Development and function of B-1 cells

Current Opinion in Immunology

Volumn 12, Issue 3, 2000, Pages 346-354

  Hayakawa, Kyoko ^a   Hardy, Richard R ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD5 ANTIGEN;

B LYMPHOCYTE; LYMPHOCYTE FUNCTION; MOUSE; MOUSE MUTANT; NONHUMAN; NOTE; TRANSGENIC MOUSE;

EID: 0034053443     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0952-7915(00)00098-4     Document Type: Review

References (59)

1. Hardy R.R., Hayakawa K. CD5 B cells, a fetal B cell lineage. Adv Immunol. 55:1994;297-339.
2. Hayakawa K., Hardy R.R. B-1 cell definition. Curr Top Micobiol Immunol. 2000;. in press.
3. + B cell lymphomas. J Immunol. 141:1988;2788-2796.
4. Li Y-S., Hayakawa K., Hardy R.R. The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver. J Exp Med. 178:1993;951-960.
5. Wasserman R., Li Y.S., Shinton S.A., Carmack C.E., Manser T., Wiest D.L., Hayakawa K., Hardy R.R. A novel mechanism for B cell repertoire maturation based on response by B cell precursors to pre-B receptor assembly. J Exp Med. 187:1998;259-264. Study of the effect of pre-BCR assembly in vitro and in vivo by analysis either of pro-B cell lines transfected with μ heavy chain or of transgenic mice. Provides the first evidence that the ability of μ heavy chain to assemble with surrogate light chain has different effects on subsequent clonal expansion in fetal liver and adult bone marrow.
6. Kline G.H., Hartwell L., Beck-Engeser G.B., Keyna U., Zaharevitz S., Klinman N.R., Jack H.M. Pre-B cell receptor-mediated selection of pre-B cells synthesizing functional mu heavy chains. J Immunol. 161:1998;1608-1618.
7. ten Boekel E., Melchers F., Rolink A.G. Changes in the V(H) gene repertoire of developing precursor B lymphocytes in mouse bone marrow mediated by the pre-B cell receptor. Immunity. 7:1997;357-368.
8. + B cells regardless of PtC binding activity but shows differences in Jκ usage (there is a Jκ4/Jκ5 bias in non-PtC-binding antibodies). The authors regard this as demonstrating that antigen-independent VH12/Vκ4 biased association occurs, together with antigen-dependent differentiation into B-1 cells by use of appropriate Jκ chains (we suggest a different interpretation of this Jκ usage bias, see text). Also shows anti-PtC B cells in the primary follicles in the spleen, indicating that B-1 cells are not inherently marginal zone cells.
9. + B cells in such mice though only in VH12μ 'single-positive' cells. The authors explain this as being due to a difference in IgM surface density although, potentially, variable expression of light chains or variable B cell origin may complicate this interpretation.
10. Gui M., Wiest D.L., Li J., Kappes D., Hardy R.R., Hayakawa K. Peripheral CD4+ T cell maturation recognized by increased expression of Thy-1/CD90 bearing the 6C10 carbohydrate epitope. J Immunol. 163:1999;4796-4804.
11. + B cell generation and serum natural autoantibody; an antithymocyte autoantibody Tgμ mouse system was used. Together with [10], this also demonstrates that a carbohydrate epitope on the Thy-1 glycoprotein is the physiologic antigen recognized by this natural autoantibody.
12. + B cells).
13. Litzenburger T., Fassler R., Bauer J., Lassmann H., Linington C., Wekerle H., Iglesias A. B lymphocytes producing demyelinating autoantibodies: development and function in gene-targeted transgenic mice. J Exp Med. 188:1998;169-180. Shows a significant role for autoantibody to myelin/oligodendrocyte-glycoprotein in the pathogenesis of EAE (experimental allergic encephalomyelitis). Demonstrates generation of functional autoreactive B cells (B-2) when autoantigen is segregated to distinctive sites; however such cells are apparently not B-1a. Curiously their data suggest that this specificity seems to be predominantly encoded in the H-chain, with less contribution by the L-chain.
