Marginal zone B cells exacerbate endotoxic shock via interleukin-6 secretion induced by Fcα/μR-coupled TLR4 signalling

Nature Communications

Volumn 7, Issue , 2016, Pages

  Honda, Shin Ichiro ^a   Sato, Kazuki ^a   Totsuka, Naoya ^a   Fujiyama, Satoshi ^a   Fujimoto, Manabu ^a   Miyake, Kensuke ^b   Nakahashi Oda, Chigusa ^a   Tahara Hanaoka, Satoko ^a   Shibuya, Kazuko ^a   Shibuya, Akira ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; FC RECEPTOR ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; OLIGOMER; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; FCALPHA-MU PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANTIBODY; BLOOD; CELLS AND CELL COMPONENTS; COLIFORM BACTERIUM; IMMUNE RESPONSE; PATHOGEN; POLYSACCHARIDE; PROTEIN; RODENT; SECRETION; SURVIVAL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE EXACERBATION; ESCHERICHIA COLI; FEMALE; IMMUNOPATHOGENESIS; MARGINAL ZONE B CELL; MOUSE; NONHUMAN; OLIGOMERIZATION; PROTEIN PROTEIN INTERACTION; SEPTIC SHOCK; SIGNAL TRANSDUCTION; SURVIVAL; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ANIMAL; C3H MOUSE; C57BL MOUSE; DRUG EFFECT; ESCHERICHIA COLI INFECTION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY; SECRETION (PROCESS);

MUS;

ANIMALS; B-LYMPHOCYTES; ESCHERICHIA COLI INFECTIONS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; NF-KAPPA B; RECEPTORS, FC; SHOCK, SEPTIC; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84966708361     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11498     Document Type: Article

References (48)

