Maintenance of CD5+ B cells at an early developmental stage by interleukin-5: evidence from immunoglobulin gene usage in interleukin-5 transgenic mice.

We have characterized the development and expansion of CD5+ B cells in interleukin-5 (IL-5) transgenic mice in terms of autoantibody production and immunoglobulin gene usage. CD5+IL-5R alpha+ B cells maintained in the presence of IL-5 secreted fewer autoantibodies and had fewer N nucleotides at the 3' end of the D elements compared with CD5- B cells. The reduction in nucleotides, along with the finding that CD5+IL-5R alpha+ B cells in IL-5 transgenic mice use Q52 families more frequently than age-matched control B cells, also suggests that these cells have the characteristics of fetus-type B cells and represent an early stage of B-cell development. All of the VH11 families were expressed with JH1 and the Q52 families were frequently expressed with JH1. Furthermore, JH proximal DQ52 was frequently used in IL-5 transgenic mice. All of these characteristics in terms of immunoglobulin gene usage have been described for CD5+ B cells. These results suggest that IL-5 maintains CD5+ B cells that have a fetus-type of immunoglobulin gene usage. This cytokine could be responsible for prolonging the life span of immature CD5+ B cells, which subsequently mature to CD5- B cells that secrete polyreactive natural antibodies.

[1]  T. Honjo,et al.  Antigen-induced apoptotic death of Ly-1 B cells responsible for autoimmune disease in transgenic mice , 1992, Nature.

[2]  A. Kantor,et al.  Layered Evolution in the Immune System , 1992 .

[3]  L. Herzenberg,et al.  Characteristics and Development of the Murine B‐lb (Ly‐1 B Sister) Cell Population , 1992, Annals of the New York Academy of Sciences.

[4]  R. Hardy,et al.  Generation of Ly‐1 B Cells from Developmentally Distinct Precursors , 1992, Annals of the New York Academy of Sciences.

[5]  A. Cumano,et al.  Bipotential precursors of B cells and macrophages in murine fetal liver , 1992, Nature.

[6]  J. Kearney,et al.  An embryonic source of Ly1 but not conventional B cells. , 1991, International immunology.

[7]  H. Wortis,et al.  Treatment of murine CD5- B cells with anti-Ig, but not LPS, induces surface CD5: two B-cell activation pathways. , 1991, International immunology.

[8]  I. Sanz,et al.  Comparison of D, JH, and junctional diversity in the fetal, adult, and aged B cell repertoires. , 1991, Journal of immunology.

[9]  N. Yamaguchi,et al.  In vivo administration of antibody to murine IL-5 receptor inhibits eosinophilia of IL-5 transgenic mice. , 1991, International immunology.

[10]  J. Miyazaki,et al.  Transgenic mice expressing a B cell growth and differentiation factor gene (interleukin 5) develop eosinophilia and autoantibody production , 1991, The Journal of experimental medicine.

[11]  A. Feeney Lack of N regions in fetal and neonatal mouse immunoglobulin V-D-J junctional sequences , 1990, The Journal of experimental medicine.

[12]  M. Migita,et al.  Elevated Expression of Proto‐Oncogenes during Interleukin‐5‐Induced Growth and Differentiation of Murine B Lineage Cells , 1990, Microbiology and immunology.

[13]  J. Teale,et al.  Contribution of the CD5+ B cell to D-proximal VH family expression early in ontogeny. , 1990, Journal of immunology.

[14]  L. Schook,et al.  Clonal analysis of gene expression by PCR. , 1990, BioTechniques.

[15]  T. Suda,et al.  Structural comparison of murine T-cell (B151K12)-derived T-cell-replacing factor (IL-5) with rIL-5: dimer formation is essential for the expression of biological activity. , 1990, Molecular immunology.

[16]  A. Rolink,et al.  Characterization of the interleukin 5‐reactive splenic B cell population , 1990, European journal of immunology.

[17]  D. Mosier,et al.  The immunoglobulin allotype contributed by peritoneal cavity B cells dominates in SCID mice reconstituted with allotype-disparate mixtures of splenic and peritoneal cavity B cells , 1990, The Journal of experimental medicine.

[18]  S. Shinton,et al.  Rearrangement and selection of VH11 in the Ly-1 B cell lineage , 1990, The Journal of experimental medicine.

