Marginal zone B cells regulate antigen capture by marginal zone macrophages

Journal of Immunology

Volumn 186, Issue 4, 2011, Pages 2172-2181

  You, Yuying ^a,c   Myers, Riley C ^a   Freeberg, Larry ^a   Foote, Jeremy ^a,d   Kearney, John F ^a   Justement, Louis B ^a   Carter, Robert H ^b  

^a University of Alabama at Birmingham   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d AUBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C TYPE LECTIN SPECIFIC INTRACELLULAR ADHESION MOLECULE GRABBING NONINTEGRIN RECEPTOR 1; CD19 ANTIGEN; CELL ADHESION MOLECULE; FINGOLIMOD; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; FLOW CYTOMETRY; IMMUNOFLUORESCENCE TEST; MACROPHAGE; MARGINAL ZONE B CELL; MARGINAL ZONE MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; ANTIGENS; ANTIGENS, CD19; B-LYMPHOCYTE SUBSETS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL MOVEMENT; LECTINS, C-TYPE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RECEPTORS, CELL SURFACE; SPLEEN;

EID: 79951838640     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002106     Document Type: Article

References (33)

1. Mebius, R. E., and G. Kraal. 2005. Structure and function of the spleen. Nat. Rev. Immunol. 5: 606-616.
2. Kang, Y. S., J. Y. Kim, S. A. Bruening, M. Pack, A. Charalambous, A. Pritsker, T. M. Moran, J. M. Loeffler, R. M. Steinman, and C. G. Park. 2004. 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.
3. Taylor, P. R., L. Martinez-Pomares, M. Stacey, H. H. Lin, G. D. Brown, and S. Gordon. 2005. Macrophage receptors and immune recognition. Annu. Rev. Immunol. 23: 901-944.
4. Elomaa, O., M. Kangas, C. Sahlberg, J. Tuukkanen, R. Sormunen, A. Liakka, I. Thesleff, G. Kraal, and K. Tryggvason. 1995. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80: 603-609.
5. Ito, S., M. Naito, Y. Kobayashi, H. Takatsuka, S. Jiang, H. Usuda, H. Umezu, G. Hasegawa, M. Arakawa, L. D. Shultz, et al. 1999. Roles of a macrophage receptor with collagenous structure (MARCO) in host defense and heterogeneity of splenic marginal zone macrophages. Arch. Histol. Cytol. 62: 83-95.
6. Lanoue, A., M. R. Clatworthy, P. Smith, S. Green, M. J. Townsend, H. E. Jolin, K. G. Smith, P. G. Fallon, and A. N. McKenzie. 2004. SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J. Exp. Med. 200: 1383-1393.
7. Kang, Y. S., Y. Do, H. K. Lee, S. H. Park, C. Cheong, R. M. Lynch, J. M. Loeffler, R. M. Steinman, and C. G. Park. 2006. A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125: 47-58.
8. Pillai, S., A. Cariappa, and S. T. Moran. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23: 161-196.
9. Guinamard, R., M. Okigaki, J. Schlessinger, and J. V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1: 31-36.
10. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629.
11. Ferguson, A. R., M. E. Youd, and R. B. Corley. 2004. Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells. Int. Immunol. 16: 1411-1422.
12. Cinamon, G., M. A. Zachariah, O. M. Lam, F. W. Foss, Jr., and J. G. Cyster. 2008. Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 9: 54-62.
13. You, Y., H. Zhao, Y. Wang, and R. H. Carter. 2009. Cutting edge: Primary and secondary effects of CD19 deficiency on cells of the marginal zone. J. Immunol. 182: 7343-7347.
14. Crowley, M. T., C. R. Reilly, and D. Lo. 1999. Influence of lymphocytes on the presence and organization of dendritic cell subsets in the spleen. J. Immunol. 163: 4894-4900. (Pubitemid 29501254)
15. Karlsson, M. C., R. Guinamard, S. Bolland, M. Sankala, R. M. Steinman, and J. V. Ravetch. 2003. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 198: 333-340.
16. Nolte, M. A., R. Arens, M. Kraus, M. H. van Oers, G. Kraal, R. A. van Lier, and R. E. Mebius. 2004. B cells are crucial for both development and maintenance of the splenic marginal zone. J. Immunol. 172: 3620-3627.
