A population of CD19highCD45R-/lowCD21low B lymphocytes poised for spontaneous secretion of IgG and IgA antibodies

Journal of Immunology

Volumn 179, Issue 8, 2007, Pages 5326-5334

  De Andrés, Belén ^a   Cortegano, Isabel ^b   Serrano, Natalia ^a   Del Rio, Borja ^a   Martín, Paloma ^c   Gonzalo, Pilar ^a   Marcos, Miguel A R ^b   Gaspar, María Luisa ^a  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b CSIC   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD45RA ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; IMMUNOGLOBULIN; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; CD45 ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL REGENERATION; CLINICAL FEATURE; CONTROLLED STUDY; EMBRYO; GENE FREQUENCY; GENETIC TRAIT; GESTATIONAL AGE; HEMATOPOIETIC STEM CELL; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INOCULATION; MOUSE; MULTIPOTENT STEM CELL; NEWBORN; NONHUMAN; ONTOGENY; OVARY FOLLICLE CELL; PERINATAL PERIOD; PHENOTYPE; PLASMA CELL; PRIORITY JOURNAL; SECRETORY CELL; SPLEEN; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; CBA MOUSE; CELL AGING; CELL CULTURE; CELL MOTION; CYTOLOGY; FETUS; IMMUNOLOGY; LIVER; METABOLISM; MOUSE MUTANT; PRENATAL DEVELOPMENT; SECRETION;

ANIMALS; ANTIGENS, CD19; ANTIGENS, CD45; B-LYMPHOCYTE SUBSETS; BONE MARROW CELLS; CELL AGING; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; FETUS; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LIVER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, KNOCKOUT; MULTIPOTENT STEM CELLS; PLASMA CELLS; RECEPTORS, COMPLEMENT 3D; SPLEEN;

EID: 38449116801     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.8.5326     Document Type: Article

References (59)

1. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature 381: 751-758.
2. Martin, F., and J. F. Kearney. 2001. B1 cells: similarities and differences with other B cell subsets. Curr. Opin. Immunol. 13: 195-201.
3. Lopes-Carvalho, T., J. Foote, and J. F. Kearney. 2005. Marginal zone B cells in lymphocyte activation and regulation. Curr. Opin. Immunol. 17: 244-250.
4. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18.
5. Hayakawa, K., M. Asano, S. A. Shinton, M. Gui, L. J. Wen, J. Dashoff, and R. R. Hardy. 2003. Positive selection of anti-thy-1 autoreactive B-1 cells and natural serum autoantibody production independent from bone marrow B cell development. J. Exp. Med. 197: 87-99.
6. Medzhitov, R., and C. Janeway, Jr. 2000. Innate immunity. N. Engl. J. Med. 343: 338-344.
7. Bendelac, A., M. Bonneville, and J. F. Kearney. 2001. Autoreactivity by design: innate B and T lymphocytes. Nat. Rev. Immunol. 1: 177-186.
8. Marcos, M. A., S. Morales-Alcelay, I. E. Godin, F. Dieterlen-Lievre, S. G. Copin, and M. L. Gaspar. 1997. Antigenic phenotype and gene expression pattern of lymphohemopoietic progenitors during early mouse ontogeny. J. Immunol. 158: 2627-2637.
9. Carlyle, J. R., and J. C. Zuñiga-Pflucker. 1998. Lineage commitment and differentiation of T and natural killer lymphocytes in the fetal mouse. Immunol. Rev. 165: 63-74.
10. Ikawa, T., K. Masuda, M. Lu, N. Minato, Y. Katsura, and H. Kawamoto. 2004. Identification of the earliest prethymic T-cell progenitors in murine fetal blood. Blood 103: 530-537.
11. de Andres, B., P. Gonzalo, S. Minguet, J. A. Martinez-Marin, P. G. Soro, M. A. Marcos, and M. L. Gaspar. 2002. The first 3 days of B-cell development in the mouse embryo. Blood 100: 4074-4081.
12. Montecino-Rodriguez, E., H. Leathers, and K. Dorshkind. 2006. Identification of a B-1 B cell-specified progenitor. Nat. Immunol. 7: 293-301.
13. Okabe, M., M. Ikawa, K. Kominami, T. Nakanishi, and Y. Nishimune. 1997. "Green mice" as a source of ubiquitous green cells. FEBS Lett. 407: 313-319.
14. Weijer, K., C. H. Uittenbogaart, A. Voordouw, F. Couwenberg, J. Seppen, B. Blom, F. A. Vyth-Dreese, and H. Spits. 2002. Intrathymic and extrathymic development of human plasmacytoid dendritic cell precursors in vivo. Blood 99: 2752-6759.
15. 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.
16. low(CD45/TER119)-hepatic cell progenitors of 11-day postcoitus mouse embryo liver reconstitutes cell-depleted liver organoids. J. Clin. Invest. 112: 1152-1163.
17. Martinez, M. J., S. Minguet, P. Gonzalo, P. G. Soro, B. de Andres, A. Izcue, M. A. Marcos, and M. L. Gaspar. 2001. Long-lived polyclonal B-cell lines derived from midgestation mouse embryo lymphohematopoietic progenitors reconstitute adult immunodeficient mice. Blood 98: 1862-1871.
18. Soro, P. G., A. P. Morales, M. J. Martinez, A. S. Morales, S. G. Copin, M. A. Marcos, and M. L. Gaspar. 1999. Differential involvement of the transcription factor Blimp-1 in T cell-independent and -dependent B cell differentiation to plasma cells. J. Immunol. 163: 611-617.
19. ten Boekel, E., F. Melchers, and A. Rolink. 1995. The status of Ig loci rearrangements in single cells from different stages of B cell development. Int. Immunol. 7: 1013-1019.
20. Velardi, A., and M. D. Cooper. 1984. An immunofluorescence analysis of the ontogeny of myeloid, T, and B lineage cells in mouse hemopoietic tissues. J. Immunol. 133: 672-677.
21. Montecino-Rodriguez, E., H. Leathers, and K. Dorshkind. 2001. Bipotential B-macrophage progenitors are present in adult bone marrow. Nat. Immunol. 2: 83-88.
22. Tung, J. W., M. D. Mrazek, Y. Yang, L. A. Herzenberg, and L. A. Herzenberg. 2006. Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc. Natl. Acad. Sci. USA 103: 6293-6298.
23. Lam, K. P., and A. M. Stall. 1994. Major histocompatibility complex class II expression distinguishes two distinct B cell developmental pathways during ontogeny. J. Exp. Med. 180: 507-516.
24. Hathcock, K. S., H. Hirano, S. Murakami, and R. J. Hodes. 1993. CD44 expression on activated B cells: differential capacity for CD44-dependent binding to hyaluronic acid. J. Immunol. 151: 6712-6722.
25. - memory B cell compartment. J. Exp. Med. 191: 1149-1166.
26. Kosco-Vilbois, M. H., J. Y. Bonnefoy, and Y. Chvatchko. 1997. The physiology of murine germinal center reactions. Immunol. Rev. 156: 127-136.
27. Marcos, M. A., F. Huetz, P. Pereira, J. L. Andreu, C. Martinez-A, and A. Coutinho. 1989. Further evidence for coelomic-associated B lymphocytes Eur. J. Immunol. 19: 2031-2035.
28. Kramer, D. R., and J. J. Cebra. 1995. Early appearance of "natural" mucosal IgA responses and germinal centers in suckling mice developing in the absence of maternal antibodies. J. Immunol. 154: 2051-2062.
29. Rawlings, D. J., D. C. Saffran, S. Tsukada, D. A. Largaespada, J. C. Grimaldi, L. Cohen, R. N. Mohr, J. F. Bazan, M. Howard, N. G. Copeland, et al. 1993. Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 261: 358-361.
30. Shapiro-Shelef, M., K. I. Lin, D. Savitsky, J. Liao, and K. Calame. 2005. Blimp-1 is required for maintenance of long-lived plasma cells in the bone marrow. J. Exp. Med. 202: 1471-1476.
31. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190: 75-89.
32. Rickert, R. C. 2005. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr. Opin. Immunol. 17: 237-243.