14. Qin X.F., Schwers S., Yu W., Papavasiliou F., Suh H., Nussenzweig A., Rajewsky K., Nussenzweig M.C. Secondary V(D)J recombination in B-1 cells. Nature. 397:1999;355-359. The authors show that B-1 cells, like germinal-center B cells, can express Rag-1 and Rag-2 and undergo secondary V(D)J recombination of their immunoglobulin genes. Furthermore, B cells from autoimmune-prone NZB mice show particularly high levels of Rag messenger RNA and recombination, suggesting an association with the development of autoreactive antibodies.
15. Carroll M.C. The role of complement and complement receptors in induction and regulation of immunity. Annu Rev Immunol. 16:1998;545-568. Characterization of knockout mice deficient in complement components C3 or C4, or the complement receptors CD21 and CD35, indicate that complement can regulate both B-1 and B-2 cells. Importantly, it appears that natural antibody (probably produced by B-1 cells) provides a major recognition role in activation of the complement system, which in turn enhances activation of antigen-specific (B-2) B cells.
16. Suzuki H., Terauchi Y., Fujiwara M., Aizawa S., Yazaki Y., Kadowaki T., Koyasu S. Xid-like immunodeficiency in mice with disruption of the p85 alpha subunit of phosphoinositide 3-kinase. Science. 283:1999;390-392.
17. Fruman D.A., Snapper S.B., Yballe C.M., Davidson L., Yu J.Y., Alt F.W., Cantley L.C. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85 alpha. Science. 283:1999;393-397.
18. O'Rourke L.M., Tooze R., Turner M., Sandoval D.M., Carter R.H., Tybulewicz V.L., Fearon D.T. CD19 as a membrane-anchored adaptor protein of B lymphocytes: costimulation of lipid and protein kinases by recruitment of Vav. Immunity. 8:1998;635-645. The authors show the role of Vav in the action of CD19 as a BCR adaptor/accessory molecule that functions in antigen-dependent BCR signaling. Specifically they show that vav association mediates activation of lipid and protein kinases important in B cell activation.
19. Sen G., Bikah G., Venkataraman C., Bondada S. Negative regulation of antigen receptor-mediated signaling by constitutive asociation of CD5 with the SHP-1 protein tyrosine phosphatase in B-1 B cells. Eur J Immunol. 29:1999;3319-3328.
20. Perez-Villar J.J., Whitney G.S., Bowen M.A., Hewgill D.H., Aruffo A.A., Kanner S.B. CD5 negatively regulates the T-cell antigen receptor signal transduction pathway: involvement of SH2-containing phosphotyrosine phosphatase SHP-1. Mol Cell Biol. 19:1999;2903-2912. The authors show that CD5 is constitutively associated with phosphotyrosine phosphatase activity in Jurkat T cells, and specifically with the Src homology 2 (SH2)-domain-containing hematopoietic phosphotyrosine phosphatase SHP-1 in both Jurkat cells and normal phytohemagglutinin-expanded T lymphoblasts, suggesting one way that CD5 can modulate antigen receptor signaling.
21. Nishimura H., Minato N., Nakano T., Honjo T. Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int Immunol. 10:1998;1563-1572.
22. Takeshita H., Taniuchi I., Kato J., Watanabe T. Abrogation of autoimmune disease in Lyn-deficient mice by the mutation of the Btk gene. Int Immunol. 10:1998;435-444.
23. Calvo J., Padilla O., Places L., Vigorito E., Vila J.M., Vilella R., Mila J., Vives J., Bowen M.A., Lozano F. Relevance of individual CD5 extracellular domains on antibody recognition, glycosylation and co-mitogenic signalling. Tissue Antigens. 54:1999;16-26.
24. McAlister M.S., Brown M.H., Willis A.C., Rudd P.M., Harvey D.J., Aplin R., Shotton D.M., Dwek R.A., Barclay A.N., Driscoll P.C. Structural analysis of the CD5 antigen - expression, disulphide bond analysis and physical characterisation of CD5 scavenger receptor superfamily domain 1. Eur J Biochem. 257:1998;131-141.
25. Rudd P.M., Wormald M.R., Harvey D.J., Devasahayam M., McAlister M.S., Brown M.H., Davis S.J., Barclay A.N., Dwek R.A. Oligosaccharide analysis and molecular modeling of soluble forms of glycoproteins belonging to the Ly-6, scavenger receptor, and immunoglobulin superfamilies expressed in Chinese hamster ovary cells. Glycobiology. 9:1999;443-458.
26. Bikah G., Lynd F.M., Aruffo A.A., Ledbetter J.A., Bondada S. A role for CD5 in cognate interactions between T cells and B cells, and identification of a novel ligand for CD5. Int Immunol. 10:1998;1185-1196.
