Anti-CXCL13 antibody can inhibit the formation of gastric lymphoid follicles induced by Helicobacter infection

Mucosal Immunology

Volumn 7, Issue 5, 2014, Pages 1244-1254

  Yamamoto, K ^a   Nishiumi, S ^a   Yang, L ^a   Klimatcheva, E ^b   Pandina, T ^b   Takahashi, S ^c   Matsui, H ^d   Nakamura, M ^d   Zauderer, M ^b   Yoshida, M ^a,e   Azuma, T ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b VACCINEX INC   (United States)

^c KYORIN UNIVERSITY   (Japan)

^d KITASATO UNIVERSITY   (Japan)

^e KOBE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL13 ANTIBODY; CXCL13 CHEMOKINE; CYTOKINE ANTIBODY; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VACCINEX; CXCL13 PROTEIN, MOUSE; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; BACTERIAL CLEARANCE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DISEASE ASSOCIATION; DRUG EFFECT; FOLLICULAR DENDRITIC CELL; GENE EXPRESSION REGULATION; GERMINAL CENTER; HELICOBACTER; HELICOBACTER INFECTION; HELICOBACTER SUIS; INTESTINE LYMPHATIC TISSUE; LYMPH FOLLICLE; MARGINAL ZONE LYMPHOMA; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STOMACH LYMPHOMA; TREATMENT DURATION; TREATMENT RESPONSE; ANIMAL; DRUG EFFECTS; GASTRIC MUCOSA; GASTRITIS; HELICOBACTER HEILMANNII; IMMUNOLOGY; MICROBIOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; POLYMERASE CHAIN REACTION;

ANIMALS; ANTIBODIES, MONOCLONAL; CHEMOKINE CXCL13; GASTRIC MUCOSA; GASTRITIS; GENE EXPRESSION REGULATION; HELICOBACTER HEILMANNII; HELICOBACTER INFECTIONS; LYMPHOMA, B-CELL, MARGINAL ZONE; MICE; POLYMERASE CHAIN REACTION;

EID: 84903936591     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.14     Document Type: Article

References (56)