[19]  K. Rajewsky,et al.  Sequence homologies, N sequence insertion and JH gene utilization in VHDJH joining: implications for the joining mechanism and the ontogenetic timing of Ly1 B cell and B‐CLL progenitor generation. , 1990, The EMBO journal.

[20]  P. Poncet,et al.  All VH11 genes expressed in peritoneal lymphocytes encode anti‐bromelain‐treated mouse red blood cell autoantibodies but other VH gene families contribute to this specificity , 1990, European journal of immunology.

[21]  N. Yamaguchi,et al.  Distribution of IL-5 receptor-positive B cells. Expression of IL-5 receptor on Ly-1(CD5)+ B cells. , 1990, Journal of immunology.

[22]  H. Sugiyama,et al.  Estimation of D segment usage in initial D to JH joinings in a murine immature B cell line. Preferential usage of DFL16.1, the most 5' D segment and DQ52, the most JH-proximal D segment. , 1990, Journal of immunology.

[23]  A. Freitas,et al.  VH gene family repertoires of “viable motheaten” (mev) mice , 1990, European journal of immunology.

[24]  C. Bona,et al.  Autoantibodies, LY-1, and immunoglobulin V gene expression in hybridomas obtained from young and from old New Zealand black mice. , 1990, Arthritis and rheumatism.

[25]  N. Yamaguchi,et al.  Characterization of the murine interleukin 5 receptor by using a monoclonal antibody. , 1990, International immunology.

[26]  S. Clarke,et al.  Organization and expression of vh gene families preferentially expressed by ly‐1+ (cd5) b cells , 1989, European journal of immunology.

[27]  Y. Kurosawa,et al.  Only dfl16, dsp2, and dq52 gene families exist in mouse immunoglobulin heavy chain diversity gene loci, of which dfl16 and dsp2 originate from the same primordial dh gene , 1989, European journal of immunology.

[28]  A. Coutinho,et al.  Beyond Clonal Selection and Network , 1989, Immunological reviews.

[29]  R. Coffman,et al.  Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. , 1989, Science.

[30]  A. Coutinho,et al.  Immunoglobulin VH gene expression in Ly‐1+ and conventional B lymphocytes , 1989, European journal of immunology.

[31]  S. Shinton,et al.  A single VH gene is utilized predominantly in anti-BrMRBC hybridomas derived from purified Ly-1 B cells. Definition of the VH11 family. , 1989, Journal of immunology.

[32]  T. Honjo,et al.  Characterization of high-affinity receptors for interleukin 5 on interleukin 5-dependent cell lines. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[33]  K. G. Nickerson,et al.  Early human IgH gene assembly in Epstein-Barr virus-transformed fetal B cell lines. Preferential utilization of the most JH-proximal D segment (DQ52) and two unusual VH-related rearrangements , 1989, The Journal of experimental medicine.

[34]  L. Herzenberg,et al.  Feedback regulation of murine Ly‐1 B cell development , 1989, European journal of immunology.

[35]  L. Herzenberg,et al.  Ly-1 B-cell clones similar to human chronic lymphocytic leukemias routinely develop in older normal mice and young autoimmune (New Zealand Black-related) animals. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[36]  L. Arnold,et al.  Normal mouse peritoneum contains a large population of Ly-1+ (CD5) B cells that recognize phosphatidyl choline. Relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes , 1988, The Journal of experimental medicine.

[37]  S. Rudikoff,et al.  Relationships between B cell and myeloid differentiation. Studies with a B lymphocyte progenitor line, HAFTL-1 , 1988, The Journal of experimental medicine.

[38]  R. Coffman,et al.  The Role of Helper T Cell Products in Mouse B Cell Differentiation and Isotype Regulation , 1988, Immunological reviews.

[39]  N. Yamaguchi,et al.  T Cell‐Replacing Factor (TRF)/Interleukin 5 (IL‐5): Molecular and Functional Properties , 1988, Immunological reviews.

[40]  C. Sanderson,et al.  Molecular and Cellular Biology of Eosinophil Differentiation Factor (Interleukin‐5) and its Effects on Human and Mouse B Cells , 1988, Immunological reviews.

[41]  R. Coffman,et al.  Isolation and characterization of lymphokine cDNA clones encoding mouse and human IgA-enhancing factor and eosinophil colony-stimulating factor activities: relationship to interleukin 5. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Mazié,et al.  Age-related natural antibody specificities among hybridoma clones originating from NZB spleen. , 1987, Immunology.

