Unraveling effector functions of B cells during infection: The hidden world beyond antibody production

Infectious Disorders - Drug Targets

Volumn 12, Issue 3, 2012, Pages 213-221

  León, Beatriz ^a   Ballesteros Tato, André ^a   Misra, Ravi S ^a   Wojciechowski, Wojciech ^a   Lund, Frances E ^a,b  

^a University of Alabama at Birmingham   (United States)

^b NONE   (United States)

Author keywords

Antibody; Antigen presentation; B lymphocytes; Cytokines; Infectious disease

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR; INTERLEUKIN 6; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; VASCULOTROPIN A;

ANTIBODY PRODUCTION; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELLULAR IMMUNITY; CHLAMYDIASIS; CYTOKINE PRODUCTION; DENDRITIC CELL; HELIGMOSOMOIDES POLYGYRUS; HEMATOPOIETIC CELL; HUMAN; HUMORAL IMMUNE DEFICIENCY; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFECTION; LEISHMANIASIS; LYMPH VESSEL; MICROENVIRONMENT; NONHUMAN; PATHOGENESIS; PLASMODIUM CHABAUDI INFECTION; PNEUMOCYSTOSIS; REVIEW; SALMONELLOSIS; TYPHOID FEVER; WILD TYPE;

EID: 84861171827     PISSN: 18715265     EISSN: 18755852     Source Type: Journal    
DOI: 10.2174/187152612800564437     Document Type: Review

References (95)

