Helicobacter pylori infection triggers aberrant expression of activation-induced cytidine deaminase in gastric epithelium

Nature Medicine

Volumn 13, Issue 4, 2007, Pages 470-476

  Matsumoto, Yuko ^a   Marusawa, Hiroyuki ^a   Kinoshita, Kazuo ^b   Endo, Yoko ^a   Kou, Tadayuki ^a   Morisawa, Toshiyuki ^a   Azuma, Takeshi ^c   Okazaki, Il Mi ^a   Honjo, Tasuku ^a   Chiba, Tsutomu ^a  

^a KYOTO UNIVERSITY   (Japan)

^b SHIGA MEDICAL CENTER FOR ADULTS   (Japan)

^c KOBE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTIDINE DEAMINASE; DNA; ENZYME; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEOTIDE; PROTEIN P53; RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; CARCINOGENESIS; CONTROLLED STUDY; EPITHELIUM CELL; GASTRIC CARCINOGENESIS; GENE MUTATION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH EPITHELIUM; STOMACH MUCOSA; TUMOR SUPPRESSOR GENE; UPREGULATION;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CYTIDINE DEAMINASE; DNA PRIMERS; GASTRIC MUCOSA; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, P53; HELICOBACTER INFECTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; MODELS, BIOLOGICAL; MUTAGENESIS; NF-KAPPA B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS;

HELICOBACTER PYLORI;

EID: 34147180434     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm1566     Document Type: Article

References (45)

1. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994 IARC Monogr. Eval. Carcinog. Risks Hum. 61, 1-241 (1994).
2. Tomb, J.F. et al. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539-547 (1997).
3. Blaser, M.J. Helicobacter pylori and gastric diseases. Br. Med. J. 316, 1507-1510 (1998).
4. Peek, R.M., Jr et al. Heightened inflammatory response and cytokine expression in vivo to cagA+ Helicobacter pylori strains. Lab. Invest. 73, 760-770 (1995).
5. Crabtree, J.E. et al. Systemic and mucosal humoral responses to Helicobacter pylori in gastric cancer. Gut 34, 1339-1343 (1993).
6. Blaser, M.J. 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).
7. Parsonnet, J., Friedman, G.D., Orentreich, N. & Vogelman, H. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 40, 297-301 (1997).
8. Zhang, H. et al. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424, 94-98 (2003).
9. Honjo, T., Kinoshita, K. & Muramatsu, M. Molecular mechanism of class switch recombination: linkage with somatic hypermutation. Annu. Rev. Immunol. 20, 165-196 (2002).
10. Wedekind, J.E., Dance, G.S., Sowden, M.P. & Smith, H.C. Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business. Trends Genet. 19, 207-216 (2003).
11. Cascalho, M. Advantages and disadvantages of cytidine deamination. J. Immunol. 172, 6513-6518 (2004).
12. Kinoshita, K. & Nonaka, T. The dark side of activation-induced cytidine deaminase: relationship with leukemia and beyond. Int. J. Hematol. 83, 201-207 (2006).
13. Okazaki, I.M. et al. Constitutive expression of AID leads to tumorigenesis. J. Exp. Med. 197, 1173-1181 (2003).
14. Kou, T. et al. Expression of activation-induced cytidine deaminase in human hepatocytes during hepatocarcinogenesis. Int. J. Cancer 120, 469-476 (2007).
15. Greeve, J. et al. Expression of activation-induced cytidine deaminase in human B-cell non-Hodgkin lymphomas. Blood 101, 3574-3580 (2003).
16. Albesiano, E. et al. Activation-induced cytidine deaminase in chronic lymphocytic leukemia B cells: expression as multiple forms in a dynamic, variably sized fraction of the clone. Blood 102, 3333-3339 (2003).
17. Pasqualucci, L. et al. Expression of the AID protein in normal and neoplastic B cells. Blood 104, 3318-3325 (2004).
18. Lossos, I.S., Levy, R. & Alizadeh, A.A. AID is expressed in germinal center B-cell-like and activated B-cell-like diffuse large-cell lymphomas and is not correlated with intraclonal heterogeneity. Leukemia 18, 1775-1779 (2004).
19. Hollstein, M., Sidransky, D., Vogelstein, B. & Harris, C.C. p53 mutations in human cancers. Science 253, 49-53 (1991).
20. 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, 1259-1264 (1996).
21. Faili, A. et al. AID-dependent somatic hypermutation occurs as a DNA single-strand event in the BL2 cell line. Nat. Immunol. 3, 815-821 (2002).
22. Babbage, G., Ottensmeier, C.H., Blaydes, J., Stevenson, F.K. & Sahota, S.S. Immunoglobulin heavy chain locus events and expression of activation-induced cytidine deaminase in epithelial breast cancer cell lines. Cancer Res. 66, 3996-4000 (2006).
23. Peek, R.M., Jr. IV. Helicobacter pylori strain-specific activation of signal transduction cascades related to gastric inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G525-G530 (2001).
24. Keates, S., Hitti, Y.S., Upton, M. & Kelly, C.P. Helicobacter pylori infection activates NF-κB in gastric epithelial cells. Gastroenterology 113, 1099-1109 (1997).
25. Doi, T., Kinoshita, K., Ikegawa, M., Muramatsu, M. & Honjo, T. De novo protein synthesis is required for the activation-induced cytidine deaminase function in classswitch recombination. Proc. Natl. Acad. Sci. USA 100, 2634-2638 (2003).
26. Stock, M. & Otto, F. Gene deregulation in gastric cancer. Gene 360, 1-19 (2005).
27. Ramiro, A.R., Stavropoulos, P., Jankovic, M. & Nussenzweig, M.C. Transcription enhances AID-mediated cytidine deamination by exposing single-stranded DNA on the nontemplate strand. Nat. Immunol. 4, 452-456 (2003).
28. Chaudhuri, J. et al. Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422, 726-730 (2003).
29. Peek, R.M., Jr. & Blaser, M.J. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2, 28-37 (2002).
30. Morgan, C. et al. Detection of p53 mutations in precancerous gastric tissue. Br. J. Cancer 89, 1314-1319 (2003).
31. Yoshikawa, K. et al. AID enzyme-induced hypermutation in an actively transcribed gene in fibroblasts. Science 296, 2033-2036 (2002).
32. Fenoglio-Preiser, C.M., Wang, J., Stemmermann, G.N. & Noffsinger, A. TP53 and gastric carcinoma: a review. Hum. Mutat. 21, 258-270 (2003).
33. Karin, M. Nuclear factor-κB in cancer development and progression. Nature 441, 431-436 (2006).
34. Muramatsu, M. et al. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274, 18470-18476 (1999).
35. Dedeoglu, F., Horwitz, B., Chaudhuri, J., Alt, F.W. & Geha, R.S. Induction of activation-induced cytidine deaminase gene expression by IL-4 and CD40 ligation is dependent on STAT6 and NF-κB. Int. Immunol. 16, 395-404 (2004).
36. Viala, J. et al. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5, 1166-1174 (2004).
37. Chiba, T., Seno, H., Marusawa, H., Wakatsuki, Y. & Okazaki, K. Host factors are important in determining clinical outcomes of Helicobacter pylori infection. J. Gastroenterol. 41, 1-9 (2006).
38. Glickman, J.N. & Antonioli, D.A. Gastritis. Gastrointest. Endosc. Clin. N. Am. 11, 717-740 (2001).
39. Uchida, K. et al. Analysis of cytokines in the early development of gastric secondary lymphoid follicles in Helicobacter pylori-infected BALB/c mice with neonatal thymectomy. Infect. Immun. 69, 6749-6754 (2001).
40. Matsumoto, Y. et al. Eradication of Helicobacter pylori and resolution of gastritis in the gastric mucosa of IL-10-deficient mice. Helicobacter 10, 407-415 (2005).
41. Marusawa, H., Hijikata, M., Watashi, K., Chiba, T. & Shimotohno, K. Regulation of Fas-mediated apoptosis by NF-κB activity in human hepatocyte derived cell lines. Microbiol. Immunol. 45, 483-489 (2001).
42. Ta, V.T. et al. AID mutant analyses indicate requirement for class-switch-specific cofactors. Nat. Immunol. 4, 843-848 (2003).
43. Iwai, A. et al. Role of a novel oncogenic protein, gankyrin, in hepatocyte proliferation. J. Gastroenterol. 38, 751-758 (2003).
44. Toda, Y. et al. Application of tyramide signal amplification system to immunohistochemistry: a potent method to localize antigens that are not detectable by ordinary method. Pathol. Int. 49, 479-483 (1999).
45. Kanda, N. et al. Involvement of cyclooxygenase-2 in gastric mucosal hypertrophy in gastrin transgenic mice. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G519-G527 (2006).