17. McCright, B., X. Gao, L. Shen, J. Lozier, Y. Lan, M. Maguire, D. Herzlinger, G. Weinmaster, R. Jiang, and T. Gridley. 2001. Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128: 491-502. (Pubitemid 32229592)
18. Allende, M. L., T. Yamashita, and R. L. Proia. 2003. G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102: 3665-3667.
19. Saito, T., S. Chiba, M. Ichikawa, A. Kunisato, T. Asai, K. Shimizu, T. Yamaguchi, G. Yamamoto, S. Seo, K. Kumano, et al. 2003. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685. (Pubitemid 36588584)
20. Cinamon, G., M. Matloubian, M. J. Lesneski, Y. Xu, C. Low, T. Lu, R. L. Proia, and J. G. Cyster. 2004. Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 5: 713-720.
21. Geijtenbeek, T. B., P. C. Groot, M. A. Nolte, S. J. van Vliet, S. T. Gangaram-Panday, G. C. van Duijnhoven, G. Kraal, A. J. van Oosterhout, and Y. van Kooyk. 2002. Marginal zone macrophages express a murine homologue of DCSIGN that captures blood-borne antigens in vivo. Blood 100: 2908-2916.
22. Koppel, E. A., M. Litjens, V. C. van den Berg, Y. van Kooyk, and T. B. Geijtenbeek. 2008. Interaction of SIGNR1 expressed by marginal zone macrophages with marginal zone B cells is essential to early IgM responses against Streptococcus pneumoniae. Mol. Immunol. 45: 2881-2887.
23. Moens, L., A. Jeurissen, G. Wuyts, P. G. Fallon, B. Louis, J. L. Ceuppens, and X. Bossuyt. 2007. Specific intracellular adhesion molecule-grabbing nonintegrin R1 is not involved in the murine antibody response to pneumococcal polysaccharides. Infect. Immun. 75: 5748-5752.
24. Chen, Y., T. Pikkarainen, O. Elomaa, R. Soininen, T. Kodama, G. Kraal, and K. Tryggvason. 2005. Defective microarchitecture of the spleen marginal zone and impaired response to a thymus-independent type 2 antigen in mice lacking scavenger receptors MARCO and SR-A. J. Immunol. 175: 8173-8180. (Pubitemid 41798381)
25. Claassen, E., N. Kors, and N. Van Rooijen. 1986. Influence of carriers on the development and localization of anti-2,4,6-trinitrophenyl (TNP) antibody-forming cells in the murine spleen. II. Suppressed antibody response to TNP-Ficoll after elimination of marginal zone cells. Eur. J. Immunol. 16: 492-497.
26. Kraal, G., H. Ter Hart, C. Meelhuizen, G. Venneker, and E. Claassen. 1989. Marginal zone macrophages and their role in the immune response against T-independent type 2 antigens: modulation of the cells with specific antibody. Eur. J. Immunol. 19: 675-680.
27. Anthony, R. M., F. Wermeling, M. C. Karlsson, and J. V. Ravetch. 2008. Identification of a receptor required for the anti-inflammatory activity of IVIG. Proc. Natl. Acad. Sci. USA 105: 19571-19578.
28. Balázs, M., F. Martin, T. Zhou, and J. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17: 341-352. (Pubitemid 35279554)
29. Rickert, R. C., K. Rajewsky, and J. Roes. 1995. Impairment of T-cell-dependent B-cell responses and B-1 cell development in CD19-deficient mice. Nature 376: 352-355.
30. van Vliet, E., M. Melis, and W. van Ewijk. 1985. Marginal zone macrophages in the mouse spleen identified by a monoclonal antibody. Anatomical correlation with a B cell subpopulation. J. Histochem. Cytochem. 33: 40-44.
31. Dijkstra, C. D., E. Van Vliet, E. A. Döpp, A. A. van der Lelij, and G. Kraal. 1985. Marginal zone macrophages identified by a monoclonal antibody: characterization of immuno- and enzyme-histochemical properties and functional capacities. Immunology 55: 23-30. (Pubitemid 15114582)
32. van der Laan, L. J., E. A. Döpp, R. Haworth, T. Pikkarainen, M. Kangas, O. Elomaa, C. D. Dijkstra, S. Gordon, K. Tryggvason, and G. Kraal. 1999. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J. Immunol. 162: 939-947. (Pubitemid 29035419)
33. Xue, L., S. W. Morris, C. Orihuela, E. Tuomanen, X. Cui, R. Wen, and D. Wang. 2003. Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells. Nat. Immunol. 4: 857-865.