1. De Groote., D. et al. 'Candidatus Helicobacter suis', a gastric helicobacter from pigs, and its phylogenetic relatedness to other gastrospirilla. Int. J. Syst. Bacteriol. 49, 1769-1777 (1999).
2. Priestnall, S.L. et al. Evaluation of & quot;Helicobacter heilmannii"subtypes in the gastric mucosa of cats and dogs. J. Clin.Microbiol. 42, 2144-2151 (2004).
3. Haesebrouck, F. et al. Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health. Clin. Microbiol. Rev. 22, 202-223 (2009).
4. Meining, A., Kroher, G. & Stolte, M. Animal reservoirs in the transmission of Helicobacter heilmannii. Results of a questionnaire-based study. Scand. J. Gastroenterol. 33, 795-798 (1998).
5. Hellemans, A. et al. Prevalence of 'Candidatus Helicobacter suis' in pigs of different ages. Vet. Rec. 161, 189-192 (2007).
6. Nakamura, M. et al. "Candidatus Helicobacter heilmannii" from a cynomolgus monkey induces gastric mucosa-associated lymphoid tissue lymphomas in C57BL/6 mice. Infect. Immun. 75, 1214-1222 (2007).
7. Morgner, A. et al. Helicobacter heilmannii associated primary gastric lowgrade MALT lymphoma: complete remission after curing the infection. Gastroenterology 118, 821-828 (2000).
8. Eidt, S., Stolte, M. & Fischer, R. Helicobacter pylori gastritis and primary gastric non-Hodgkin's lymphomas. J. Clin. Pathol. 47, 436-439 (1994).
9. Parsonnet, J. et al. Helicobacter pylori infection and the risk of gastric carcinoma. N. Engl. J. Med. 325, 1127-1131 (1991).
10. Wotherspoon, A.C., Ortiz-Hidalgo, C., Falzon, M.R. & Isaacson, P.G. Helicobacter pylori-associated gastritis and primary B-cell gastric lymphoma. Lancet 338, 1175-1176 (1991).
11. Nakamura, S. et al. Helicobacter pylori and primary gastric lymphoma. A histopathologic and immunohistochemical analysis of 237 patients. Cancer 79, 3-11 (1997).
12. Eidt, S. & Stolte, M. Prevalence of lymphoid follicles and aggregates in Helicobacter pylori gastritis in antral and body mucosa. J. Clin. Pathol. 46, 832-835 (1993).
13. Wyatt, J.I. & Rathbone, B.J. Immune response of the gastric mucosa to Campylobacter pylori. Scand. J. Gastroenterol. 142, 44-49 (1988).
14. Genta, R.M., Hamner, H.W. & Graham, D.Y. Gastric lymphoid follicles in Helicobacter pylori infection: frequency, distribution, and response to triple therapy. Hum. Pathol. 24, 577-558 (1993).
15. Gunn, M.D. et al. A B-cell-homing chemokine made in lymphoid follicles activates Burkitt's lymphoma receptor-1. Nature 391, 799-803 (1998).
16. Legler, D.F. et al. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BLR1/CXCR5. J. Exp. Med. 187, 655-660 (1998).
17. Ansel, K.M. et al. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406, 309-314 (2000).
18. Förster, R. et al. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87, 1037-1047 (1996).
19. Cyster, J.G., Ngo, V.N., Ekland, E.H., Gunn, M.D., Sedgwick, J.D. & Ansel, K.M. Chemokines and B-cell homing to follicles. Curr. Top. Microbiol. Immunol. 246, 87-92 (1999).
20. Amft, N. et al. Ectopic expression of theB cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjögren's syndrome. Arthritis Rheum. 44, 2633-2641 (2001).
21. Carlsen, H.S., Baekkevold, E.S., Johansen, F.E., Haraldsen, G. & Brandtzaeg, P. B cell attracting chemokine 1 (CXCL13) and its receptor CXCR5 are expressed in normal and aberrant gut associated lymphoid tissue. Gut 51, 364-371 (2002).
22. Magliozzi, R., Columba-Cabezas, S., Serafini, B. & Aloisi, F. Intracerebral expression of CXCL13 and BAFF is accompanied by formation of lymphoid follicle-like structures in the meninges of mice with relapsing experimental autoimmune encephalomyelitis. J. Neuroimmunol. 148, 11-23 (2004).
23. Luther, S.A., Lopez, T.,Bai,W., Hanahan,D. & Cyster, J.G.BLC expression in pancreatic islets causes B cell recruitment and lymphotoxindependent lymphoid neogenesis. Immunity 12, 471-481 (2000).
24. Takemura, S. et al. Lymphoid neogenesis in rheumatoid synovitis. J. Immunol. 167, 1072-1080 (2001).
25. Zheng, B. et al. CXCL13 neutralization reduces the severity of collageninduced arthritis. Arthritis Rheum. 52, 620-626 (2005).
26. Barone, F. et al. Association of CXCL13 and CCL21 expression with the progressive organization of lymphoid-like structures in Sjögren's syndrome. Arthritis Rheum. 52, 1773-1784 (2005).
27. Salomonsson, S. et al. Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjögren's syndrome. Scand. J. Immunol. 55, 336-342 (2002).
28. Oshima, C. et al. Induction of follicular gastritis following postthymectomy autoimmune gastritis in Helicobacter pylori-infected BALB/c mice. Infect. Immun. 68, 100-106 (2000).
29. Shomer, N.H., Fox, J.G., Juedes, A.E. & Ruddle, N.H. Helicobacterinduced chronic active lymphoid aggregates have characteristics of tertiary lymphoid tissue. Infect. Immun. 71, 3572-3577 (2003).
