Table of Contents
Pathology Research International
Volume 2011, Article ID 193149, 8 pages
http://dx.doi.org/10.4061/2011/193149
Review Article

Molecular Aspects of H. pylori-Related MALT Lymphoma

Department of Pathology, The University of Michigan, 1301 Catherine Rd., Room M5224 Medical Science I, Ann Arbor, MI 48109, USA

Received 12 November 2010; Accepted 27 December 2010

Academic Editor: Brian P. Rubin

Copyright © 2011 Scott R. Owens and Lauren B. Smith. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. L. Peterson, “Helicobacter pylori and peptic ulcer disease,” The New England Journal of Medicine, vol. 324, no. 15, pp. 1043–1048, 1991. View at Google Scholar · View at Scopus
  2. S. J. O. Veldhuyzen van Zanten and P. M. Sherman, “Helicobacter pylori infection as a cause of gastritis, duodenal ulcer, gastric cancer and nonulcer dyspepsia: a systematic overview,” Canadian Medical Association Journal, vol. 150, no. 2, pp. 177–185, 1994. View at Google Scholar · View at Scopus
  3. B. J. Marshall and J. R. Warren, “Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration,” The Lancet, vol. 1, no. 8390, pp. 1311–1314, 1984. View at Google Scholar · View at Scopus
  4. N. Uemura, S. Okamoto, and S. Okamoto, “Helicobacter pylori infection and the development of gastric cancer,” The New England Journal of Medicine, vol. 345, no. 11, pp. 784–789, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Morgner, E. Bayerdörffer, A. Neubauer, and M. Stolte, “Malignant tumors of the stomach: gastric mucosa-associated lymphoid tissue lymphoma and Helicobacter pylori,” Gastroenterology Clinics of North America, vol. 29, no. 3, pp. 593–607, 2000. View at Google Scholar · View at Scopus
  6. P. G. Isaacson and M. Q. Du, “Gastrointestinal lymphoma: where morphology meets molecular biology,” Journal of Pathology, vol. 205, no. 2, pp. 255–274, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. J. K. Greenson et al., “MALT lymphoma,” in Diagnostic Pathology: Gastrointestinal, pp. 2:70–2:75, Amirsys, Inc., Salt Lake City, Utah, USA, 2010. View at Google Scholar
  8. M. Q. Du, “MALT lymphoma : recent advances in aetiology and molecular genetics,” Journal of Clinical and Experimental Hematopathology, vol. 47, no. 2, pp. 31–42, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Q. Du and P. G. Isaccson, “Gastric MALT lymphoma: from aetiology to treatment,” The Lancet Oncology, vol. 3, no. 2, pp. 97–104, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. R. A. Hamoudi, A. Appert, and A. Appert, “Differential expression of NF-κB target genes in MALT lymphoma with and without chromosome translocation: insights into molecular mechanism,” Leukemia, vol. 24, pp. 1487–1497, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. H. Inagaki, “Mucosa-associated lymphoid tissue lymphoma: molecular pathogenesis and clinicopathological significance,” Pathology International, vol. 57, no. 8, pp. 474–484, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. A. Andriani, A. Miedico, and A. Miedico, “Management and long-term follow-up of early stage H. pylori-associated gastric MALT-lymphoma in clinical practice: an Italian, multicentre study,” Digestive and Liver Disease, vol. 41, no. 7, pp. 467–473, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. K. Hori, T. Nishigami, T. Chiba, Y. Matsushima, and T. Kojima, “Regression of MALT lymphomas coexisting in the duodenal bulb and the stomach by eradiction of Helicobacter pylori,” Journal of Gastroenterology, vol. 37, no. 4, pp. 288–292, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Montalban, A. Santon, and A. Santon, “Treatment of low-grade gastric mucosa-associated lymphoid tissue lymphoma in stage I with Helicobacter pylori eradication. Long-term results after sequential histologic and molecular follow-up,” Haematologica, vol. 86, no. 6, pp. 609–617, 2001. View at Google Scholar
  15. S. Nakamura, T. Matsumoto, S. Nakamura, Y. Kusano, M. Esaki, K. Kurahara, and T. Fukuda, “Duodenal mucosa-associated lymphoid tissue lymphoma treated by eradication of Helicobacter pylori: report of 2 cases including EUS findings,” Gastrointestinal Endoscopy, vol. 54, no. 6, pp. 772–775, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. D. Niino, K. Yamamoto, and K. Yamamoto, “Regression of rectal mucosa-associated lymphoid tissue (MALT) lymphoma after antibiotic treatments,” Pathology International, vol. 60, no. 6, pp. 438–442, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  17. A. C. Wotherspoon, C. Doglioni, T. C. Diss, L. Pan, A. Moschini, M. De Boni, and P. G. Isaacson, “Regression of primary low-grade-B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori,” The Lancet, vol. 342, no. 8871, pp. 575–577, 1993. View at Publisher · View at Google Scholar · View at Scopus
