The significance of virulence factors in Helicobacter pylori

Journal of Digestive Diseases

Volumn 14, Issue 7, 2013, Pages 341-349

  Shiota, Seiji ^a   Suzuki, Rumiko ^a   Yamaoka, Yoshio ^a,b  

^a OITA UNIVERSITY   (Japan)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Helicobacter pylori; Stomach neoplasms; Virulence factor

Indexed keywords

BABA PROTEIN; BACTERIAL PROTEIN; BACTERIUM ANTIBODY; CAGA PROTEIN; DUPA PROTEIN; ICEA PROTEIN; OIPA PROTEIN; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VACUOLATING TOXIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; GENE EXPRESSION; GENE LOCUS; GENE SEQUENCE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; META ANALYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; TYPE IV SECRETION SYSTEM;

BACTERIAL PROTEINS; GENES, BACTERIAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; STOMACH NEOPLASMS; VIRULENCE; VIRULENCE FACTORS;

EID: 84878415544     PISSN: 17512972     EISSN: 17512980     Source Type: Journal    
DOI: 10.1111/1751-2980.12054     Document Type: Article

References (78)

1. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002; 347: 1175-1186.
2. Kusters JG, van Vliet AH, Kuipers EJ. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 2006; 19: 449-490.
3. Goh KL, Chan WK, Shiota S, Yamaoka Y. Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter 2011; 16 Suppl 1: 1-9.
4. Yamaoka Y. Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 2010; 7: 629-641.
5. Censini S, Lange C, Xiang Z etal. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 1996; 93: 14648-14653.
6. Asahi M, Azuma T, Ito S etal. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J Exp Med 2000; 191: 593-602.
7. Backert S, Selbach M. Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 2008; 10: 1573-1581.
8. Shimoyama T, Fukuda S, Tanaka M, Mikami T, Munakata A, Crabtree JE. CagA seropositivity associated with development of gastric cancer in a Japanese population. J Clin Pathol 1998; 51: 225-228.
9. Yamaoka Y, Kodama T, Kashima K, Graham DY. Antibody against Helicobacter pylori CagA and VacA and the risk for gastric cancer. J Clin Pathol 1999; 52: 215-218.
10. Shiota S, Matsunari O, Watada M, Yamaoka Y. Serum Helicobacter pylori CagA antibody as a biomarker for gastric cancer in east-Asian countries. Future Microbiol 2010; 5: 1885-1893.
11. Hatakeyama M. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat Rev Cancer 2004; 4: 688-694.
12. Vilaichone RK, Mahachai V, Tumwasorn S, Wu JY, Graham DY, Yamaoka Y. Molecular epidemiology and outcome of Helicobacter pylori infection in Thailand: a cultural cross roads. Helicobacter 2004; 9: 453-459.
13. Yamaoka Y, Kodama T, Kashima K, Graham DY, Sepulveda 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.
14. Yamaoka Y, Orito E, Mizokami M etal. Helicobacter pylori in North and South America before Columbus. FEBS Lett 2002; 517: 180-184.
15. Matsunari O, Shiota S, Suzuki R etal. Association between Helicobacter pylori virulence factors and gastroduodenal diseases in Okinawa, Japan. J Clin Microbiol 2012; 50: 876-883.
16. Truong BX, Mai VT, Tanaka H etal. Diverse characteristics of the CagA gene of Helicobacter pylori strains collected from patients from Southern Vietnam with gastric cancer and peptic ulcer. J Clin Microbiol 2009; 47: 4021-4028.
17. Xia Y, Yamaoka Y, Zhu Q, Matha I, Gao X. A comprehensive sequence and disease correlation analyses for the C-terminal region of CagA protein of Helicobacter pylori. PLoS ONE 2009; 4: e7736.
