.
31. Eaton KA, Krakowka S. Effect of gastric pH on urease-dependent colonization of gnotobiotic piglets by Helicobacter pylori. Infect Immun 1994;62:3604-3607.
32. Berg D, Hoffman P, Appelmelk B, Kusters J. The Helicobacter pylori genome sequence: genetic factors for long life in the gastric mucosa. Trends Microbiol 1997;5:468-473.
33. Ricci V, Sommi P, Fiocca R, Romano M, Solcia E, Ventura U. Helicobacter pylori vacuolating toxin accumulates within the endosomal-vacuolar compartment of cultured gastric cells and potentates the vacuolating activity of ammonia. J Pathol 1997;183:453-459.
34. Eaton KA, Morgan DR, Krakowka S. Motility as a factor in the colonization of gnotobiotic piglets by Helicobacter pylori. J Med Microbiol 1992;37:123-127.
35. Geis G, Suerbaum S, Forsthoff B, Leying H, Opferkuch W. Ultrastructure and biochemical studies of the flagellar sheath of Helicobocter pylori. J Med Microbiol 1993;38:371-377.
36. Josenhans C, Labigne A, Suerbaum S. Comparative ultraestructural and functional studies of Helicofaocter pylori and Helicofaocter mustelae flagellin mutants: Both flagellin subunits, FlaA and FlaB, are necessary for full motility in Helicobacter species. J Bacteriol 1995;177:3010-3020.
37. Eaton KA, Suerbaum S, Josenhans C, Krakowka S. Colonization of gnotobiotic piglets by Helicobaccter pylori deficient in two flagellin genes. Infect Immun 1996;64:2445-2448.
38. Dubreuil JD, Giudice GD, Rappuoli R. Helicobacter pylori interactions with host serum and extracellular matrix proteins: Potential role in the infectious process. Microbiol Mol Biol Rev 2002;66:617-629.
39. Guruge JL, Falk PG, Lorenz RG, Dans M, Wirth HP, Blaser MJ et al. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc Natl Acad Sci 1998;95:3925-3930.
40. Hennig EE, Mernaugh R, Edl J, Cao P, Cover TL. Heterogeneity among Helicobacter pylori Strains in expression of the outer membrane protein BabA. Infect Immun 2004;72:3429-3435.
41. Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, Roche N et al. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002;297:573-578.
42. Kronvall G, Jönson K. Receptins: A novel term for an expanding spectrum of natural and engineered microbial proteins with binding properties for mammalian protein. J Mol Recognit 1999;12:38-44.
43. Simoons-Smit IM, Appelmelk BJ, Verboom T, Negrini R, Penner JL, Aspinall GO et al. Typing of Helicobacter pylori with monoclonal antibodies against Lewis antigens in lipopolysaccharide. J Clin Microbiol 1996;34:2196-2200.
44. Abdulhamid M, Alkout M, Blackwell CC, Weir DM. Increased inflammatory responses of persons of blood group O to Helicobacter pytori. J Infect Dis 2000;181:1364-1369.
45. Aspinall GO, Monteiro MA. Lipopolysaccharides of Helicobacter pylori strains P466 and MO19: structures of the O antigen and core oligosaccharide strains. Biochemistry 1996;35:2498-2504.
46. Appelmelk BJ, Martino MC, Veenhof E, Monteiro MA, Maaskant JJ, Negrini R et al. Phase variation in H type I and Lewis a epitopes of Helicobacter pylori lipopolysaccharide. Infect Immun 2000;68:5928-5932.
47. Monteiro MA, Chan KH, Rasko DA Taylor DE, Zheng PY, Appelmelk BJ et al. Simultaneous expression of type I and type 2 Lewis blood group antigens Helicobacter pylori lipopolysaccharides. J Biol Chem 1998;273:11533-11543.
48. Moran AP, Prendergast MM, Appelmelk BL. Molecular mimicry of host structure by bacterial lipopolysaccharides and contribution to disease. FEMS Immunol Med Microbiol 1996;16:105-115.
49. Takata T, El-Omar E, Camorlinga M, Thompson SA, Minohara Y, Ernst PB et al. Helicobocter pylori does not require Lewis X or Lewis Y expression to colonize C3H/HeJ mice. Infect Immun 2002;70: 3073-3079.
50. Negrini R, Lisato L, Zanella I, Cavazzini L, Gullini S. Villanacci V et al Helicobacter pylori infection induced antibodies cross reacting with human gastric mucosa. Gastroenterology 1991;101:437-439.
