Pivotal advance: Peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells

Journal of Leukocyte Biology

Volumn 91, Issue 4, 2012, Pages 525-536

  Parra, David ^a   Rieger, Aja M ^b   Li, Jun ^a   Zhang, Yong An ^a   Randall, Louise M ^a   Hunter, Christopher A ^a   Barreda, Daniel R ^b   Oriol Sunyer, J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Antigen Presentation; Evolution; Mouse; Particulate; Phagocytosis

Indexed keywords

LYMPHOCYTE ANTIGEN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; BACTERICIDAL ACTIVITY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; INTERNALIZATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PERITONEAL CAVITY; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, BACTERIAL; B-LYMPHOCYTE SUBSETS; BACTERIA; CD4-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; IMMUNITY, INNATE; MICE; PERITONEAL CAVITY; PHAGOCYTOSIS;

AMPHIBIA; MAMMALIA; REPTILIA;

EID: 84860879274     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0711372     Document Type: Article

References (47)

1. Desjardins, M., Houde, M., Gagnon, E. (2005) Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol. Rev. 207, 158-165.
2. Stuart, L. M., Ezekowitz, R. A. (2005) Phagocytosis: elegant complexity. Immunity 22, 539-550.
3. Watts, C, Amigorena, S. (2001) Phagocytosis and antigen presentation. Semin. Immunol. 13, 373-379.
4. Rabinovitch, M. (1995) Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 5, 85-87.
5. Ochando, J. C, Homma, C, Yang, Y., Hidalgo, A., Garin, A, Tacke, F., Angeli, V., Li, Y, Boros, P., Ding, Y, Jessberger, R., Trinchieri, G., Lira, S. A, Randolph, G. J., Bromberg, J. S. (2006) Alloantigen-presenting plas-macytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 7, 652-662.
6. Li, J., Barreda, D. R, Zhang, Y A, Boshra, H., Gelman, A. E., Lapatra, S., Tort, L., Sunyer, J. O. (2006) B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 7, 1116-1124.
7. Zhang, Y A, Salinas, I., Li, J., Parra, D., Bjork, S., Xu, Z., Lapatra, S. E., Bartholomew, J., Sunyer, J. O. (2010) IgT, a primitive immunoglobulin class specialized in mucosal immunity. Nat. Immunol. 11, 827-835.
8. Øverland, H. S., Pettersen, E. F., Ronneseth, A., Wergeland, H. I. (2010) Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 28, 193-204.
9. Zimmerman, L. M., Vogel, L. A, Edwards, K. A, Bowden, R M. (2010) Phagocytic B cells in a reptile. Biol. Lett. 6, 270-273.
10. Vidard, L., Kovacsovics-Bankowski, M., Kraeft, S. K, Chen, L. B., Benacer-raf, B., Rock, K L. (1996) Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J. Immunol. 156, 2809-2818.
11. Borrello, M. A, Phipps, R P. (1996) The B/macrophage cell: an elusive link between CD5+ B lymphocytes and macrophages. Immunol. Today 17, 471-475.
12. Katsura, Y (2002) Redefinition of lymphoid progenitors. Nat. Rev. Immunol. 2, 127-132.
13. Kawamoto, H. (2006) A close developmental relationship between the lymphoid and myeloid lineages. Trends Immunol. 27, 169-175.
14. Cumano, A, Paige, C. J., Iscove, N. N., Brady, G. (1992) Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 356, 612-615.
15. Montecino-Rodriguez, E., Leathers, H., Dorshkind, K. (2001) Bipotential B-macrophage progenitors are present in adult bone marrow. Nat. Immunol. 2, 83-88.
16. Rieger, A. M., Hall, B. E., Barreda, D. R (2010) Macrophage activation differentially modulates particle binding, phagocytosis and downstream antimicrobial mechanisms. Dev. Comp. Immunol. 34, 1144-1159.
17. Ramachandra, L., Song, R, Harding, C. V. (1999) Phagosomes are fully competent antigen-processing organelles that mediate the formation of peptide:class II MHC complexes. J. Immunol. 162, 3263-3272.
18. Barnden, M. J., Allison, J., Heath, W. R, Carbone, F. R (1998) Defective TCR expression in transgenic mice constructed using cDNA-based α- and β-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76, 34-40.
19. Ghosn, E. E., Cassado, A. A, Govoni, G. R, Fukuhara, T., Yang, Y, Mo-nack, D. M., Bortoluci, K. R, Almeida, S. R, Herzenberg, L. A, Herzen-berg, L. A. (2010) Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. USA 107, 2568-2573.
20. Abrahaõ, T. B., Freymuller, E., Mortara, R. A., Lopes, J. D., Mariano, M. (2003) Morphological characterization of mouse B-1 cells. Immunobiology 208, 401-411.
21. Batista, F. D., Neuberger, M. S. (2000) B cells extract and present immobilized antigen: implications for affinity discrimination. EMBO J. 19, 513-520.