[43]  T. Honjo,et al.  Production of a monoclonal antibody useful in the molecular characterization of murine T-cell-replacing factor/B-cell growth factor II. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[44]  P. Gearhart,et al.  Adult B-cell repertoire is biased toward two heavy-chain variable-region genes that rearrange frequently in fetal pre-B cells. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[45]  T. Honjo,et al.  Cloning of complementary DNA encoding T-cell replacing factor and identity with B-cell growth factor II , 1986, Nature.

[46]  R. Hardy,et al.  Development and Physiology of LY‐1 B and its Human Homolog, LEU‐1 B , 1986, Immunological reviews.

[47]  L. Herzenberg,et al.  The LY‐1B Cell Lineage , 1986 .

[48]  R. Hardy,et al.  Production of immunoglobulin isotypes by Ly-1+ B cells in viable motheaten and normal mice. , 1986, Science.

[49]  R. Hardy,et al.  Progenitors for Ly-1 B cells are distinct from progenitors for other B cells , 1985, The Journal of experimental medicine.

[50]  S. Hardy,et al.  Autoantibodies against mouse bromelain-modified RBC are specifically inhibited by a common membrane phospholipid, phosphatidylcholine. , 1985, Immunology.

[51]  A. Coutinho,et al.  High frequency of natural autoantibodies in normal newborn mice. , 1985, Journal of immunology.

[52]  L. Shultz,et al.  "Viable motheaten," a new allele at the motheaten locus. I. Pathology. , 1984, The American journal of pathology.

[53]  R. Hardy,et al.  The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice , 1983, The Journal of experimental medicine.

[54]  R. Hardy,et al.  B‐CELL SUBPOPULATIONS IDENTIFIABLE BY TWO‐COLOR FLUORESCENCE ANALYSIS USING A DUAL‐LASER FACS * , 1982, Annals of the New York Academy of Sciences.

[55]  W. Leiserson,et al.  Expression of Lyt-1 by a subset of B lymphocytes. , 1982, Journal of immunology.

[56]  S. Tonegawa,et al.  Organization, structure, and assembly of immunoglobulin heavy chain diversity DNA segments , 1982, The Journal of experimental medicine.

[57]  I. Weissman,et al.  B220: a B cell-specific member of the T200 glycoprotein family , 1981, Nature.

[58]  Hitoshi Sakano,et al.  Two types of somatic recombination are necessary for the generation of complete immunoglobulin heavy-chain genes , 1980, Nature.

[59]  M. Migita,et al.  Conversion of Normal Ly-1-Positive B-Lineage Cells into Ly-1-Positive Macrophages in Long-Term Bone Marrow Cultures , 1990, Developmental immunology.

[60]  P. Casali,et al.  Probing the human B-cell repertoire with EBV: polyreactive antibodies and CD5+ B lymphocytes. , 1989, Annual review of immunology.

[61]  S. Nishikawa,et al.  Establishment of IL-5-dependent early B cell lines by long-term bone marrow cultures. , 1989, Growth factors.

[62]  N. Yamaguchi,et al.  Interleukin-5 induces maturation but not class switching of surface IgA-positive B cells into IgA-secreting cells. , 1989, Immunology.

[63]  J. Kearney,et al.  The role of idiotypic interactions and B-cell subsets in development of the B-cell repertoire. , 1989, Cold Spring Harbor symposia on quantitative biology.

[64]  C. Kocks,et al.  Stable expression and somatic hypermutation of antibody V regions in B-cell developmental pathways. , 1989, Annual review of immunology.

[65]  R. Hardy,et al.  Normal, autoimmune, and malignant CD5+ B cells: the Ly-1 B lineage? , 1988, Annual review of immunology.

[66]  D. Holmberg High connectivity, natural antibodies preferentially use 7183 and QUPC52 VH families , 1987, European journal of immunology.

[67]  K. Rajewsky,et al.  Expansion and functional activity of Ly‐1+ B cells upon transfer of peritoneal cells into allotype‐congenic, newborn mice , 1987, European journal of immunology.

[68]  R. Hardy,et al.  Immunoglobulin‐bearing B cells reconstitute and maintain the murine Ly‐1 B cell lineage , 1986, European journal of immunology.

[69]  Y. Kanai,et al.  Naturally occurring antibodies to poly(ADP-ribose) in autoimmune MRL/Mp-lpr/lpr mice. , 1985, Clinical and experimental immunology.