1. Sallusto, F.; Lanzavecchia, A.; Araki, K.; Ahmed, R. From vaccines to memory and back. Immunity, 2010, 33(4), 451-463.
2. Drolet, J. P.; Frangie, H.; Guay, J.; Hajoui, O.; Hamid, Q.; Mazer, B. D. B lymphocytes in inflammatory airway diseases. Clin. Exp. Allergy, 2010, 40(6), 841-849.
3. Townsend, M. J.; Monroe, J. G.; Chan, A. C. B-cell targeted therapies in human autoimmune diseases: an updated perspective. Immunol. Rev., 2010, 237(1), 264-283.
4. Brundler, M. A.; Aichele, P.; Bachmann, M.; Kitamura, D.; Rajewsky, K.; Zinkernagel, R. M. Immunity to viruses in B celldeficient mice: influence of antibodies on virus persistence and on T cell memory. Eur. J. Immunol., 1996, 26(9), 2257-2262.
5. Elkins, K. L.; Bosio, C. M.; Rhinehart-Jones, T. R. Importance of B cells, but not specific antibodies, in primary and secondary protective immunity to the intracellular bacterium Francisella tularensis live vaccine strain. Infection and immunity, 1999, 67(11), 6002-6007.
6. Kang, H.; Remington, J. S.; Suzuki, Y. Decreased resistance of B cell-deficient mice to infection with Toxoplasma gondii despite unimpaired expression of IFN-gamma, TNF-alpha, and inducible nitric oxide synthase. Journal, of immunology, 2000, 164(5), 2629-2634.
7. Leef, M.; Elkins, K. L.; Barbic, J.; Shahin, R. D. Protective immunity to Bordetella pertussis requires both B cells and CD4(+) T cells for key functions other than specific antibody production. The Journal of experimental medicine, 2000, 191(11), 1841-1852.
8. Lund, F. E.; Schuer, K.; Hollifield, M.; Randall, T. D.; Garvy, B. A., Clearance of Pneumocystis carinii in mice is dependent on B cells but not on P carinii-specific antibody. Journal of immunology, 2003, 171(3), 1423-1430.
9. Mastroeni, P.; Simmons, C.; Fowler, R.; Hormaeche, C. E.; Dougan, G. Igh-6(-/-) (B-cell-deficient) mice fail to mount solid acquired resistance to oral challenge with virulent Salmonella enterica serovar typhimurium and show impaired Th1 T-cell responses to Salmonella antigens. Infection and immunity, 2000, 68(1), 46-53.
10. Lee, B. O.; Rangel-Moreno, J.; Moyron-Quiroz, J. E.; Hartson, L.; Makris, M.; Sprague, F.; Lund, F. E.; Randall, T. D., CD4 T cellindependent antibody response promotes resolution of primary influenza infection and helps to prevent reinfection. J. Immunol., 2005, 175(9), 5827-5838.
11. Serreze, D. V.; Chapman, H. D.; Varnum, D. S.; Hanson, M. S.; Reifsnyder, P. C.; Richard, S. D.; Fleming, S. A.; Leiter, E. H.; Shultz, L. D. B lymphocytes are essential for the initiation of T cell-mediated autoimmune diabetes: analysis of a new "speed congenic" stock of NOD. Ig mu null mice. The Journal of experimental medicine, 1996, 184(5), 2049-2053.
12. Akashi, T.; Nagafuchi, S.; Anzai, K.; Kondo, S.; Kitamura, D.; Wakana, S.; Ono, J.; Kikuchi, M.; Niho, Y.; Watanabe, T. Direct evidence for the contribution of B cells to the progression of insulitis and the development of diabetes in non-obese diabetic mice. International immunology, 1997, 9(8), 1159-1164.
13. Chan, O. T.; Hannum, L. G.; Haberman, A. M.; Madaio, M. P.; Shlomchik, M. J. A novel mouse with B cells but lacking serum antibody reveals an antibody-independent role for B cells in murine lupus. J. Exp. Med., 1999, 189(10), 1639-1648.
14. Yu, S.; Maiti, P. K.; Dyson, M.; Jain, R.; Braley-Mullen, H. B celldeficient NOD. H-2h4 mice have CD4+CD25+ T regulatory cells that inhibit the development of spontaneous autoimmune thyroiditis. The Journal of experimental medicine, 2006, 203(2), 349-358.
15. Robinson, C. P.; Brayer, J.; Yamachika, S.; Esch, T. R.; Peck, A. B.; Stewart, C. A.; Peen, E.; Jonsson, R.; Humphreys-Beher, M. G. Transfer of human serum IgG to nonobese diabetic Igmu null mice reveals a role for autoantibodies in the loss of secretory function of exocrine tissues in Sjogren's syndrome. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(13), 7538-7543.