51. Tummuru MKR, Cover TL, Blaser MJ. Cloning and expression of a high-molecular-mass major antigen of Helicobocter pylori: Evidence of linkage to cytotoxin production. Infect Immun 1993;61:1799-1809.
52. Xiang Z, Censini S, Bayeli PF, Telford JL, Figura N, Rappuoli R et al. Analysis of expression of CagA and VacA virulence factors in 43 strains of Helicobacter pylori reveals that clinical isolates can be divided into two mayor types and that CagA is not necessary for expression of the vacuolating toxin. Infect Immun 1995;63:94-98.
53. Tummuru MKR, Cover TL, Blaser MJ. Mutation of the cytotoxin-associated CagA gene does not affect the vacuolating cytotoxin activity of Helicobacter pylori. Infect Immun 1994;62:2609-2613.
54. Telford JL, Covacci A, Ghiara P, Montecucco C, Rappuoli R. Unravelling the pathogenic role of Helicobacter pylori in peptic ulcer: Potential new therapies and vaccines. TIBTECH 1993;12:420-425.
55. Evans DJ, Queiroz DMM, Mendes EN, Evans DG. Diversity in the variable region of Helicobacter pylori CagA gene involves more than simple repetition of a 102-nucleotide sequence. Biochem Biophys Res Commun 1998;245:780-784.
56. Yamaoka Y, Kodama T, Kashima K, Graham DY, Sepúlveda AR. Variants of the 3′ region of the CagA gene in Helicobacter pylori isolates from patients with different H. pylori-associated diseases. J Clin Microbiol 1998;36:2258-2263.
57. Yamaoka Y, El-Zimaity HMT, Gutiérrez O, Figura N, Kim JK, Kodama T et al. Relationship between the CagA 3′ repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology 1999;117:342-349.
58. Azuma T, Yamakama A, Yamazaki S, Fukuta K, Ohtani M, Ito Y et al. Correlation between variation of the 3′ region of the CagA gene in Helicobacter pylori and disease outcome in Japan. J Infect Dis 2002;186:1621-1630.
59. Censini S, Lange C, Xiang Z, Crabtree JE, Ghiara P, Borodovsky M et al. Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci 1996;93:14648-14653.
60. Alm RA, Ling LS, Moir DT, King BL, Brown ED, Doig PC et al. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999;397:176-180.
61. Christie JP, Vogel JP. Bacterial type IV secretion: Conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 2000;8:354-360.
62. Segal ED, Falkow S, Tompkins LS. Helicobacter pylori attachment to gastric cells induces cytoskeletal rearrangements and tyrosine phosphorylation of host cell proteins. Proc Natl Acad Sci 1996;93: 1259-1264.
63. Stein M, Rappuoli R, Covacci A. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci 2000;97:1263-1268.
64. Dundon WG, De Bernard M, Montecucco C. Virulence factors of Helicobacter pylori, Int J Med Microbiol 2001;290:647-658.
65. Covacci A, Rappuoli R. Tyrosine-phosphorylated bacterial proteins: Trojan horses for the host cell. J Exp Med 2000;191:587-592.
66. Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, Falkow S. Disruption of the epithelial apical-junctional complex by Helicobater pylori CagA. Science 2003;300:1430-1434.
67. Backert S, Moese S, Selbach M, Brinkmann V, Meyer TF. Phosphorylation of tyrosine 972 of the Helicobater pylori CagA protein is essential for induction of a scattering phenotype in gastric epithelial cells. Mol Microbiol 2001;42:631-644.
68. Stein M, Bagnoli F, Halenbeck R, Rappuoli R, Fantl WJ, Covacci A. C-Src/Lyn kinase activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol 2002;43:971-980.
69. Pan ZJ, Van der Hulst RW, Feller M, Xiao SD, Tytgat GN, Dankert J et al. Equally high prevalences of infection with CagA-positive Helicobacter pylori in Chinese patients with peptic ulcer disease and those with chronic gastritis-associated dyspepsia. J Clin Microbiol 1997;35: 1344-1347.
70. Van der Ende A, Pan ZJ, Bart A, Van der Hulst RW, Feller M, Xiao SD et al. CagA-positive Helicobacter pylori populations in China and the Netherlands are distinct. Infect Immun 1998;66:1822-1826.