27. Calvo J., Places L., Padilla O., Vila J.M., Vives J., Bowen M.A., Lozano F. Interaction of recombinant and natural soluble CD5 forms with an alternative cell surface ligand. Eur J Immunol. 29:1999;2119-2129.
28. Gringhuis S.I., de Leij L.F., Coffer P.J., Vellenga E. Signaling through CD5 activates a pathway involving phosphatidylinositol 3-kinase, Vav, and Rac1 in human mature T lymphocytes. Mol Cell Biol. 18:1998;1725-1735.
29. Calvo J., Vilda J.M., Places L., Simarro M., Padilla O., Andreu D., Campbell K.S., Aussel C., Lozano F. Human CD5 signaling and constitutive phosphorylation of C-terminal serine residues by casein kinase II. J Immunol. 161:1998;6022-6029. The authors use Jurkat T cell transfectants of CD5 cytoplasmic tail mutants to detect phosphorylation sites relevant to signal transduction, demonstrating that casein kinase II (CK2) associates with and phosphorylates the carboxy-terminal region of CD5 - a conserved domain known to be relevant for the generation of second lipid messengers.
30. Raman C., Kimberly R.P. Differential CD5-dependent regulation of CD5-associated CK2 activity in mature and immature T cells: implication on TCR/CD3-mediated activation. J Immunol. 161:1998;5817-5820. The authors suggest a mechanism for the established difference in CD5 regulation of TCR-induced signaling at immature and mature stages of developing T cells. They show that CD5-specific cross-linking activates associated CK2 in thymocytes but not in mature splenocytes and propose that CD5 modulates antigen receptor activity through this developmentally regulated activation of CD5-associated CK2.
31. 2+/calmodulin-dependent kinase IIδ and Tctex-1, a light chain component of the dynein motor complex. The interaction of CD5 with calmodulin-dependent kinase was also shown in vitro using fusion proteins.
32. Simarro M., Calvo J., Vila J.M., Places L., Padilla O., Alberola-Ila J., Vives J., Lozano F. Signaling through CD5 involves acidic sphingomyelinase, protein kinase C-zeta, mitogen-activated protein kinase kinase, and c-Jun NH2-terminal kinase. J Immunol. 162:1999;5149-5155.
33. Pers J.O., Jamin C., Le Corre R., Lydyard P.M., Youinou P. Ligation of CD5 on resting B cells, but not on resting T cells, results in apoptosis. Eur J Immunol. 28:1998;4170-4176.
34. Azzam H.S., Grinberg A., Lui K., Shen H., Shores E.W., Love P.E. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J Exp Med. 188:1998;2301-2311. Study of the mechanism of CD5 upregulation during thymocyte development. The role of TCR signaling in induction of CD5 was assessed in vitro, by using self antigen (MHC class I and class II) deficient mice or TCR transgenic mice known to experience negative or positive selection. Demonstrates CD5 upregulation that depends on MHC class I/II (self-antigen) and TCR avidity/signal during thymocyte development and a role for CD5 in negative and positive selection.
35. Berland R., Wortis H.H. An NFAT-dependent enhancer is necessary for anti-IgM-mediated induction of murine CD5 expression in primary splenic B cells. J Immunol. 161:1998;277-285. Using luciferase reporter constructs, the authors demonstrate that the induction of B cell CD5 expression requires NFAT binding and binding to at least one of three additional sites in the CD5 enhancer.
36. Sakiyama T., Ikuta K., Nisitani S., Takatsu K., Honjo T. Requirement of IL-5 for induction of autoimmune hemolytic anemia in anti-red blood cell autoantibody transgenic mice. Int Immunol. 11:1999;995-1000.
37. Nisitani S., Sakiyama T., Honjo T. Involvement of IL-10 in induction of autoimmune hemolytic anemia in anti-erythrocyte Ig transgenic mice. Int Immunol. 10:1998;1039-1047.
38. Watanabe N., Nisitani S., Ikuta K., Suzuki M., Chiba T., Honjo T. Expression levels of B cell surface immunoglobulin regulate efficiency of allelic exclusion and size of autoreactive B-1 cell compartment. J Exp Med. 190:1999;461-470.
39. Vink A., Warnier G., Brombacher F., Renauld J.C. Interleukin 9-induced in vivo expansion of the B-1 lymphocyte population. J Exp Med. 189:1999;1413-1423.