16. Dorner, T.; Isenberg, D.; Jayne, D.; Wiendl, H.; Zillikens, D.; Burmester, G. Current status on B-cell depletion therapy in autoimmune diseases other than rheumatoid arthritis. Autoimmun Rev., 2009, 9(2), 82-89.
17. Davidson, A. Targeting BAFF in autoimmunity. Curr. Opin. Immunol., 2010, 22(6), 732-739.
18. Liossis, S. N.; Sfikakis, P. P. Rituximab-induced B cell depletion in autoimmune diseases: potential effects on T cells. Clin. Immunol., 2008, 127(3), 280-285.
19. Levesque, M. C.; St Clair, E. W. B cell-directed therapies for autoimmune disease and correlates of disease response and relapse. J. Allergy Clin. Immunol., 2008, 121(1), 13-21; quiz 22-23.
20. Looney, R. J.; Anolik, J. H.; Campbell, D.; Felgar, R. E.; Young, F.; Arend, L. J.; Sloand, J. A.; Rosenblatt, J.; Sanz, I., B cell depletion as a novel treatment for systemic lupus erythematosus: a phase I/II dose-escalation trial of rituximab. Arthritis and rheumatism, 2004, 50(8), 2580-2589.
21. Anolik, J. H.; Barnard, J.; Cappione, A.; Pugh-Bernard, A. E.; Felgar, R. E.; Looney, R. J.; Sanz, I. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis and rheumatism, 2004, 50(11), 3580-3590.
22. Oracki, S. A.; Walker, J. A.; Hibbs, M. L.; Corcoran, L. M.; Tarlinton, D. M., Plasma cell development and survival. Immunol. Rev., 2010, 237(1), 140-159.
23. Nimmerjahn, F.; Ravetch, J. V., Antibody-mediated modulation of immune responses. Immunol. Rev., 2010, 236, 265-275.
24. Di Rosa, F.; Matzinger, P., Long-lasting CD8 T cell memory in the absence of CD4 T cells or B cells. J. Exp. Med., 1996, 183(5), 2153-2163.
25. Epstein, M. M.; Di Rosa, F.; Jankovic, D.; Sher, A.; Matzinger, P. Successful T cell priming in B cell-deficient mice. J. Exp. Med., 1995, 182(4), 915-922.
26. Phillips, J. A.; Romball, C. G.; Hobbs, M. V.; Ernst, D. N.; Shultz, L.; Weigle, W. O., CD4+ T cell activation and tolerance induction in B cell knockout mice. J. Exp. Med., 1996, 183(4), 1339-1344.
27. van Essen, D.; Dullforce, P.; Brocker, T.; Gray, D. Cellular interactions involved in Th cell memory. J. Immunol., 2000, 165(7), 3640-3646.
28. Williams, G. S.; Oxenius, A.; Hengartner, H.; Benoist, C.; Mathis, D. CD4+ T cell responses in mice lacking MHC class II molecules specifically on B cells. Eur. J. Immunol., 1998, 28(11), 3763-3772.
29. Asano, M. S.; Ahmed, R. CD8 T cell memory in B cell-deficient mice. J. Exp. Med., 1996, 183(5), 2165-2174.
30. Shen, H.; Whitmire, J. K.; Fan, X.; Shedlock, D. J.; Kaech, S. M.; Ahmed, R. A specific role for B cells in the generation of CD8 T cell memory by recombinant Listeria monocytogenes. J. Immunol., 2003, 170(3), 1443-1451.
31. Topham, D. J.; Tripp, R. A.; Hamilton-Easton, A. M.; Sarawar, S. R.; Doherty, P. C. Quantitative analysis of the influenza virusspecific CD4+ T cell memory in the absence of B cells and Ig. J. Immunol., 1996, 157(7), 2947-2952.
32. Lund, F. E.; Garvy, B. A.; Randall, T. D.; Harris, D. P. Regulatory roles for cytokine-producing B cells in infection and autoimmune disease. Curr. Dir. Autoimmun., 2005, 8, 25-54.
33. Yang, X.; Brunham, R. C. Gene knockout B cell-deficient mice demonstrate that B cells play an important role in the initiation of T cell responses to Chlamydia trachomatis (mouse pneumonitis) lung infection. J. Immunol., 1998, 161(3), 1439-1446.
34. Langhorne, J.; Cross, C.; Seixas, E.; Li, C.; von der Weid, T. A role for B cells in the development of T cell helper function in a malaria infection in mice. Proc. Natl. Acad. Sci. USA, 1998, 95(4), 1730-1734.
35. Ronet, C.; Voigt, H.; Himmelrich, H.; Doucey, M. A.; Hauyon-La Torre, Y.; Revaz-Breton, M.; Tacchini-Cottier, F.; Bron, C.; Louis, J.; Launois, P. Leishmania major-specific B cells are necessary for Th2 cell development and susceptibility to L. major LV39 in BALB/c mice. J. Immunol., 2008, 180(7), 4825-4835.
36. Whitmire, J. K.; Asano, M. S.; Kaech, S. M.; Sarkar, S.; Hannum, L. G.; Shlomchik, M. J.; Ahmed, R. Requirement of B cells for generating CD4+ T cell memory. J. Immunol., 2009, 182(4), 1868-1876.