18. Suzuki M, Kiga K, Kersulyte D etal. Attenuated CagA oncoprotein in Helicobacter pylori from Amerindians in Peruvian Amazon. J Biol Chem 2011; 286: 29964-29972.
19. Kersulyte D, Kalia A, Gilman RH etal. Helicobacter pylori from Peruvian Amerindians: traces of human migrations in strains from remote Amazon, and genome sequence of an Amerind strain. PLoS ONE 2010; 5: e15076.
20. Shiota S, Matsunari O, Yamaoka Y. Relationship between J-Western CagA subtype and the vacA m2 region of Helicobacter pylori. J Clin Microbiol 2010; 48: 3033-3034.
21. Duncan SS, Valk PL, Shaffer CL, Bordenstein SR, Cover TL. J-Western forms of Helicobacter pylori cagA constitute a distinct phylogenetic group with a widespread geographic distribution. J Bacteriol 2012; 194: 1593-1604.
22. Matsuo Y, Shiota S, Matsunari O etal. Helicobacter pylori cagA 12-bp insertion can be a marker for duodenal ulcer in Okinawa, Japan. J Gastroenterol Hepatol 2013; 28: 291-296.
23. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol 2006; 1: 63-96.
24. Cover TL, Blanke SR. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 2005; 3: 320-332.
25. Atherton JC, Cao P, Peek RM Jr, Tummuru MK, Blaser MJ, Cover TL. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem 1995; 270: 17771-17777.
26. Cover TL, Blaser MJ. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 1992; 267: 10570-10575.
27. Leunk RD. Production of a cytotoxin by Helicobacter pylori. Rev Infect Dis 1991; 13 Suppl 8: S686-689.
28. Sugimoto M, Zali MR, Yamaoka Y. The association of vacA genotypes and Helicobacter pylori-related gastroduodenal diseases in the Middle East. Eur J Clin Microbiol Infect Dis 2009; 28: 1227-1236.
29. Sugimoto M, Yamaoka Y. The association of vacA genotype and Helicobacter pylori-related disease in Latin American and African populations. Clin Microbiol Infect 2009; 15: 835-842.
30. Nguyen TL, Uchida T, Tsukamoto Y etal. Helicobacter pylori infection and gastroduodenal diseases in Vietnam: a cross-sectional, hospital-based study. BMC Gastroenterol 2010; 10: 114.
31. Sahara S, Sugimoto M, Vilaichone RK etal. Role of Helicobacter pylori cagA EPIYA motif and vacA genotypes for the development of gastrointestinal diseases in Southeast Asian countries: a meta-analysis. BMC Infect Dis 2012; 12: 223.
32. Ogiwara H, Sugimoto M, Ohno T etal. Role of deletion located between the intermediate and middle regions of the Helicobacter pylori vacA gene in cases of gastroduodenal diseases. J Clin Microbiol 2009; 47: 3493-3500.
33. Rhead JL, Letley DP, Mohammadi M etal. A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region, is associated with gastric cancer. Gastroenterology 2007; 133: 926-936.
34. Jones KR, Jang S, Chang JY etal. Polymorphisms in the intermediate region of VacA impact Helicobacter pylori-induced disease development. J Clin Microbiol 2011; 49: 101-110.
35. Ogiwara H, Graham DY, Yamaoka Y. vacA i-region subtyping. Gastroenterology 2008; 134: 1267; author's reply 1268.
36. Lu H, Hsu PI, Graham DY, Yamaoka Y. Duodenal ulcer promoting gene of Helicobacter pylori. Gastroenterology 2005; 128: 833-848.
37. Hussein NR. The association of dupA and Helicobacter pylori-related gastroduodenal diseases. Eur J Clin Microbiol Infect Dis 2010; 29: 817-821.
38. Shiota S, Matsunari O, Watada M, Hanada K, Yamaoka Y. Systematic review and meta-analysis: the relationship between the Helicobacter pylori dupA gene and clinical outcomes. Gut Pathog 2010; 2: 13.