1. Bosmann, W. & Ward, P. A. The inflammatory response in sepsis. Trends Immunol. 34, 129-136 (2013).
2. Gentile, L. F. & Moldawer, L. L. DAMPs, PAMPs, and the origins of SIRS in bacterial sepsis. Shock 39, 113-114 (2013).
3. Beutler, R. & Rietschel, E. T. Innate immune sensing and its roots: the story of endotoxin. Nat. Rev. Immunol. 3, 169-176 (2003).
4. Martin, F., Oliver, A. & Kearney, J. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14, 617-629 (2001).
5. Balázs, M., Martin, F., Zhou, T. & Kearney, J. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17, 341-352 (2002).
6. Puga, I. et al. B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13, 170-180 (2012).
7. Martin, F. & Kearney, J. Marginal-zone B cells. Nat. Rev. Immunol. 2, 323-335 (2002).
8. Cerutti, A., Cols, M. & Puga, I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13, 118-132 (2013).
9. Tanigaki, K. et al. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immunol. 3, 443-450 (2002).
10. Rubtsov, A. et al. Lsc regulates marginal-zone B cell migration and adhesion and is required for the IgM T-dependent antibody response. Immunity 23, 527-538 (2005).
11. Guinamard, R., Okigaki, M., Schlessinger, J. & Ravetch, J. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1, 31-36 (2000).
12. Girkontaite, I. et al. Lsc is required for marginal zone B cells, regulation of lymphocyte motility and immune responses. Nat. Immunol. 2, 855-862 (2001).
13. Takai, T. Roles of Fc receptors in autoimmunity. Nat. Rev. Immunol. 2, 580-592 (2002).
14. Ravetch, J. V. & Clynes, R. A. Divergent roles for Fc receptors and complement in vivo. Annu. Rev. Immunol. 16, 421-432 (1998).
15. Shibuya, A. et al. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat. Immunol. 1, 441-446 (2000).
16. Sakamoto, N. et al. A novel Fc receptor for IgA and IgM is expressed on both hematopoietic and non-hematopoietic tissues. Eur. J. Immunol. 31, 1310-1316 (2001).
17. Shimizu, Y. et al. Fc(alpha)/mu receptor is a single gene-family member closely related to polymeric immunoglobulin receptor encoded on Chromosome 1. Immunogenetics 53, 709-711 (2001).
18. Kaetzel, C. S. The polymeric immunoglobulin receptor: bridging innate and adaptive immune responses at mucosal surfaces. Immunol. Rev. 206, 83-99 (2005).
19. Cho, Y. et al. Requirement of the cytoplasmic portion for dimer formation of Fcalpha/micro receptor expressed on cell surface. Mol. Immunol. 47, 878-882 (2010).
20. Takagaki, K., Satoh, K., Honda, S. & Shibuya, A. Molecular characterization of the dimer formation of Fcalpha/mu receptor (CD351). Mol. Immunol. 56, 23-27 (2013).
21. Honda, S. et al. Enhanced humoral immune responses against T-independent antigens in Fc alpha/muR-deficient mice. Proc. Natl Acad. Sci. USA 106, 11230-11235 (2009).
22. Reid, R. et al. Endotoxin shock in antibody-deficient mice: unraveling the role of natural antibody and complement in the clearance of lipopolysaccharide. J. Immunol. 159, 970-975 (1997).
23. Engel, P. et al. Abnormal B lymphocyte development, activation, and differentiation in mice that lack or overexpress the CD19 signal transduction molecule. Immunity 3, 39-50 (1995).
24. Cinamon, G., Zachariah, M., Lam, O., Foss, C. & Cyster, J. G. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9, 54-62 (2008).
25. Takagi, N. et al. Blockage of interleukin-6 receptor ameliorates joint disease in murine collagen-induced arthritis. Arthritis Rheum. 41, 2117-2121 (1998).
26. Xing, Z. et al. IL-6 is an antiinflammatory cytokine required for controlling local or systemic acute inflammatory responses. J. Clin. Invest. 101, 311-320 (1998).
27. Shibuya, A. & Honda, S. Molecular and functional characteristics of the Fcalpha/muR, a novel Fc receptor for IgM and IgA. Springer Semin. Immunopathol. 28, 377-382 (2006).
28. Hitomi, K. et al. An immunoglobulin-like receptor, Allergin-1, inhibits immunoglobulin E-mediated immediate hypersensitivity reactions. Nat. Immunol. 11, 601-607 (2010).
29. Nagai, K. et al. Expression and function of Allergin-1 on human primary mast cells. PLoS ONE 8, e76160 (2013).
30. Saitoh, S. et al. Lipid A antagonist, lipid IVa, is distinct from lipid A in interaction with Toll-like receptor 4 (TLR4)-MD-2 and ligand-induced TLR4 oligomerization. Int. Immunol. 16, 961-969 (2004).
31. Nagaoka, K. et al. Association of SIGNR1 with TLR4-MD-2 enhances signal transduction by recognition of LPS in gram-negative bacteria. Int. Immunol. 17, 827-836 (2005).
32. Dejager, L., Pinheiro, I., Dejonckheere, E. & Libert, C. Cecal ligation and puncture: the gold standard model for polymicrobial sepsis? Trends Microbiol. 19, 198-208 (2011).
33. Ehrenstein, M. & Notley, C. The importance of natural IgM: scavenger, protector and regulator. Nat. Rev. Immunol. 10, 778-786 (2010).
34. Kang, Y. et al. The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen. Proc. Natl Acad. Sci. USA 101, 215-220 (2004).
35. Geijtenbeek, T. B. et al. Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo. Blood 100, 2908-2916 (2002).
36. Kelly-Scumpia, K. et al. B cells enhance early innate immune responses during bacterial sepsis. J. Exp. Med. 208, 1673-1682 (2011).
37. Zouggari, Y. et al. B lymphocytes trigger monocyte mobilization and impair heart function after acute myocardial infarction. Nat. Med. 19, 1273-1280 (2013).
38. Rauch, P. et al. Innate response activator B cells protect against microbial sepsis. Science 335, 597-601 (2012).
39. Ping, S. et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 507, 366-370 (2014).
40. Yanaba, K. et al. A regulatory B cell subset with a unique CD1dhiCD5 + phenotype controls T cell-dependent inflammatory responses. Immunity 28, 639-650 (2008).
41. DiLillo, D. J., Matsushita, T. & Tedder, T. F. B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. NY Acad. Sci. 1183, 38-57 (2010).
42. Matsushita, T., Yanaba, K., Bouaziz, J., Fujimoto, M. & Tedder, T. Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118, 3420-3430 (2008).
43. Horikawa, M. et al. Regulatory B cell (B10 Cell) expansion during Listeria infection governs innate and cellular immune responses in mice. J. Immunol. 190, 1158-1168 (2013).
44. Lee, C. & Kung, J. Marginal Zone B Cell Is a Major Source of Il-10 in Listeria monocytogenes Susceptibility. J. Immunol. 189, 3319-3327 (2012).
45. Yoshizaki, A. et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491, 264-268 (2012).
46. Weller, S. et al. Human blood IgM 'memory' B cells are circulating splenic marginal zone B cells harboring a prediversified immunoglobulin repertoire. Blood 104, 3647-3654 (2004).
47. Zandvoort, A. et al. CD27 expression in the human splenic marginal zone: the infant marginal zone is populated by naive B cells. Tissue Antigens 58, 234-242 (2001).
48. Weill, J. C., Weller, S. & Reynaud, C. A. Human marginal zone B cells. Annu. Rev. Immunol. 27, 267-285 (2009).