  18. P. M. Banks, “Gastrointestinal lymphoproliferative disorders,” Histopathology, vol. 50, no. 1, pp. 42–54, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. M. Q. Du and J. C. Atherton, “Molecular subtyping of gastric malt lymphomas: implications for prognosis and management,” Gut, vol. 55, no. 6, pp. 886–893, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. T. Nakamura, H. Inagaki, M. Seto, and S. Nakamura, “Gastric low-grade B-cell MALT lymphoma: treatment, response, and genetic alteration,” Journal of Gastroenterology, vol. 38, no. 10, pp. 921–929, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. P. Isaacson and D. H. Wright, “Malignant lymphoma of mucosa-associated lymphoid tissue. A distinctive type of B-cell lymphoma,” Cancer, vol. 52, no. 8, pp. 1410–1416, 1983. View at Google Scholar · View at Scopus
  22. P. G. Isaacson, A. Chott, S. Nakamura, H. K. Muller-Hermelink, N. L. Harris, and S. H. Swerdlow, “Extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma),” in WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues, S. H. Swerdlow et al., Ed., pp. 214–217, IARCPress, Lyon, France, 2008. View at Google Scholar
  23. M. P. Siakantaris, G. A. Pangalis, and G. A. Pangalis, “Early-stage gastric MALT lymphoma: is it a truly localized disease?” The Oncologist, vol. 14, no. 2, pp. 148–154, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. S. Nakamura, T. Yao, K. Aoyagi, M. Iida, M. Fujishima, and M. Tsuneyoshi, “Helicobacter pylori and primary gastric lymphoma: a histopathologic and immunohistochemical analysis of 237 patients,” Cancer, vol. 79, no. 1, pp. 3–11, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Farinha and R. D. Gascoyne, “Molecular pathogenesis of mucosa-associated lymphoid tissue lymphoma,” Journal of Clinical Oncology, vol. 23, no. 26, pp. 6370–6378, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  26. J. L. O'Rourke, “Gene expression profiling in Helicobacter-induced MALT lymphoma with reference to antigen drive and protective immunization,” Journal of Gastroenterology and Hepatology, vol. 23, no. 2, pp. S151–S156, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  27. X. Sagaert, C. De Wolf-Peeters, H. Noels, and M. Baens, “The pathogenesis of MALT lymphomas: where do we stand?” Leukemia, vol. 21, no. 3, pp. 389–396, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  28. V. J. Craig, S. B. Cogliatti, I. Arnold, C. Gerke, J. E. Balandat, T. Wündisch, and A. Müller, “B-cell receptor signaling and CD40 ligand-independent T cell help cooperate in Helicobacter-induced MALT lymphomagenesis,” Leukemia, vol. 24, pp. 1186–1196, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  29. M. M. D'Elios, A. Amedei, M. Benagiano, A. Azzurri, and G. Del Prete, “Helicobacter pylori, T cells and cytokines: the “dangerous liaisons”,” FEMS Immunology and Medical Microbiology, vol. 44, no. 2, pp. 113–119, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  30. S. Umehara, H. Higashi, N. Ohnishi, M. Asaka, and M. Hatakeyama, “Effects of Helicobacter pylori CagA protein on the growth and survival of B lymphocytes, the origin of MALT lymphoma,” Oncogene, vol. 22, no. 51, pp. 8337–8342, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. E. D. Remstein, A. Dogan, and A. Dogan, “The incidence and anatomic site specificity of chromosomal translocations in primary extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) in North America,” American Journal of Surgical Pathology, vol. 30, no. 12, pp. 1546–1553, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  32. H. Ye, H. Liu, and H. Liu, “Variable frequencies of t(11;18)(q21;q21) in MALT lymphomas of different sites: significant association with CagA strains of H pylori in gastric MALT lymphoma,” Blood, vol. 102, no. 3, pp. 1012–1018, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  33. S. Nakamura, H. Ye, and H. Ye, “Clinical impact of genetic aberrations in gastric MALT lymphoma: a comprehensive analysis using interphase fluorescence in situ hybridisation,” Gut, vol. 56, no. 10, pp. 1358–1363, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  34. S. S. Chuang, C. Lee, and C. Lee, “High frequency of t(11;18) in gastric mucosa-associated lymphoid tissue lymphomas in Taiwan, including one patient with high-grade transformation,” British Journal of Haematology, vol. 120, no. 1, pp. 97–100, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. H. Inagaki, T. Nakamura, and T. Nakamura, “Gastric MALT lymphomas are divided into three groups based on responsiveness to Helicobacter pylori eradication and detection of API2-MALT1 fusion,” American Journal of Surgical Pathology, vol. 28, no. 12, pp. 1560–1567, 2004. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Wang, A. Auerbach, and A. Auerbach, “t(11;18)(q21;q21) in extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue in stomach: a study of 48 cases,” Modern Pathology, vol. 22, no. 1, pp. 79–86, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. J. Dierlamm, M. Baens, and M. Baens, “Detection of t(11;18)(q21;q21) by interphase fluorescence in situ hybridization using API2 and MLT specific probes,” Blood, vol. 96, no. 6, pp. 2215–2218, 2000. View at Google Scholar · View at Scopus
  38. H. Ye, L. Gong, and L. Gong, “MALT lymphoma with t(14;18)(q32;q21)/IGH-MALT1 is characterized by strong cytoplasmic MALT1 and BCL10 expression,” Journal of Pathology, vol. 205, no. 3, pp. 293–301, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. L. Ho, R. E. Davis, and R. E. Davis, “MALT1 and the API2-MALT1 fusion act between CD40 and IKK and confer NF-κB-dependent proliferative advantage and resistance against FAS-induced cell death in B cells,” Blood, vol. 105, no. 7, pp. 2891–2899, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. S. Nakamura, H. Ye, and H. Ye, “Gastric MALT lymphoma with t(14;18)(q32;q21) involving IGH and BCL2 genes that responded to Helicobacter pylori eradication,” Journal of Clinical Pathology, vol. 60, no. 10, pp. 1171–1173, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. B. Streubel, I. Simonitsch-Klupp, and I. Simonitsch-Klupp, “Variable frequencies of MALT lymphoma-associated genetic aberrations in MALT lymphomas of different sites,” Leukemia, vol. 18, no. 10, pp. 1722–1726, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. R. Achuthan, S. M. Bell, and S. M. Bell, “Novel translocation of the BCL10 gene in a case of mucosa associated lymphoid tissue lymphoma,” Genes Chromosomes and Cancer, vol. 29, no. 4, pp. 347–349, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Ye, A. Dogan, and A. Dogan, “BCL10 expression in normal and neoplastic lymphoid tissue: nuclear localization in MALT lymphoma,” American Journal of Pathology, vol. 157, no. 4, pp. 1147–1154, 2000. View at Google Scholar · View at Scopus
  44. H. Ye, E. D. Remstein, C. M. Bacon, A. G. Nicholson, A. Dogan, and M. Q. Du, “Chromosomal translocations involving BCL6 in MALT lymphoma,” Haematologica, vol. 93, no. 1, pp. 145–146, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  45. Y. W. Chen, X. T. Hu, and X. T. Hu, “High BCL6 expression predicts better prognosis, independent of BCL6 translocation status, translocation partner, or BCL6-deregulating mutations, in gastric lymphoma,” Blood, vol. 108, no. 7, pp. 2373–2383, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  46. B. Streubel, U. Vinatzer, A. Lamprecht, M. Raderer, and A. Chott, “t(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma,” Leukemia, vol. 19, no. 4, pp. 652–658, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. A. C. Wotherspoon, T. M. Finn, and P. G. Isaacson, “Trisomy 3 in low-grade B-cell lymphomas of mucosa-associated lymphoid tissue,” Blood, vol. 85, no. 8, pp. 2000–2004, 1995. View at Google Scholar · View at Scopus
  48. G. Ott, J. Kalla, and J. Kalla, “Trisomy 3 is not a common feature in malignant lymphomas of mucosa-associated lymphoid tissue type,” American Journal of Pathology, vol. 153, no. 3, pp. 689–694, 1998. View at Google Scholar · View at Scopus
  49. J. Krugmann, A. Tzankov, and A. Tzankov, “Complete or partial trisomy 3 in gastro-intestinal MALT lymphomas co-occurs with aberrations at 18q21 and correlates with advanced disease stage: a study on 25 cases,” World Journal of Gastroenterology, vol. 11, no. 46, p. 7384, 2005. View at Google Scholar · View at Scopus
  50. J. Krugmann, A. Tzankov, S. Dirnhofer, F. Fend, R. Greil, R. Siebert, and M. Erdel, “Unfavourable prognosis of patients with trisomy 18q21 detected by fluorescence in situ hybridisation in t(11;18) negative, surgically resected, gastrointestinal B cell lymphomas,” Journal of Clinical Pathology, vol. 57, no. 4, pp. 360–364, 2004. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Nakamura, T. Matsumoto, and T. Matsumoto, “Helicobacter pylori-negative gastric mucosa-associated lymphoid tissue lymphoma: a clinicopathologic and molecular study with reference to antibiotic treatment,” Cancer, vol. 107, no. 12, pp. 2770–2778, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. A. Rawal, W. G. Finn, B. Schnitzer, and R. Valdez, “Site-specific morphologic differences in extranodal marginal zone B-cell lymphomas,” Archives of Pathology and Laboratory Medicine, vol. 131, no. 11, pp. 1673–1678, 2007. View at Google Scholar · View at Scopus