39. Shiota S, Nguyen LT, Murakami K etal. Association of Helicobacter pylori dupA with the failure of primary eradication. J Clin Gastroenterol 2012; 46: 297-301.
40. Kersulyte D, Lee W, Subramaniam D etal. Helicobacter pylori's plasticity zones are novel transposable elements. PLoS ONE 2009; 4: e6859.
41. Gomes LI, Rocha GA, Rocha AM etal. Lack of association between Helicobacter pylori infection with dupA-positive strains and gastroduodenal diseases in Brazilian patients. Int J Med Microbiol 2008; 298: 223-230.
42. Hussein NR, Argent RH, Marx CK, Patel SR, Robinson K, Atherton JC. Helicobacter pylori dupA is polymorphic, and its active form induces proinflammatory cytokine secretion by mononuclear cells. J Infect Dis 2010; 202: 261-269.
43. Queiroz DM, Rocha GA, Rocha AM etal. dupA polymorphisms and risk of Helicobacter pylori-associated diseases. Int J Med Microbiol 2011; 301: 225-228.
44. Takahashi A, Shiota S, Matsunari O etal. Intact long-type dupA as a marker for gastroduodenal diseases in Okinawan subpopulation, Japan. Helicobacter 2013; 18: 66-72.
45. Yamaoka Y. Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J Med Microbiol 2008; 57: 545-553.
46. Jung SW, Sugimoto M, Shiota S, Graham DY, Yamaoka Y. The intact dupA cluster is a more reliable Helicobacter pylori virulence marker than dupA alone. Infect Immun 2012; 80: 381-387.
47. van Doorn LJ, Figueiredo C, Sanna R etal. Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 1998; 115: 58-66.
48. Peek RM Jr, Thompson SA, Donahue JP etal. Adherence to gastric epithelial cells induces expression of a Helicobacter pylori gene, iceA, that is associated with clinical outcome. Proc Assoc Am Physicians 1998; 110: 531-544.
49. Xu Q, Morgan RD, Roberts RJ etal. Functional analysis of iceA1, a CATG-recognizing restriction endonuclease gene in Helicobacter pylori. Nucleic Acids Res 2002; 30: 3839-3847.
50. Yamaoka Y, Kodama T, Gutierrez O, Kim JG, Kashima K, Graham DY. Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol 1999; 37: 2274-2279.
51. Ito Y, Azuma T, Ito S etal. Sequence analysis and clinical significance of the iceA gene from Helicobacter pylori strains in Japan. J Clin Microbiol 2000; 38: 483-488.
52. Nishiya D, Shimoyama T, Fukuda S, Yoshimura T, Tanaka M, Munakata A. Evaluation of the clinical relevance of the iceA1 gene in patients with Helicobacter pylori infection in Japan. Scand J Gastroenterol 2000; 35: 36-39.
53. Maeda S, Amarsanaa J, Mitsuno Y etal. Relationship between nuclear factor-κB activation and virulence factors of Helicobacter pylori in Japanese clinical isolates. J Gastroenterol Hepatol 2002; 17: 556-562.
54. Ando T, Tsuzuki T, Mizuno T etal. Characteristics of Helicobacter pylori-induced gastritis and the effect of H. pylori eradication in patients with chronic idiopathic thrombocytopenic purpura. Helicobacter 2004; 9: 443-452.
55. Shiota S, Watada M, Matsunari O, Iwatani S, Suzuki R, Yamaoka Y. Helicobacter pylori iceA, clinical outcomes, and correlation with cagA: a meta-analysis. PLoS ONE 2012; 7: e30354.
56. r 34, 000 proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci U S A 2000; 97: 7533-7538.
57. Wu JY, Lu H, Sun Y, Graham DY, Cheung HS, Yamaoka Y. Balance between polyoma enhancing activator 3 and activator protein 1 regulates Helicobacter pylori-stimulated matrix metalloproteinase 1 expression. Cancer Res 2006; 66: 5111-5120.
58. Kudo T, Lu H, Wu JY etal. Pattern of transcription factor activation in Helicobacter pylori-infected Mongolian gerbils. Gastroenterology 2007; 132: 1024-1038.
