Geographic differences in gastric cancer incidence can be explained by differences between Helicobacter pylori strains

Internal Medicine

Volumn 47, Issue 12, 2008, Pages 1077-1083

  Yamaoka, Yoshio ^a   Kato, Mototsugu ^b   Asaka, Masahiro ^c  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b HOKKAIDO UNIVERSITY HOSPITAL   (Japan)

^c HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

cagA; Gastric cancer; Genotypes; Helicobacter pylori; vacA

Indexed keywords

CAGA PROTEIN; DNA GLYCOSYLASE MUTY; INTERLEUKIN 1; INTERLEUKIN 18; INTERLEUKIN 6; INTERLEUKIN 8; OUTER MEMBRANE PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; RANTES; VACUOLATING TOXIN; VIRULENCE FACTOR; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; VACA PROTEIN, HELICOBACTER PYLORI;

AFRICA; ASIAN; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CANCER INCIDENCE; EUROPE; GASTRITIS; GENE MUTATION; GENETIC POLYMORPHISM; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOUSEKEEPING GENE; HUMAN; NONHUMAN; PREVALENCE; REVIEW; SIGNAL TRANSDUCTION; SOUTH ASIA; STOMACH ADENOCARCINOMA; STOMACH CANCER; STOMACH CARCINOGENESIS; STRAIN DIFFERENCE; GENETICS; HEALTH; INCIDENCE; MICROBIOLOGY; PATHOGENICITY; STOMACH TUMOR; VIRULENCE;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; GENOTYPE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; INCIDENCE; STOMACH NEOPLASMS; VIRULENCE; WORLD HEALTH;

EID: 48049120646     PISSN: 09182918     EISSN: 13497235     Source Type: Journal    
DOI: 10.2169/internalmedicine.47.0975     Document Type: Review

References (77)