37. Ngo, V. N.; Cornall, R. J.; Cyster, J. G. Splenic T zone development is B cell dependent. J. Exp. Med., 2001, 194(11), 1649-1660.
38. Joao, C.; Ogle, B. M.; Gay-Rabinstein, C.; Platt, J. L.; Cascalho, M. B cell-dependent TCR diversification. J Immunol., 2004, 172(8), 4709-4716.
39. Golovkina, T. V.; Shlomchik, M.; Hannum, L.; Chervonsky, A. Organogenic role of B lymphocytes in mucosal immunity. Science, 1999, 286(5446), 1965-1968.
40. Ngo, V. N.; Korner, H.; Gunn, M. D.; Schmidt, K. N.; Riminton, D. S.; Cooper, M. D.; Browning, J. L.; Sedgwick, J. D.; Cyster, J. G. Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen. J. Exp. Med., 1999, 189(2), 403-412.
41. Fu, Y. X.; Huang, G.; Wang, Y.; Chaplin, D. D. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin alpha-dependent fashion. J. Exp. Med., 1998, 187(7), 1009-1018.
42. Endres, R.; Alimzhanov, M. B.; Plitz, T.; Futterer, A.; Kosco-Vilbois, M. H.; Nedospasov, S. A.; Rajewsky, K.; Pfeffer, K. Mature follicular dendritic cell networks depend on expression of lymphotoxin beta receptor by radioresistant stromal cells and of lymphotoxin beta and tumor necrosis factor by B cells. J. Exp. Med., 1999, 189(1), 159-168.
43. Wang, Y. G.; Kim, K. D.; Wang, J.; Yu, P.; Fu, Y. X. Stimulating lymphotoxin beta receptor on the dendritic cells is critical for their homeostasis and expansion. J. Immunol., 2005, 175(10), 6997-7002.
44. Kabashima, K.; Banks, T. A.; Ansel, K. M.; Lu, T. T.; Ware, C. F.; Cyster, J. G. Intrinsic lymphotoxin-beta receptor requirement for homeostasis of lymphoid tissue dendritic cells. Immunity, 2005, 22(4), 439-450.
45. Finkelman, F. D.; Shea-Donohue, T.; Goldhill, J.; Sullivan, C. A.; Morris, S. C.; Madden, K. B.; Gause, W. C.; Urban, J. F., Jr. Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol., 1997, 15, 505-533.
46. Wojciechowski, W.; Harris, D. P.; Sprague, F.; Mousseau, B.; Makris, M.; Kusser, K.; Honjo, T.; Mohrs, K.; Mohrs, M.; Randall, T.; Lund, F. E., Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity, 2009, 30(3), 421-433.
47. Randolph, G. J.; Angeli, V.; Swartz, M. A. Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat. Rev. Immunol., 2005, 5(8), 617-628.
48. von Andrian, U. H.; M'Rini, C. In situ analysis of lymphocyte migration to lymph nodes. Cell Adhes. Commun., 1998, 6(2-3), 85-96.
49. Liao, S.; Ruddle, N. H. Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J. Immunol., 2006, 177(5), 3369-3379.
50. Angeli, V.; Ginhoux, F.; Llodra, J.; Quemeneur, L.; Frenette, P. S.; Skobe, M.; Jessberger, R.; Merad, M.; Randolph, G. J. B celldriven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity, 2006, 24(2), 203-215.
51. Kumar, V.; Scandella, E.; Danuser, R.; Onder, L.; Nitschke, M.; Fukui, Y.; Halin, C.; Ludewig, B.; Stein, J. V. Global lymphoid tissue remodeling during a viral infection is orchestrated by a B cell-lymphotoxin-dependent pathway. Blood, 2010, 115(23), 4725-4733.
52. Worm, M.; Geha, R. S. CD40 ligation induces lymphotoxin alpha gene expression in human B cells. Int. Immunol., 1994, 6(12), 1883-1890.
53. Villadangos, J. A.; Schnorrer, P., Intrinsic and cooperative antigenpresenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol., 2007, 7(7), 543-555.
54. Lanzavecchia, A. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes. Annual review of immunology, 1990, 8, 773-793.
55. Malynn, B. A.; Romeo, D. T.; Wortis, H. H. Antigen-specific B cells efficiently present low doses of antigen for induction of T cell proliferation. J. Immunol., 1985, 135(2), 980-988.
56. Lund, F. E.; Hollifield, M.; Schuer, K.; Lines, J. L.; Randall, T. D.; Garvy, B. A. B cells are required for generation of protective effector and memory CD4 cells in response to Pneumocystis lung infection. J. Immunol., 2006, 176(10), 6147-6154.