59. Lu H, Wu JY, Kudo T, Ohno T, Graham DY, Yamaoka Y. Regulation of interleukin-6 promoter activation in gastric epithelial cells infected with Helicobacter pylori. Mol Biol Cell 2005; 16: 4954-4966.
60. Yamaoka Y, Kudo T, Lu H, Casola A, Brasier AR, Graham DY. Role of interferon-stimulated responsive element-like element in interleukin-8 promoter in Helicobacter pylori infection. Gastroenterology 2004; 126: 1030-1043.
61. Tabassam FH, Graham DY, Yamaoka Y. OipA plays a role in Helicobacter pylori-induced focal adhesion kinase activation and cytoskeletal re-organization. Cell Microbiol 2008; 10: 1008-1020.
62. Tabassam FH, Graham DY, Yamaoka Y. Helicobacter pylori activate epidermal growth factor receptor- and phosphatidylinositol 3-OH kinase-dependent Akt and glycogen synthase kinase 3β phosphorylation. Cell Microbiol 2009; 11: 70-82.
63. Tabassam FH, Graham DY, Yamaoka Y. Helicobacter pylori-associated regulation of forkhead transcription factors FoxO1/3a in human gastric cells. Helicobacter 2012; 17: 193-202.
64. Yamaoka Y, Kikuchi S, el-Zimaity HM, Gutierrez O, Osato MS, Graham DY. Importance of Helicobacter pylori oipA in clinical presentation, gastric inflammation, and mucosal interleukin 8 production. Gastroenterology 2002; 123: 414-424.
65. Yamaoka Y, Ojo O, Fujimoto S etal. Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 2006; 55: 775-781.
66. Graham DY, Opekun AR, Osato MS etal. Challenge model for Helicobacter pylori infection in human volunteers. Gut 2004; 53: 1235-1243.
67. Yamaoka Y, Kita M, Kodama T etal. Helicobacter pylori infection in mice: role of outer membrane proteins in colonization and inflammation. Gastroenterology 2002; 123: 1992-2004.
68. Sugimoto M, Ohno T, Graham DY, Yamaoka Y. Gastric mucosal interleukin-17 and -18 mRNA expression in Helicobacter pylori-induced Mongolian gerbils. Cancer Sci 2009; 100: 2152-2159.
69. Sugimoto M, Ohno T, Graham DY, Yamaoka Y. Helicobacter pylori outer membrane proteins on gastric mucosal interleukin 6 and 11 expression in Mongolian gerbils. J Gastroenterol Hepatol 2011; 26: 1677-1684.
70. Fujimoto S, Olaniyi Ojo O, Arnqvist A etal. Helicobacter pylori BabA expression, gastric mucosal injury, and clinical outcome. Clin Gastroenterol Hepatol 2007; 5: 49-58.
71. Kawai M, Furuta Y, Yahara K etal. Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes. BMC Microbiol 2011; 11: 104.
72. Furuta Y, Kawai M, Yahara K etal. Birth and death of genes linked to chromosomal inversion. Proc Natl Acad Sci U S A 2011; 108: 1501-1506.
73. Yamaoka Y. Roles of Helicobacter pylori BabA in gastroduodenal pathogenesis. World J Gastroenterol 2008; 14: 4265-4272.
74. Colbeck JC, Hansen LM, Fong JM, Solnick JV. Genotypic profile of the outer membrane proteins BabA and BabB in clinical isolates of Helicobacter pylori. Infect Immun 2006; 74: 4375-4378.
75. Hennig EE, Allen JM, Cover TL. Multiple chromosomal loci for the babA gene in Helicobacter pylori. Infect Immun 2006; 74: 3046-3051.
76. Toller IM, Neelsen KJ, Steger M etal. Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci U S A 2011; 108: 14944-14949.
77. de Sablet T, Piazuelo MB, Shaffer CL etal. Phylogeographic origin of Helicobacter pylori is a determinant of gastric cancer risk. Gut 2011; 60: 1189-1195.
78. Shiota S, Matsunari O, Watada M, Yamaoka Y. Virulence factors or ancestral origin of Helicobacter pylori: which is a better predictor of gastric cancer risk? Gut 2012; 61: 469-470.