1. Blaser MJ, Perez-Perez GI, Kleanthous H, et al. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 55: 2111-2115, 1995.
2. Kuipers EJ, Perez-Perez GI, Meuwissen SG, Blaser MJ. Helicobacter pylori and atrophic gastritis: importance of the cagA status. J Natl Cancer Inst 87: 1777-1780, 1995.
3. Nomura AM, Lee J, Stemmermann GN, Nomura RY, Perez-Perez GI, Blaser MJ. Helicobacter pylori CagA seropositivity and gastric carcinoma risk in a Japanese American population. J Infect Dis 186: 1138-1144, 2002.
4. Parsonnet J, Friedman GD, Orentreich N, Vogelman H. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 40: 297-301, 1997.
5. Rugge M, Busatto G, Cassaro M, et al. Patients younger than 40 years with gastric carcinoma: Helicobacter pylori genotype and associated gastritis phenotype. Cancer 85: 2506-2511, 1999.
6. van Doorn LJ, Figueiredo C, Megraud F, et al. Geographic distribution of vacA allelic types of Helicobacter pylori. Gastroenterology 116: 823-830, 1999.
7. Achtman M, Azuma T, Berg DE, et al. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 32: 459-470, 1999.
8. Eppinger M, Baar C, Linz B, et al. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2: e120, 2006.
9. Falush D, Wirth T, Linz B, et al. Traces of human migrations in Helicobacter pylori populations. Science 299: 1582-1585, 2003.
10. Ghose C, Perez-Perez GI, Dominguez-Bello MG, Pride DT, Bravi CM, Blaser MJ. East Asian genotypes of Helicobacter pylori strains in Amerindians provide evidence for its ancient human carriage. Proc Natl Acad Sci U S A 99: 15107-15111, 2002.
11. Gressmann H, Linz B, Ghai R, et al. Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1: e43, 2005.
12. Linz B, Balloux F, Moodley Y, et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445: 915-918, 2007.
13. Wirth T, Wang X, Linz B, et al. Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci U S A 101: 4746-4751, 2004.
14. Yamaoka Y, Orito E, Mizokami M, et al. Helicobacter pylori in North and South America before Columbus. FEBS Lett 517: 180-184, 2002.
15. Covacci A, Censini S, Bugnoli M, et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci U S A 90: 5791-5795, 1993.
16. Tummuru MK, Cover TL, Blaser MJ. Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect Immun 61: 1799-1809, 1993.
17. 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 36: 2258-2263, 1998.
18. Yamaoka Y, El-Zimaity HM, Gutierrez O, et al. Relationship between the cagA 3′ repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology 117: 342-349, 1999.
19. Yamaoka Y, Osato MS, Sepulveda AR, et al. Molecular epidemiology of Helicobacter pylori: separation of H. pylori from East Asian and non-Asian countries. Epidemiol Infect 124: 91-96, 2000.
20. Yamaoka Y, Graham DY. Clarifications regarding the 3′ repeat region of the cagA gene in Helicobacter pylori and clinical outcome. J Clin Microbiol 39: 2369-2370, 2001.
21. Argent RH, Kidd M, Owen RJ, Thomas RJ, Limb MC, Atherton JC. Determinants and consequences of different levels of CagA phosphorylation for clinical isolates of Helicobacter pylori. Gastroenterology 127: 514-523, 2004.
22. Azuma T, Yamakawa A, Yamazaki S, et al. Correlation between variation of the 3′ region of the cagA gene in Helicobacter pylori and disease outcome in Japan. J Infect Dis 186: 1621-1630, 2002.
23. Hirata Y, Yanai A, Shibata W, et al. Functional variability of cagA gene in Japanese isolates of Helicobacter pylori. Gene 343: 165-172, 2004.
24. Censini S, Lange C, Xiang Z, et al. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci U S A 93: 14648-14653, 1996.
25. Asahi M, Azuma T, Ito S, et al. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J Exp Med 191: 593-602, 2000.
26. Backert S, Ziska E, Brinkmann V, et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol 2: 155-164, 2000.
27. Odenbreit S, Puls J, Sedlmaier B, Gerland E, Fischer W, Haas R. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500, 2000.
28. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci U S A 96: 14559-14564, 1999.
29. Stein M, Rappuoli R, Covacci A. Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci U S A 97: 1263-1268, 2000.
30. Viala J, Chaput C, Boneca IG, et al. Nod1 responds to peptidogly-can delivered by the Helicobacter pylori cag pathogenicity island. Nat Immunol 5: 1166-1174, 2004.
31. Judd LM, Alderman BM, Howlett M, et al. Gastric cancer development in mice lacking the SHP2 binding site on the IL-6 family co-receptor gp130. Gastroenterology 126: 196-207, 2004.
32. Higashi H, Tsutsumi R, Fujita A, et al. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci U S A 99: 14428-14433, 2002.
33. Naito M, Yamazaki T, Tsutsumi R, et al. Influence of EPIYA-repeat polymorphism on the phosphorylation-dependent biological activity of Helicobacter pylori CagA. Gastroenterology 130: 1181-1190, 2006.
34. 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 9: 453-459, 2004.
35. Azuma T, Yamakawa A, Yamazaki S, et al. Distinct diversity of the cag pathogenicity island among Helicobacter pylori strains in Japan. J Clin Microbiol 42: 2508-2517, 2004.
36. Atherton JC. The pathogenesis of Helicobacter pylori-induced gastro-duodenal diseases. Annu Rev Pathol Mech Dis 1: 63-96, 2006.
37. Cover TL, Blanke SR. Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 3: 320-332, 2005.
38. Kusters JG, van Vliet AH, Kuipers EJ. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19: 449-490, 2006.
39. Boncristiano M, Paccani SR, Barone S, et al. The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J Exp Med 198: 1887-1897, 2003.
40. Gebert B, Fischer W, Weiss E, Hoffmann R, Haas R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301: 1099-1102, 2003.
