B cells have distinct roles in host protection against different nematode parasites

Journal of Immunology

Volumn 184, Issue 9, 2010, Pages 5213-5223

  Liu, Qian ^a   Kreider, Timothy ^a   Bowdridge, Scott ^a   Liu, Zhugong ^a   Song, Youngmia ^a   Gaydo, Andrew G ^a   Urban Jr , Joseph F ^b   Gause, William C ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; CD4 ANTIGEN; CYTOKINE;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; BAGG ALBINO MOUSE; CELL TRANSFER; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; GENE EXPRESSION; HELIGMOSOMOIDES POLYGYRUS; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNITY; INOCULATION; MOUSE; MUCOSA; NEMATODE; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH2 CELL; WORM EXPULSION; ANIMAL; COMPARATIVE STUDY; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MOUSE MUTANT; NEMATOSPIROIDES DUBIUS; NIPPOSTRONGYLUS; PARASITOLOGY; PATHOLOGY; STRONGYLE INFECTION; TRANSPLANTATION;

ANIMALS; B-LYMPHOCYTE SUBSETS; FEMALE; HOST-PARASITE INTERACTIONS; IMMUNOLOGIC MEMORY; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; NEMATOSPIROIDES DUBIUS; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS; TH2 CELLS;

EID: 77954494295     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902879     Document Type: Article

References (40)