33. Fischer, M. B., S. Goerg, L. Shen, A. P. Prodeus, C. C. Goodnow, G. Kelsoe, and M. C. Carroll. 1998. Dependence of germinal center B cells on expression of CD21/CD35 for survival. Science 280: 582-585.
34. Barrington, R. A., M. Zhang, X. Zhong, H. Jonsson, N. Holodick, A. Cherukuri, S. K. Pierce, T. L. Rothstein, and M. C. Carroll. 2005. CD21/CD19 coreceptor signaling promotes B cell survival during primary immune responses. J. Immunol. 175: 2859-2867.
35. -/- mice: enhanced affinity maturation but impaired antibody persistence. J. Immunol. 164: 4522-4532.
36. Gatto, D., T. Pfister, A. Jegerlehner, S. W. Martin, M. Kopf, and M. F. Bachmann. 2005. Complement receptors regulate differentiation of bone marrow plasma cell precursors expressing transcription factors Blimp-1 and XBP-1. J. Exp. Med. 201: 993-1005.
37. Paus, D., T. G. Phan, T. D. Chan, S. Gardam, A. Basten, and R. Brink. 2006. Antigen recognition strength regulates the choice between extrafollicular plasma cell and germinal center B cell differentiation. J. Exp. Med. 203: 1081-1091.
38. 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.
39. Gatto, D., C. Ruedl, B. Odermatt, and M. F. Bachmann. 2004. Rapid response of marginal zone B cells to viral particles. J. Immunol. 173: 4308-4316.
40. Kaminski, D. A., and J. Stavnezer. 2006. Enhanced IgA class switching in marginal zone and B1 B cells relative to follicular/B2 B cells. J. Immunol. 177: 6025-6029.
41. Pape, K. A., V. Kouskoff, D. Nemazee, H. L. Tang, J. G. Cyster, L. E. Tze, K. L. Hippen, T. W. Behrens, and M. K. Jenkins. 2003. Visualization of the genesis and fate of isotype-switched B cells during a primary immune response. J. Exp. Med. 197: 1677-1687.
42. de Waard, R., P. M. Dammers, J. W. Tung, A. B. Kantor, J. A. Wilshire, N. A. Bos, L. A. Herzenberg, and F. G. Kroese. 1998. Presence of germline and full-length IgA RNA transcripts among peritoneal B-1 cells. Dev. Immunol. 6: 81-87.
43. Macpherson, A. J., A. Lamarre, K. McCoy, G. R. Harriman, B. Odermatt, G. Dougan, H. Hengartner, and R. M. Zinkernagel. 2001. IgA production without μ or δ chain expression in developing B cells. Nat. Immunol. 2: 625-631.
44. Seagal, J., E. Edry, Z. Keren, N. Leider, O. Benny, M. Machluf, and D. Melamed. 2003. A fail-safe mechanism for negative selection of isotype-switched B cell precursors is regulated by the Fas/FasL pathway. J. Exp. Med. 198: 1609-1619.
45. Underhill, G. H., H. A. Minges Wols, J. L. Fornek, P. L. Witte, and G. S. Kansas. 2002. IgG plasma cells display a unique spectrum of leukocyte adhesion and homing molecules. Blood 99: 2905-2912.
46. Zemlin, M., G. Hoersch, C. Zemlin, A. Pohl-Schickinger, M. Hummel, C. Berek, R. F. Maier, and K. Bauer. 2007. The postnatal maturation of the immunoglobulin heavy chain IgG repertoire in human preterm neonates is slower than in term neonates. J. Immunol. 178: 1180-1188.
47. Bachmann, M. F., R. M. Zinkernagel, and A. Oxenius. 1998. Immune responses in the absence of costimulation: viruses know the trick. J. Immunol. 161: 5791-5794.
48. Hardy, R. R. 2006. B-1 B cell development. J. Immunol. 177: 2749-2754.
49. Avrameas, S. 1991. Natural autoantibodies: from "horror autotoxicus" to "gnothi seauton". Immunol. Today 12: 154-159.
50. Fornek, J. L., L. T. Tygrett, T. J. Waldschmidt, V. Poli, R. C. Rickert, and G. S. Kansas. 2006. Critical role for Stat3 in T-dependent terminal differentiation of IgG B cells. Blood 107: 1085-1091.
51. Kallies, A., J. Hasbold, D. M. Tarlinton, W. Dietrich, L. M. Corcoran, P. D. Hodgkin, and S. L. Nutt. 2004. Plasma cell ontogeny defined by quantitative changes in Blimp-1 expression. J. Exp. Med. 200: 967-977.
52. Shapiro-Shelef, M., K. I. Lin, L. J. McHeyzer-Williams, J. Liao, M. G. McHeyzer-Williams, and K. Calame. 2003. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19: 607-620.
53. Bell, J., and D. Gray. 2003. Antigen-capturing cells can masquerade as memory B cells. J. Exp. Med. 197: 1233-1244.
54. - cells after primary NP challenge in mice. J. Immunol. 177: 2072-2079.
55. Phan, T. G., M. Amesbury, S. Gardam, J. Crosbie, J. Hasbold, P. D. Hodgkin, A. Basten, and R. Brink. 2003. B cell receptor-independent stimuli trigger immunoglobulin (Ig) class switch recombination and production of IgG autoantibodies by anergic self-reactive B cells. J. Exp. Med. 197: 845-860.
56. - B lymphocyte subset producing natural antibodies. J. Immunol. 148: 2690-2702.
57. Gokmen, E., F. M. Raaphorst, D. H. Boldt, and J. M. Teale. 1998. Ig heavy chain third complementarity determining regions (H CDR3s) after stem cell transplantation do not resemble the developing human fetal H CDR3s in size distribution and Ig gene utilization. Blood 92: 2802-2814.
58. Storek, J., R. P. Witherspoon, D. G. Maloney, T. R. Chauncey, and R. Storb. 1997. Improved reconstitution of CD4 T cells and B cells but worsened reconstitution of serum IgG levels after allogeneic transplantation of blood stem cells instead of marrow. Blood 89: 3891-3893.
59. Storek, J., A. Joseph, G. Espino, M. A. Dawson, D. C. Douek, K. M. Sullivan, M. E. Flowers, P. Martin, G. Mathioudakis, R. A. Nash, et al. 2002. Immunity of patients surviving 20 to 30 years after allogeneic or syngeneic bone marrow transplantation. Blood 98: 3505-3512.