41. Sundrud MS, Torres VJ, Unutmaz D, Cover TL. Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion. Proc Natl Acad Sci U S A 101: 7727-7732, 2004.
42. 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 270: 17771-17777, 1995.
43. Atherton JC, Peek RM Jr, Tham KT, Cover TL, Blaser MJ. Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology 112: 92-99, 1997.
44. Fujikawa A, Shirasaka D, Yamamoto S, et al. Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat Genet 33: 375-381, 2003.
45. Marchetti M, Arico B, Burroni D, Figura N, Rappuoli R, Ghiara P. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 267: 1655-1658, 1995.
46. Ogura K, Maeda S, Nakao M, et al. Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbil. J Exp Med 192: 1601-1610, 2000.
47. Wada A, Yamasaki E, Hirayama T. Helicobacter pylori vacuolating cytotoxin, VacA, is responsible for gastric ulceration. J Biochem (Tokyo) 136: 741-746, 2004.
48. Cover TL, Blaser MJ. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 267: 10570-10575, 1992.
49. Leunk RD. Production of a cytotoxin by Helicobacter pylori. Rev Infect Dis 13 Suppl 8: S686-S689, 1991.
50. Letley DP, Atherton JC. Natural diversity in the N terminus of the mature vacuolating cytotoxin of Helicobacter pylori determines cytotoxin activity. J Bacteriol 182: 3278-3280, 2000.
51. Letley DP, Rhead JL, Twells RJ, Dove B, Atherton JC. Determinants of non-toxicity in the gastric pathogen Helicobacter pylori. J Biol Chem 278: 26734-26741, 2003.
52. Figueirede C, Machado JC, Pharoah P, et al. Helicobacter pylori and interleukin 1 genotyping: an opportunity to identify high-risk individuals for gastric carcinoma. J Natl Cancer Inst 94: 1680-1687, 2002.
53. Kidd M, Lastovica AJ, Atherton JC, Louw JA. Heterogeneity in the Helicobacter pylori vacA and cagA genes: association with gastroduodenal disease in South Africa? Gut 45: 499-502, 1999.
54. Miehlke S, Kirsch C, gha-Amiri K, et al. The Helicobacter pylori vacA sl, ml genotype and cagA is associated with gastric carcinoma in Germany. Int J Cancer 87: 322-327, 2000.
55. Yamaoka Y, Kodama T, Kita M, Imanishi J, Kashima K. Graham DY. Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome. Helicobacter 3: 241-253, 1998.
56. van Doorn LJ, Figueiredo C, Sanna R, et al. Expanding allelic diversity of Helicobacter pylori vacA. J Clin Microbiol 36: 2597-2603, 1998.
57. Mukhopadhyay AK, Kersulyte D, Jeong JY, et al. Distinctiveness of genotypes of Helicobacter pylori in Calcutta,. India. J Bacteriol 182: 3219-3227, 2000.
58. Rhead JL, Letley DP, Mohammadi M, et al. A new Helicobacter pylori vacuolating cytotoxin determinant, the intermediate region, is associated with gastric cancer. Gastroenterology 133: 926-936, 2007.
59. Ogiwara H, Graham D Y, Yamaoka Y. vacA i-region subtyping: another false lead for a disease-associated marker. 2008 (in press).
60. Kudo T, Lu H, Wu JY, Graham DY, Casola A, Yamaoka Y. Regulation of RANTES promoter activation in gastric epithelial cells infected with Helicobacter pylori. Infect Immun 73: 7602-7612, 2005.
61. 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 16: 4954-4966, 2005.
62. Yamaoka Y, Kita M, Kodama T, et al. Helicobacter pylori infection in mice: Role of outer membrane proteins in colonization and inflammation. Gastroenterology 123: 1992-2004, 2002.
63. 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 123: 414-424, 2002.
64. Yamauchi K, Choi U, Lu H, Ogiwara H, Graham DY, Yamaoka Y. Regulation of IL-18 in Helicobacter pylori infection. J Immunol 180: 1207-1216, 2008.
65. 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 126: 1030-1043, 2004.
66. Yamaoka Y, Kwon DH, Graham DY. A M(r) 34,000. proinflammatory outer membrane protein (oipA) of Helicobacter pylori. Proc Natl Acad Sci U S A 97: 7533-7538, 2000.
67. Yimaoka Y, Ojo O, Fujimoto S, et al. Helicobacter pylori outer membrane proteins and gastroduodenal disease. Gut 55: 775-781, 2006.
68. Ando T, Peek RM, Pride D, et al. Polymorphisms of Helicobacter pylori HP0638 reflect geographic origin and correlate with cagA status. J Clin Microbiol 40: 239-246, 2002.
69. de Jonge R, Pot RG, Loffeld RJ, van Vlict AH, Kuipers EJ, Kusters JG. The functional status of the Helicobacter pylori sabB adhesin gene as a putative marker or disease outcome. Helicobacter 9: 158-164, 2004.
70. Lehours P,Menard A, Dupouy S, et al. Evaluation of the association of mine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun 72: 880-888, 2004.
71. Dossumbekova A, Prinz C, Mages J, et al. Helicobacter pylori HopH (OipA) and bacterial pathogenicity: genetic and functional genomic analysis of hopH gene polymorphisms J Infect Dis 194: 1346-1355, 2006.
72. ILver D, Arnqvist, A, Ogren J, et al. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 279: 373-377, 1998.
73. Gerhard M, Lehn N, Neumayer N, et. al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci U S A 96: 12778-12783, 1999.
74. Pride DT, Meinersmann RJ, Blaser MJ. Allelic Variation within Helicobacter pylori babA and babB. Infect Immun 69: 1160-1171, 2001.
75. Aspholm-Hurtig M, Dailide G, Lahmann M, et al. Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 305: 519-522, 2004.
76. Odenbreit S, Till M, Hofreuter D, Faller G, Haas R. Genetic and functional characterization of the alpAB gene locus essential for the adhesion of Helicobacter pylori to human gastric tissue. Mol Microbiol 31: 1537-1548, 1999.
77. Lu H, Wu JY, Beswick EJ, et al. Functional and intracellular signaling differences associated with the Helicobacter pylori AlpAB adhesin from Western and East Asian strains. J Biol Chem 282: 6242-6254, 2007.