57. Barr, T. A.; Brown, S.; Mastroeni, P.; Gray, D. TLR and B cell receptor signals to B cells differentially program primary and memory Th1 responses to Salmonella enterica. J. Immunol., 2010, 185(5), 2783-2789.
58. Fillatreau, S.; Gray, D. T cell accumulation in B cell follicles is regulated by dendritic cells and is independent of B cell activation. J. Exp. Med., 2003, 197(2), 195-206.
59. King, C.; Tangye, S. G.; Mackay, C. R. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol., 2008, 26, 741-766.
60. Zaretsky, A. G.; Taylor, J. J.; King, I. L.; Marshall, F. A.; Mohrs, M.; Pearce, E. J. T follicular helper cells differentiate from Th2 cells in response to helminth antigens. J. Exp. Med., 2009, 206(5), 991-999.
61. Johnston, R. J.; Poholek, A. C.; DiToro, D.; Yusuf, I.; Eto, D.; Barnett, B.; Dent, A. L.; Craft, J.; Crotty, S. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cell differentiation. Science, 2009, 325(5943), 1006-1010.
62. Haynes, N. M.; Allen, C. D.; Lesley, R.; Ansel, K. M.; Killeen, N.; Cyster, J. G. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol., 2007, 179(8), 5099-5108.
63. Deenick, E. K.; Chan, A.; Ma, C. S.; Gatto, D.; Schwartzberg, P. L.; Brink, R.; Tangye, S. G. Follicular helper T cell differentiation requires continuous antigen presentation that is independent of unique B cell signaling. Immunity, 2010, 33(2), 241-253.
64. Crotty, S., Follicular Helper CD4 T Cells (T(FH). Annu. Rev. Immunol., 2011, 29, 621-663.
65. Pelletier, N.; McHeyzer-Williams, L. J.; Wong, K. A.; Urich, E.; Fazilleau, N.; McHeyzer-Williams, M. G. Plasma cells negatively regulate the follicular helper T cell program. Nat. Immunol., 2010, 11(12), 1110-1118.
66. Agrawal, S.; Gupta, S., TLR1/2, TLR7, and TLR9 Signals Directly Activate Human Peripheral Blood Naive and Memory B Cell Subsets to Produce Cytokines, Chemokines, and Hematopoietic Growth Factors. J. Clin. Immunol., 2011, 31(1), 89-98.
67. Barr, T. A.; Brown, S.; Ryan, G.; Zhao, J.; Gray, D. TLR-mediated stimulation of APC: Distinct cytokine responses of B cells and dendritic cells. Eur. J. Immunol., 2007, 37(11), 3040-3053.
68. Yanaba, K.; Bouaziz, J. D.; Haas, K. M.; Poe, J. C.; Fujimoto, M.; Tedder, T. F. A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity, 2008, 28(5), 639-650.
69. Yanaba, K.; Bouaziz, J. D.; Matsushita, T.; Tsubata, T.; Tedder, T. F., The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J. Immunol., 2009, 182(12), 7459-7472.
70. Ganapamo, F.; Dennis, V. A.; Philipp, M. T. CD19(+) cells produce IFN-gamma in mice infected with Borrelia burgdorferi. Eur. J. Immunol., 2001, 31(12), 3460-3468.
71. Harris, D. P.; Haynes, L.; Sayles, P. C.; Duso, D. K.; Eaton, S. M.; Lepak, N. M.; Johnson, L. L.; Swain, S. L.; Lund, F. E. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat. Immunol., 2000, 1(6), 475-482.
72. Lieberman, L. A.; Hunter, C. A. The role of cytokines and their signaling pathways in the regulation of immunity to Toxoplasma gondii. Int. Rev. Immunol., 2002, 21(4-5), 373-403.
73. Harris, D. P.; Goodrich, S.; Gerth, A. J.; Peng, S. L.; Lund, F. E. Regulation of IFN-gamma production by B effector 1 cells: essential roles for T-bet and the IFN-gamma receptor. J. Immunol., 2005, 174(11), 6781-6790.
74. Harris, D. P.; Goodrich, S.; Mohrs, K.; Mohrs, M.; Lund, F. E. 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., 2005, 175(11), 7103-7107.
75. Durali, D.; de Goer de Herve, M. G.; Giron-Michel, J.; Azzarone, B.; Delfraissy, J. F.; Taoufik, Y. In human B cells, IL-12 triggers a cascade of molecular events similar to Th1 commitment. Blood, 2003, 102(12), 4084-4089.
76. Yoshimoto, T.; Okamura, H.; Tagawa, Y. I.; Iwakura, Y.; Nakanishi, K. Interleukin 18 together with interleukin 12 inhibits IgE production by induction of interferon-gamma production from activated B cells. Proc. Natl. Acad. Sci. USA, 1997, 94(8), 3948-3953.
77. Mauri, C.; Blair, P. A. Regulatory B cells in autoimmunity: developments and controversies. Nat. Rev. Rheumatol., 2010, 6(11), 636-643.