1. Hotez, P. J., P. J. Brindley, J. M. Bethony, C. H. King, E. J. Pearce, and J. Jacobson. 2008. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 118: 1311-1321.
2. Diemert, D. J., J. M. Bethony, and P. J. Hotez. 2008. Hookworm vaccines. Clin. Infect. Dis. 46: 282-288.
3. Scales, H. E., M. X. Ierna, and C. E. Lawrence. 2007. The role of IL-4, IL-13 and IL-4Ralpha in the development of protective and pathological responses to Trichinella spiralis. Parasite Immunol. 29: 81-91.
4. Finkelman, F. D., T. Shea-Donohue, S. C. Morris, L. Gildea, R. Strait, K. B. Madden, L. Schopf, and J. F. Urban, Jr. 2004. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201: 139-155.
5. Anthony, R. M., L. I. Rutitzky, J. F. Urban, Jr., M. J. Stadecker, and W. C. Gause. 2007. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7: 975-987.
6. Gause, W. C., J. F. Urban, Jr., and M. J. Stadecker. 2003. The immune response to parasitic helminths: insights from murine models. Trends Immunol. 24: 269-277.
7. Hernandez, H. J., Y. Wang, and M. J. Stadecker. 1997. In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation. J. Immunol. 158: 4832-4837.
8. Moulin, V., F. Andris, K. Thielemans, C. Maliszewski, J. Urbain, and M. Moser. 2000. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J. Exp. Med. 192: 475-482.
9. Blackwell, N. M., and K. J. Else. 2001. B cells and antibodies are required for resistance to the parasitic gastrointestinal nematode Trichuris muris. Infect. Immun. 69: 3860-3868.
10. Johansson-Lindbom, B., and C. A. Borrebaeck. 2002. Germinal center B cells constitute a predominant physiological source of IL-4: implication for Th2 development in vivo. J. Immunol. 168: 3165-3172.
11. Harris, D. P., S. Goodrich, K. Mohrs, M. Mohrs, and F. E. Lund. 2005. Cutting edge: the development of IL-4-producing B cells (B effector 2 cells) is controlled by IL-4, IL-4 receptor alpha, and Th2 cells. J. Immunol. 175: 7103-7107.
12. Lund, F. E. 2008. Cytokine-producing B lymphocytes-key regulators of immunity. Curr. Opin. Immunol. 20: 332-338.
13. Linton, P. J., B. Bautista, E. Biederman, E. S. Bradley, J. Harbertson, R. M. Kondrack, R. C. Padrick, and L. M. Bradley. 2003. Costimulation via OX40L expressed by B cells is sufficient to determine the extent of primary CD4 cell expansion and Th2 cytokine secretion in vivo. J. Exp. Med. 197: 875-883.
14. Lu, P., J. F. Urban, X. D. Zhou, S. J. Chen, K. Madden, M. Moorman, H. Nguyen, S. C. Morris, F. D. Finkelman, and W. C. Gause. 1996. CD40-mediated stimulation contributes to lymphocyte proliferation, antibody production, eosinophilia, and mastocytosis during an in vivo type 2 response, but is not required for T cell IL-4 production. J. Immunol. 156: 3327-3333.
15. Lu, P., X. Zhou, S. J. Chen, M. Moorman, S. C. Morris, F. D. Finkelman, P. Linsley, J. F. Urban, and W. C. Gause. 1994. CTLA-4 ligands are required to induce an in vivo interleukin 4 response to a gastrointestinal nematode parasite. J. Exp. Med. 180: 693-698.
16. Liu, Q., Z. Liu, C. T. Rozo, H. A. Hamed, F. Alem, J. F. Urban, Jr., and W. C. Gause. 2007. The role of B cells in the development of CD4 effector T cells during a polarized Th2 immune response. J. Immunol. 179: 3821-3830.
17. Linton, P. J., J. Harbertson, and L. M. Bradley. 2000. A critical role for B cells in the development of memory CD4 cells. J. Immunol. 165: 5558-5565.
18. McCoy, K. D., M. Stoel, R. Stettler, P. Merky, K. Fink, B. M. Senn, C. Schaer, J. Massacand, B. Odermatt, H. C. Oettgen, et al. 2008. Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4: 362-373.
19. Wojciechowski, W., D. P. Harris, F. Sprague, B. Mousseau, M. Makris, K. Kusser, T. Honjo, K. Mohrs, M. Mohrs, T. Randall, and F. E. Lund. 2009. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 30: 421-433.
20. Liu, Z., Q. Liu, J. Pesce, J. Whitmire, M. J. Ekkens, A. Foster, J. VanNoy, A. H. Sharpe, J. F. Urban, Jr., and W. C. Gause. 2002. Nippostrongylus brasiliensis can induce B7-independent antigen-specific development of IL-4-producing T cells from naive CD4 T cells in vivo. J. Immunol. 169: 6959-6968.
21. Anthony, R. M., J. F. Urban, Jr., F. Alem, H. A. Hamed, C. T. Rozo, J. L. Boucher, N. Van Rooijen, and W. C. Gause. 2006. Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12: 955-960.
22. Liu, Q., Z. Liu, J. Whitmire, F. Alem, H. Hamed, J. Pesce, J. F. Urban, Jr., and W. C. Gause. 2006. IL-18 stimulates IL-13-mediated IFN-gamma-sensitive host resistance in vivo. Eur. J. Immunol. 36: 1187-1198.
23. Urban, J. F., Jr., N. Noben-Trauth, D. D. Donaldson, K. B. Madden, S. C. Morris, M. Collins, and F. D. Finkelman. 1998. IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8: 255-264.
24. McKenzie, G. J., C. L. Emson, S. E. Bell, S. Anderson, P. Fallon, G. Zurawski, R. Murray, R. Grencis, and A. N. McKenzie. 1998. Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9: 423-432.
25. Finkelman, F. D., I. M. Katona, J. F. Urban, Jr., J. Holmes, J. Ohara, A. S. Tung, J. V. Sample, and W. E. Paul. 1988. IL-4 is required to generate and sustain in vivo IgE responses. J. Immunol. 141: 2335-2341.
26. Urban, J. F., Jr., I. M. Katona, and F. D. Finkelman. 1991. Heligmosomoides polygyrus: CD4+ but not CD8+ T cells regulate the IgE response and protective immunity in mice. Exp. Parasitol. 73: 500-511.
27. Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W. C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15: 505-533.
28. Urban, J. F., Jr., I. M. Katona, W. E. Paul, and F. D. Finkelman. 1991. Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proc. Natl. Acad. Sci. U.S.A. 88: 5513-5517.
29. Svetić, A., K. B. Madden, X. D. Zhou, P. Lu, I. M. Katona, F. D. Finkelman, J. F. Urban, Jr., and W. C. Gause. 1993. A primary intestinal helminthic infection rapidly induces a gut-associated elevation of Th2-associated cytokines and IL-3. J. Immunol. 150: 3434-3441.
30. Sfikakis, P. P., V. L. Souliotis, K. G. Fragiadaki, H. M. Moutsopoulos, J. N. Boletis, and A. N. Theofilopoulos. 2007. Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis. Clin. Immunol. 123: 66-73.
31. Hu, C. Y., D. Rodriguez-Pinto, W. Du, A. Ahuja, O. Henegariu, F. S. Wong, M. J. Shlomchik, and L. Wen. 2007. Treatment with CD20-specific antibody prevents and reverses autoimmune diabetes in mice. J. Clin. Invest. 117: 3857-3867.
32. Ekkens, M. J., Z. Liu, Q. Liu, J. Whitmire, S. Xiao, A. Foster, J. Pesce, J. VanNoy, A. H. Sharpe, J. F. Urban, and W. C. Gause. 2003. The role of OX40 ligand interactions in the development of the Th2 response to the gastrointestinal nematode parasite Heligmosomoides polygyrus. J. Immunol. 170: 384-393.
33. Coombes, J. L., and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435-446.
34. Saenz, S. A., B. C. Taylor, and D. Artis. 2008. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol. Rev. 226: 172-190.
35. Herbert, D. R., T. J. Nolan, G. A. Schad, and D. Abraham. 2002. The role of B cells in immunity against larval Strongyloides stercoralis in mice. Parasite Immunol. 24: 95-101.
36. Gu, Y., J. Li, X. Zhu, J. Yang, Q. Li, Z. Liu, S. Yu, and Y. Li. 2008. Trichinella spiralis: characterization of phage-displayed specific epitopes and their protective immunity in BALB/c mice. Exp. Parasitol. 118: 66-74.
37. Bethony, J., A. Loukas, M. Smout, S. Brooker, S. Mendez, J. Plieskatt, G. Goud, M. E. Bottazzi, B. Zhan, Y. Wang, et al. 2005. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB J. 19: 1743-1745.
38. Harris, N. L., I. Spoerri, J. F. Schopfer, C. Nembrini, P. Merky, J. Massacand, J. F. Urban, Jr., A. Lamarre, K. Burki, B. Odermatt, et al. 2006. Mechanisms of neonatal mucosal antibody protection. J. Immunol. 177: 6256-6262.
39. Ghosh, K., and P. J. Hotez. 1999. Antibody-dependent reductions in mouse hookworm burden after vaccination with Ancylostoma caninum secreted protein 1. J. Infect. Dis. 180: 1674-1681.
40. Patel, N., T. Kreider, J. F. Urban, Jr., and W. C. Gause. 2009. Characterisation of effector mechanisms at the host:parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int. J. Parasitol. 39: 13-21.