  53. R. Lai, L. M. Weiss, K. L. Chang, and D. A. Arber, “Frequency of CD43 expression in non-Hodgkin lymphoma: a survey of 742 cases and further characterization of rare CD43+ follicular lymphomas,” American Journal of Clinical Pathology, vol. 111, no. 4, pp. 488–494, 1999. View at Google Scholar · View at Scopus
  54. E. D. Hsi, J. K. Greenson, T. P. Singleton, J. Siddiqui, B. Schnitzer, and C. W. Ross, “Detection of immunoglobulin heavy chain gene rearrangement by polymerase chain reaction in chronic active gastritis associated with Helicobacter pylori,” Human Pathology, vol. 27, no. 3, pp. 290–296, 1996. View at Publisher · View at Google Scholar · View at Scopus
  55. S. D. Georgopoulos, K. Triantafyllou, M. Fameli, P. Kitsanta, C. Spiliadi, D. Anagnostou, and S. D. Ladas, “Molecular analysis of B-cell clonality in Helicobacter pylori gastritis,” Digestive Diseases and Sciences, vol. 50, no. 9, pp. 1616–1620, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. J. N. Steiff, A. Neubauer, M. Stolte, and T. Wündisch, “Clonality analyses in gastric MALT (mucosa-associated lymphoid tissue),” Pathology Research and Practice, vol. 202, no. 7, pp. 503–507, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. C. Montalban, A. Santón, and A. Santón, “Long-term persistence of molecular disease after histological remission in low-grade gastric MALT lymphoma treated with H. pylori eradication. Lack of association with translocation t(11;18): a 10-year updated follow-up of a prospective study,” Annals of Oncology, vol. 16, no. 9, pp. 1539–1544, 2005. View at Publisher · View at Google Scholar · View at PubMed
  58. T. Wündisch, C. Thiede, and C. Thiede, “Long-term follow-up of gastric MALT lymphoma after Helicobacter pylori eradication,” Journal of Clinical Oncology, vol. 23, no. 31, pp. 8018–8024, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  59. H. Suzuki, Y. Saito, and T. Hibi, “Helicobacter pylori and gastric mucosa-associated lymphoid tissue (MALT) lymphoma: updated review of clinical outcomes and the molecular pathogenesis,” Gut and Liver, vol. 3, no. 2, pp. 81–87, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. C. Montalban and F. Norman, “Treatment of gastric mucosa-associated lymphoid tissue lymphoma: Helicobacter pylori eradication and beyond,” Expert Review of Anticancer Therapy, vol. 6, no. 3, pp. 361–371, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. M. Lévy, C. Copie-Bergman, and C. Copie-Bergman, “Treatment of t(11;18)-positive gastric mucosa-associated lymphoid tissue lymphoma with rituximab and chlorambucil: clinical, histological, and molecular follow-up,” Leukemia and Lymphoma, vol. 51, no. 2, pp. 284–290, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. S. Nakamura, T. Matsumoto, and T. Matsumoto, “Long-term clinical outcome of Helicobacter pylori eradication for gastric mucosa-associated lymphoid tissue lymphoma with a reference to second-line treatment,” Cancer, vol. 104, no. 3, pp. 532–540, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. W. Fischbach, M. E. Goebeler-Kolve, B. Dragosics, A. Greiner, and M. Stolte, “Long term outcome of patients with gastric marginal zone B cell lymphoma of mucosa associated lymphoid tissue (MALT) following exclusive Helicobacter pylori eradication therapy: experience from a large prospective series,” Gut, vol. 53, no. 1, pp. 34–37, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. W. Fischbach, M. E. Goebeler, A. Ruskone-Fourmestraux, T. Wündisch, A. Neubauer, M. Raderer, and A. Savio, “Most patients with minimal histological residuals of gastric MALT lymphoma after successful eradication of Helicobacter pylori can be managed safely by a watch and wait strategy: experience from a large international series,” Gut, vol. 56, no. 12, pp. 1685–1687, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  65. S.-H. Kuo, L.-T. Chen, and L.-T. Chen, “Long-term follow-up of gastrectomized patients with mucosa-associated lymphoid tissue lymphoma: need for a revisit of surgical treatment,” Annals of Surgery, vol. 247, no. 2, pp. 265–269, 2008. View at Publisher · View at Google Scholar · View at PubMed