30. Mazzucchelli, L. et al. BCA-1 is highly expressed in Helicobacter pyloriinduced mucosa-associated lymphoid tissue and gastric lymphoma. J. Clin. Invest. 104, 49-54 (1999).
31. Nobutani, K. et al. Helicobacter heilmannii can induce gastric lymphoid follicles in mice via a Peyer's patch-independent pathway. FEMS Immunol. Med. Microbiol. 60, 156-164 (2010).
32. O'Rourke, J.L., Dixon, M.F., Jack, A., Enno, A. & Lee, A. Gastric B-cell mucosa-associated lymphoid tissue (MALT) lymphoma in an animal model of 'Helicobacter heilmannii' infection. J. Pathol. 203, 896-903 (2004).
33. Aloisi, F. & Pujol-Borrell, R. Lymphoid neogenesis in chronic inflammatory diseases. Nat. Rev. Immunol. 6, 205-217 (2006).
34. Suto, H., Katakai, T., Sugai, M., Kinashi, T. & Shimizu, A. CXCL13 production by an established lymph node stromal cell line via lymphotoxinbeta receptor engagement involves the cooperation of multiple signaling pathways. Int. Immunol. 21, 467-476 (2009).
35. Fu, Y.X. & Chaplin, D.D. Development and maturation of secondary lymphoid tissues. Annu. Rev. Immunol. 17, 399-433 (1999).
36. Matsumoto, M. Role of TNF ligand and receptor family in the lymphoid organogenesis defined by gene targeting. J. Med. Invest. 46, 141-150 (1999).
37. Pasparakis, M., Kousteni, S., Peschon, J. & Kollias, G. Tumor necrosis factor and the p55TNF receptor are required for optimal development of the marginal sinus and for migration of follicular dendritic cell precursors into splenic follicles. Cell Immunol. 201, 33-41 (2000).
38. Mimura, T. et al. IFN-g plays an essential role in the pathogenesis of gastric lymphoid follicles formation caused by Helicobacter suis infection. FEMS Immunol. Med. Microbiol. 63, 25-34 (2011).
39. Okiyama, Y., Matsuzawa, K., Hidaka, E., Sano, K., Akamatsu, T. & Ota, H. Helicobacter heilmannii infection: clinical, endoscopic and histopathological features in Japanese patients. Pathol. Int. 55, 398-404 (2005).
40. Forne, M. et al. Accuracy of an enzyme immunoassay for the detection of Helicobacter pylori in stool specimens in the diagnosis of infection and posttreatment check-up. Am. J. Gastroenterol. 95, 2200-2205 (2000).
41. Slayman, Y.B. et al. Neonatal Fc receptor for IgG (FcRn) expressed in the gastric epithelium regulates bacterial infection in mice. Mucosal Immunol. 5, 87-98 (2012).
42. Sonoda, E. et al. Transforming growth factor b induces IgA production and acts additively with interleukin 5 for IgA production. J. Exp. Med. 170, 1415-1420 (1989).
43. Beagley, K.W. et al. Interleukins and IgA synthesis. Human and murine interleukin 6 induce high rate IgA secretion in IgA-committedBcells. J. Exp. Med. 169, 2133-2148 (1989).
44. Stolte, M., Wellens, E., Bethke, B., Ritter, M. & Eidt, H. Helicobacter heilmannii (formerly Gastrospirillum hominis) gastritis: an infection transmitted by animals? Scand. J. Gastroenterol. 29, 1061-1064 (1994).
45. Yamamoto, K. et al. Helicobacter suis KB1 derived from pig gastric lymphoid follicles induces the formation of gastric lymphoid follicles inmice through the activation of Bcells and CD4positive cells. Microbes Infect. 13, 697-708 (2011).
46. Winter, S. et al. The chemokine receptor CXCR5 is pivotal for ectopic mucosa-associated lymphoid tissue neogenesis in chronic Helicobacter pylori-induced inflammation. J. Mol. Med. 88, 1169-1180 (2010).
47. Yoshida, M. et al. Human neonatal Fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20, 769-783 (2004).
48. Woof, J.M. & Mestecky, J. Mucosal immunoglobulins. Immunol. Rev. 206, 64-82 (2005).
49. Fagarasan, S., Kinoshita, K., Muramatsu, M., Ikuta, K. & Honjo, T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413, 639-643 (2001).
50. Suzuki, K., Meek, B., Doi, Y., Honjo, T. & Fagarasan, S. Two distinctive pathways for recruitment of naive and primed IgM+ B cells to the gut lamina propria. Proc. Natl. Acad. Sci. USA 102, 2482-2486 (2005).
51. Uematsu, S. et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9, 769-776 (2008).
52. Park, J.H., Seok, S.H., Baek, M.W., Lee, H.Y., Kim, D.J. & Park, J.H. Gastric lesions and immune responses caused by long-term infection with Helicobacter heilmannii in C57BL/6 mice. J. Comp. Pathol. 139, 208-217 (2008).
53. Shirai, Y. et al. Induction and maintenance of immune effector cells in the gastric tissue of mice orally immunized to Helicobacter pylori requires salivary glands. Gastroenterology 118, 749-759 (2000).
54. Cerutti, A. et al. CD40 ligand and appropriate cytokines induce switching to IgG, IgA, and IgE and coordinated germinal center and plasmacytoid phenotypic differentiation in a human monoclonal IgM+IgD+ B cell line. J. Immunol. 160, 2145-2157 (1998).
55. He, B. et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26, 812-826 (2007).
56. Baele, M. et al. Multiplex PCR assay for differentiation of Helicobacter felis, H. bizzozeronii, and H. salomonis. J. Clin. Microbiol. 42, 1115-1122 (2004).