78. DiLillo, D. J.; Matsushita, T.; Tedder, T. F. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. N.Y. Acad. Sci., 2010, 1183, 38-57.
79. Evans, J. G.; Chavez-Rueda, K. A.; Eddaoudi, A.; Meyer-Bahlburg, A.; Rawlings, D. J.; Ehrenstein, M. R.; Mauri, C. Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol., 2007, 178(12), 7868-7878.
80. Yang, M.; Sun, L.; Wang, S.; Ko, K. H.; Xu, H.; Zheng, B. J.; Cao, X.; Lu, L. Novel function of B cell-activating factor in the induction of IL-10-producing regulatory B cells. J. Immunol., 2010, 184(7), 3321-3325.
81. Menard, L. C.; Minns, L. A.; Darche, S.; Mielcarz, D. W.; Foureau, D. M.; Roos, D.; Dzierszinski, F.; Kasper, L. H.; Buzoni-Gatel, D. B cells amplify IFN-gamma production by T cells via a TNF-alphamediated mechanism. J. Immunol., 2007, 179(7), 4857-4866.
82. Amu, S.; Saunders, S. P.; Kronenberg, M.; Mangan, N. E.; Atzberger, A.; Fallon, P. G. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J. Allergy Clin. Immunol., 2010, 125(5), 1114-1124 e8.
83. Wilson, M. S.; Taylor, M. D.; O'Gorman, M. T.; Balic, A.; Barr, T. A.; Filbey, K.; Anderton, S. M.; Maizels, R. M. Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur. J. Immunol., 2010, 40(6), 1682-1696.
84. Moulin, V.; Andris, F.; Thielemans, K.; Maliszewski, C.; Urbain, J.; Moser, M. B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B celldeficient mice results in T helper cell type 1 deviation. J. Exp. Med., 2000, 192(4), 475-482.
85. Sacks, D.; Noben-Trauth, N. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol., 2002, 2(11), 845-858.
86. Noben-Trauth, N.; Lira, R.; Nagase, H.; Paul, W. E.; Sacks, D. L. The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J. Immunol., 2003, 170(10), 5152-5158.
87. Ronet, C.; Hauyon-La Torre, Y.; Revaz-Breton, M.; Mastelic, B.; Tacchini-Cottier, F.; Louis, J.; Launois, P. Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production. J. Immunol., 2010, 184(2), 886-894.
88. Pistoia, V. Production of cytokines by human B cells in health and disease. Immunology today, 1997, 18(7), 343-350.
89. Duddy, M.; Niino, M.; Adatia, F.; Hebert, S.; Freedman, M.; Atkins, H.; Kim, H. J.; Bar-Or, A. Distinct effector cytokine profiles of memory and naive human B cell subsets and implication in multiple sclerosis. Journal of immunology, 2007, 178(10), 6092-6099.
90. Duddy, M. E.; Alter, A.; Bar-Or, A. Distinct profiles of human B cell effector cytokines: a role in immune regulation? Journal of immunology, 2004, 172(6), 3422-3427.
91. Airoldi, I.; Gri, G.; Marshall, J. D.; Corcione, A.; Facchetti, P.; Guglielmino, R.; Trinchieri, G.; Pistoia, V. Expression and function of IL-12 and IL-18 receptors on human tonsillar B cells. Journal of immunology, 2000, 165(12), 6880-6888.
92. Gagro, A.; Servis, D.; Cepika, A. M.; Toellner, K. M.; Grafton, G.; Taylor, D. R.; Branica, S.; Gordon, J. Type I cytokine profiles of human naive and memory B lymphocytes: a potential for memory cells to impact polarization. Immunology, 2006, 118(1), 66-77.
93. Jagannathan, M.; Hasturk, H.; Liang, Y.; Shin, H.; Hetzel, J. T.; Kantarci, A.; Rubin, D.; McDonnell, M. E.; Van Dyke, T. E.; Ganley-Leal, L. M.; Nikolajczyk, B. S., TLR cross-talk specifically regulates cytokine production by B cells from chronic inflammatory disease patients. J. Immunol., 2009, 183(11), 7461-7470.
94. Bar-Or, A.; Fawaz, L.; Fan, B.; Darlington, P. J.; Rieger, A.; Ghorayeb, C.; Calabresi, P. A.; Waubant, E.; Hauser, S. L.; Zhang, J.; Smith, C. H. Abnormal B-cell cytokine responses a trigger of Tcell-mediated disease in MS? Ann. Neurol., 2010, 67(4), 452-461.
95. Hajoui, O.; Janani, R.; Tulic, M.; Joubert, P.; Ronis, T.; Hamid, Q.; Zheng, H.; Mazer, B. D. Synthesis of IL-13 by human B lymphocytes: regulation and role in IgE production. The Journal of allergy and clinical immunology, 2004, 114(3), 657-663.