71. Higashi H. Tsutsumi R, Fujita A, Yamazaki S, Asaka M, Azuma T et al. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci 2002;99:14428-14433.
72. Catrenich C, Chestnut M. Character and origin of vacuoles induced in mammalian cells by the cytotoxin of Helicobacter pylori. J Med Microbiol 1992;37:389-395.
73. Harris PR, Cover TL. Crowe DR, Orenstein JM, Graham MF, Blaser MJ et al. Helicobacter pylori cytotoxin induces vacuolation of primary human mucosal epithelial cell. Infect Immun 1996;64:4867-4871.
74. Telford J, Ghiara P, Dell'Orco M, Comanducci M, Burroni D, Bugnoli M. Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J Exp Med 1994;179:1653-1658.
75. Tummuru M, Cover T, Blaser M. Cloning and expression of high molecular weight major antigen of Helicobacter pylori: Evidence of linkage to cytotoxin production. Infect Immun 1993;61:1799-1809.
76. Atherton J, Cao P, Peek R, Tummuru M, Blaser M, Cover T. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. J Biol Chem 1995;270:17771-17777.
77. Garner J, Cover T. Analysis of genetic diversity in cytotoxin-producing and non-cytotxin-producing Helicobter pylori strains. J Infect Dis 1995;172:290-293.
78. Van Doom LJ, Figueiredo C, Sanna R, Pena S, Midolo P, Ng EK et al. Expanding allelic diversity of Helicobacter pylori VacA. J Clin Microbiol 1998;36:2597-2603.
79. Strobel S, Bereswill S, Balig P, Allgaier P, Sonntag HG, Kist M. Identification and analysis of a new VacA genotype variant of Helicobacter pylori in different patient groups in Germany. J Clin Microbiol 1998;36:1285-1289.
80. Huseyin S, Salih BA. Yamaoka Y, Sander E. Analysis of Helicobacter pylori genotypes and correlation with clinical outcome in Turkey J Clin Microbiol 2004;42:1648-1651.
81. Morales-Espinosa R, Castillo-Rojas G, Ponce de Leon S, Cravioto A, Atherton JC, Lopez-Vidal Y. Colonization of Mexican patients by multiple Helicobacter pylori strains with different VacA and CagA genotypes. J Clin Microbiol 1999;37:3001-3004.
82. Moll G, Papini E, Colonna R, Burroni D, Telford J, Rappuoli R et al. Lipid interaction of the 37-kDa and 58-kDa fragments of the Helicofaocter pylori cytotoxin. Eur J Biochem 1995;234:947-952.
83. Lanzavecchia S, Bellon PL.Three-dimensional reconstruction of metal replicas of the Helicobacter pylori vacuolating cytotoxin. J Struct Biol 1998;121:9-18.
84. Seto K, Hayashi-Kuwabara Y, Yoneta T, Suda H. Tamaki H. Vacuolation induced by cytotoxin from Helicobacter pylori is mediated by the EGF receptor in HeLa cell. FEBS Lett 1998;431:347-350.
85. Yahiro K, Niidome T, Hatakeyama T, Aoyagi H, Kurazono H, Padilla PI et al. Helicobacter pylori vacuolating cytotoxin binds to the 140-kDa protein in human gastric cancer cell linesAZ-521 and AGS. Biochem Biophys Res Commun 1997;238:629-632.
86. Papini E, De Bernard M. Milia E, Bugnoli M. Zerial M, Rappuoli R et al. Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Nat Acad Sci 1994;91:9720-9724.
87. Papini E, Gottardi E, Satin B, De Bernard M, Massari P. Telford J et al. The vacuolar ATPase proton pump is present on intracellular vacuoles induced by Helicobacter pylori. J Med Microbiol 1996;45:84-89.
88. Tombola F, Carlesso C, Szabo I, De Bernard M, Reyrat JM, Telford JL et al. Helicobacter pylori vacuolating toxin forms anion-selective channels in planar lipid bilayers: Possible implications for the mechanism of cellular vacuolation. Biophys J 1999;76:1401-1409.
89. Blaser MJ, Atherton JC. Helicobacter pylori persistence: Biology and disease. J Clin Invest 2004;113:321-333.
90. Weel JF, Van der Hulst RW, Gerrits Y, Roorda P, Feller M, Dankert J et al. The interrelationship between cytotoxin-assodated gene A, vacuolating cytotoxin, and Helicobcter pylori-related diseases. J Infect Dis 1996;173:1171-1175.