22. Chesnut, R. W., Colon, S. M., Grey, H. M. (1982) Antigen presentation by normal B cells, B cell tumors, and macrophages: functional and biochemical comparison. J. Immunol. 128, 1764-1768.
23. Mohan, C., Morel, L., Yang, P., Wakeland, E. K. (1998) Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum. 41, 1652-1662.
24. Utsinger, P. D., Yount, W. J., Fuller, C. R., Logue, M. J., Orringer, E. P. (1977) Hairy cell leukemia: B-lymphocyte and phagocytic properties. Blood 49, 19-27.
25. Souwer, Y., Griekspoor, A., Jorritsma, T., de Wit, J., Janssen, H., Neefjes, J., van Ham, S. M. (2009) B cell receptor-mediated internalization of salmonella: a novel pathway for autonomous B cell activation and antibody production. J. Immunol. 182, 7473-7481.
26. Almeida, S. R., Aroeira, L. S., Frymuller, E., Dias, M. A., Bogsan, C. S., Lopes, J. D., Mariano, M. (2001) Mouse B-1 cell-derived mononuclear phagocyte, a novel cellular component of acute non-specific inflammatory exudate. Int. Immunol. 13, 1193-1201.
27. Baumgarth, N., Tung, J. W., Herzenberg, L. A. (2005) Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26, 347-362.
28. Fagarasan, S., Honjo, T. (2000) T-Independent immune response: new aspects of B cell biology. Science 290, 89-92.
29. Yoshimoto, M., Montecino-Rodriguez, E., Ferkowicz, M. J., Porayette, P., Shelley, W. C., Conway, S. J., Dorshkind, K., Yoder, M. C. (2011) Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc. Natl. Acad. Sci. USA 108, 1468-1473.
30. Delamarre, L., Pack, M., Chang, H., Mellman, I., Trombetta, E. S. (2005) Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307, 1630-1634.
31. Chen, X., Peter, J. (2008) The role of B lymphocytes as antigen-presenting cells. Arch. Immunol. Ther. Exp. (Warsz.) 56, 77-83.
32. Lanzavecchia, A. (1985) Antigen-specific interaction between T and B cells. Nature 314, 537-539.
33. Zhong, X., Gao, W., Degauque, N., Bai, C., Lu, Y., Kenny, J., Oukka, M., Strom, T. B., Rothstein, T. L. (2007) Reciprocal generation of Th1/Th17 and T(reg) cells by B1 and B2 B cells. Eur. J. Immunol. 37, 2400-2404.
34. Viau, M., Zouali, M. (2005) B-lymphocytes, innate immunity, and autoim-munity. Clin. Immunol. 114, 17-26.
35. Tsark, E. C., Wang, W., Teng, Y. C., Arkfeld, D., Dodge, G. R., Kovats, S. (2002) Differential MHC class II-mediated presentation of rheumatoid arthritis autoantigens by human dendritic cells and macrophages. J. Immunol. 169, 6625-6633.
36. Vasilevsky, S., Colino, J., Puliaev, R., Canaday, D. H., Snapper, C. M. (2008) Macrophages pulsed with Streptococcus pneumoniae elicit a T cell-dependent antibody response upon transfer into naive mice. J. Immunol. 181, 1787-1797.
37. Tel, J., Lambeck, A. J., Cruz, L. J., Tacken, P. J., de Vries, I. J., Figdor, C. G. (2010) Human plasmacytoid dendritic cells phagocytose, process, and present exogenous particulate antigen. J. Immunol. 184, 4276-4283.
38. Schlosser, E., Mueller, M., Fischer, S., Basta, S., Busch, D. H., Gander, B., Groettrup, M. (2008) TLR ligands and antigen need to be coencapsu-lated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses. Vaccine 26, 1626-1637.
39. Johansen, P., Estevez, F., Zurbriggen, R., Merkle, H. P., Gluck, R., Corra-din, G., Gander, B. (2000) Towards clinical testing of a single-administration tetanus vaccine based on PLA/PLGA microspheres. Vaccine 19, 1047-1054.
40. Waeckerle-Men, Y., Allmen, E. U., Gander, B., Scandella, E., Schlosser, E., Schmidtke, G., Merkle, H. P., Groettrup, M. (2006) Encapsulation of proteins and peptides into biodegradable poly(D,L-lactide-co-glycolide) microspheres prolongs and enhances antigen presentation by human dendritic cells. Vaccine 24, 1847-1857.
41. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-252.
42. Savina, A., Amigorena, S. (2007) Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219, 143-156.
43. Vidard, L., Rock, K. L., Benacerraf, B. (1992) Heterogeneity in antigen processing by different types of antigen-presenting cells. Effect of cell culture on antigen processing ability. J. Immunol. 149, 1905-1911.
44. Suzuki, K., Maruya, M., Kawamoto, S., Fagarasan, S. (2010) Roles of B-1 and B-2 cells in innate and acquired IgA-mediated immunity. Immunol. Rev. 237, 180-190.
45. Cerutti, A., Rescigno, M. (2008) The biology of intestinal immunoglobu-lin A responses. Immunity 28, 740-750.
46. Plytycz, B., Seljelid, R. (1999) Dual origin of lymphocytes? Immunol. Today 20, 53-54.
47. Herzenberg, L. A., Kantor, A. B. (1992) Layered evolution in the immune system. A model for the ontogeny and development of multiple lymphocyte lineages. Ann. N. Y. Acad. Sci. 651, 1-9.