40. Potter M., Wax J.S., Hansen C.T., Kenny J.J. BALB/c.CBA/N mice carrying the defective Btk(xid) gene are resistant to pristane-induced plasmacytomagenesis. Int Immunol. 11:1999;1059-1064.
41. Boes M., Prodeus A.P., Schmidt T., Carroll M.C., Chen J. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med. 188:1998;2381-2386.
42. Boes M., Esau C., Fischer M.B., Schmidt T., Carroll M., Chen J. Enhanced B-1 cell development, but impaired IgG antibody responses in mice deficient in secreted IgM. J Immunol. 160:1998;4776-4787.
43. Yang Y.G., deGoma E., Barth R., Sergio J.J., Sykes M. B-cell reconstitution and xenoreactive anti-pig natural antibody production in severe combined immunodeficient mice reconstituted with immunocompetent B cells from varying sources. Transplantation. 66:1998;89-95.
44. Yang Y.G., deGoma E., Ohdan H., Bracy J.L., Xu Y., Iacomini J., Thall A.D., Sykes M. Tolerization of anti-Gal alpha1-3 Gal natural antibody-forming B cells by induction of mixed chimerism. J Exp Med. 187:1998;1335-1342.
45. Kroese F.G., Bos N.A. Peritoneal B-1 cells switch in vivo to IgA and these IgA antibodies can bind to bacteria of the normal intestinal microflora. Curr Top Microbiol Immunol. 246:1999;343-349.
46. de Waard R., Dammers P.M., Tung J.W., Kantor A.B., Wilshire J.A., Bos N.A., Herzenberg L.A., Kroese F.G. Presence of germline and full-length IgA RNA transcripts among peritoneal B-1 cells. Dev Immunol. 6:1998;81-87.
47. Bao S., Beagley K.W., Murray A.M., Caristo V., Matthaei K.I., Young I.G., Husband A.J. Intestinal IgA plasma cells of the B1 lineage are IL-5 dependent. Immunology. 94:1998;181-188.
48. Itoh M., Ishihara K., Hiroi T., Lee B.O., Maeda H., Iijima H., Yanagita M., Kiyono H., Hirano T. Deletion of bone marrow stromal cell antigen-1 (CD157) gene impaired systemic thymus independent-2 antigen-induced IgG3 and mucosal TD antigen-elicited IgA responses. J Immunol. 161:1998;3974-3983.
49. Ben-Yehuda A., Szabo P., LeMaoult J., Manavalan J.S., Weksler M.E. Increased VH 11 and VH Q52 gene use by splenic B cells in old mice associated with oligoclonal expansions of CD5 + B cells. Mech Ageing Dev. 103:1998;111-121.
50. LeMaoult J., Manavalan J.S., Dyall R., Szabo P., Nikolic-Zugic J., Weksler M.E. Cellular basis of B cell clonal populations in old mice. J Immunol. 162:1999;6384-6391.
51. Davidson W.F., Giese T., Fredrickson T.N. Spontaneous development of plasmacytoid tumors in mice with defective Fas-Fas ligand interactions. J Exp Med. 187:1998;1825-1838.
52. Karras J.G., Wang Z., Huo L., Howard R.G., Frank D.A., Rothstein T.L. Signal transducer and activator of transcription-3 (STAT3) is constitutively activated in normal, self-renewing B-1 cells but only inducibly expressed in conventional B lymphocytes. J Exp Med. 185:1997;1035-1042.
53. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., Darnell J.E. Jr. Stat3 as an oncogene. Cell. 98:1999;295-303.
54. Tanguay D.A., Colarusso T.P., Pavlovic S., Irigoyen M., Howard R.G., Bartek J., Chiles T.C., Rothstein T.L. Early induction of cyclin D2 expression in phorbol ester-responsive B-1 lymphocytes. J Exp Med. 189:1999;1685-1690.
55. Hamano Y., Hirose S., Ida A., Abe M., Zhang D., Kodera S., Jiang Y., Shirai J., Miura Y., Nishimura H., Shirai T. Susceptibility alleles for aberrant B-1 cell proliferation involved in spontaneously occurring B-cell chronic lymphocytic leukemia in a model of New Zealand white mice. Blood. 92:1998;3772-3779.
56. Appleyard G.D., Wilkie B.N. Porcine CD5 gene and gene product identified on the basis of inter-species conserved cytoplasmic domain sequences. Vet Immunol Immunopathol. 60:1998;275-283.
57. Appleyard G.D., Wilkie B.N. Characterization of porcine CD5 and CD5+ B cells. Clin Exp Immunol. 111:1998;225-230.
58. Chevallier N., Berthelemy M., Laine V., Le Rhun D., Femenia F., Polack B., Naessens J., Levy D., Schwartz-Cornil I. B-1-like cells exist in sheep. Characterization of their phenotype and behaviour. Immunology. 95:1998;178-184.
59. Koskinen R., Gobel T.W., Tregaskes C.A., Young J.R., Vainio O. The structure of avian CD5 implies a conserved function. J Immunol. 160:1998;4943-4950.