Home LiteratureArticle Details
PMID: 8070406 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

The IgM antigen receptor of B lymphocytes is associated with prohibitin and a prohibitin-related protein.

The EMBO journal ·Vol. 13 ·No. 16 ·1994-08-15 ·Pages 3782-92

Terashima M, Kim KM, Adachi T, Nielsen PJ, Reth M, Köhler G, Lamers MC

Abstract

The two major classes of antigen receptors on murine B lymphocytes, mIgM and mIgD, are both contained in a complex with two additional molecules, Ig-alpha and Ig-beta, which permit signal transduction. Accordingly, early biochemical events after antigen binding to either receptor are similar; biological effects, however, are different. Here, we describe three newly discovered intracellular proteins of 32, 37 and 41 kDa molecular mass, that are non-covalently associated with mIgM, but not with mIgD. These proteins coprecipitate with mIgM in Triton X-100 and Nonidet P-40, but not in digitonin lysates. In addition, mIgM is to some extent associated with 29 and 31 kDa proteins that are predominantly associated with mIgD (see accompanying paper). Amino acid sequencing of p32 and p37 identified p32 as mouse prohibitin; this was corroborated by Western blot analysis with antibodies specific for rat prohibitin. p37 is a newly discovered protein. cDNA clones for both proteins were isolated and sequenced. The deduced amino acid sequence of p32 is identical to that of rat prohibitin. p37 is highly homologous to p32. Since prohibitin was identified as an inhibitor of cell proliferation, its association with mIgM, but not mIgD, could explain the different biological events elicited after engagement of each receptor.

MeSH Terms
Amino Acid Sequence Animals B-Lymphocytes/immunology Base Sequence Cloning, Molecular Immunoglobulin D/analysis Immunoglobulin M/analysis Mice Mice, Inbred C57BL Molecular Sequence Data Prohibitins Proteins/analysis,genetics Receptors, Antigen, B-Cell/analysis,chemistry Repressor Proteins Sequence Analysis Sequence Homology, Amino Acid Spleen/cytology
Chemicals
Immunoglobulin D Immunoglobulin M Prohibitins Proteins Receptors, Antigen, B-Cell Repressor Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Terashima M
Max-Planck-Institut für Immunobiologie, Freiburg, Germany.
Kim K M
Adachi T
Nielsen P J
Reth M
Köhler G
Lamers M C
References (79)
79 references, click to expand
  1. The genes for a mouse hematopoietic differentiation marker called the heat-stable antigen.
    Eur J Immunol. 1991 Apr;21(4):1039-46 PMID: 2019286
  2. Sequence and expression of the Cc gene, a member of the dopa decarboxylase gene cluster of Drosophila: possible translational regulation.
    Nucleic Acids Res. 1986 Aug 11;14(15):6169-83 PMID: 3092183
  3. The alpha/beta sheath and its cytoplasmic tyrosines are required for signaling by the B-cell antigen receptor but not for capping or for serine/threonine-kinase recruitment.
    Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):474-8 PMID: 8290550
  4. Absence of prohibitin gene mutations in human epithelial ovarian tumors.
    Gynecol Oncol. 1993 Jul;50(1):34-7 PMID: 8349162
  5. Regulation of IgM and IgD synthesis in B lymphocytes. I. Changes in biosynthesis of mRNA for mu- and delta-chains.
    J Immunol. 1984 Mar;132(3):1561-5 PMID: 6420468
  6. Transmembrane signals and intracellular "second messengers" in the regulation of quiescent B-lymphocyte activation.
    Immunol Rev. 1987 Feb;95:37-57 PMID: 2437013
  7. Membrane IgD and membrane IgM differ in capacity to transduce inhibitory signals within the same human B cell clonal populations.
    J Immunol. 1989 Sep 1;143(5):1565-74 PMID: 2788188
  8. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  9. Functional differences between immunoglobulins M and D expressed on the surface of an immature B-cell line.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6914-8 PMID: 3137579
  10. Molecular requirements for the mu-induced light chain gene rearrangement in pre-B cells.
    EMBO J. 1991 Aug;10(8):2147-55 PMID: 1712291
  11. Immunoglobulin receptor-associated molecules.
    Adv Immunol. 1993;54:337-92 PMID: 8379465
  12. Effects of neonatal anti-delta antibody treatment on the murine immune system. II. Functional capacity of a stable sIgM+sIa+sIgD- B cell population.
    J Immunol. 1983 Aug;131(2):601-5 PMID: 6602841
  13. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene.
    Nature. 1991 Apr 4;350(6317):423-6 PMID: 1901381
  14. Immunoglobulin M and D antigen receptors are both capable of mediating B lymphocyte activation, deletion, or anergy after interaction with specific antigen.
    J Exp Med. 1992 Oct 1;176(4):991-1005 PMID: 1402669
  15. Anti-IgM but not anti-IgD antibodies inhibit cell division of normal human mature B cells.
    J Immunol. 1992 Jan 1;148(1):29-34 PMID: 1727873
  16. Growth regulation of a human mature B cell line, B104, by anti-IgM and anti-IgD antibodies.
    J Immunol. 1991 Feb 1;146(3):819-25 PMID: 1988498
  17. A novel 34-kd protein co-isolated with the IgM molecule in surface IgM-expressing cells.
    EMBO J. 1988 Nov;7(11):3451-6 PMID: 3264786
  18. Induction of apoptosis in fibroblasts by c-myc protein.
    Cell. 1992 Apr 3;69(1):119-28 PMID: 1555236
  19. Cloning of B cells positive or negative for surface IgD. II. Triggering and tolerance in the T-dependent splenic focus assay.
    J Immunol. 1979 Aug;123(2):709-13 PMID: 379216
  20. Signal transduction by immunoglobulin is mediated through Ig alpha and Ig beta.
    J Exp Med. 1993 Sep 1;178(3):1049-55 PMID: 7688784
  21. Protein conformational prediction.
    Trends Biochem Sci. 1989 Jul;14(7):295-9 PMID: 2672453
  22. Signal sequences. The limits of variation.
    J Mol Biol. 1985 Jul 5;184(1):99-105 PMID: 4032478
  23. Immunoglobulin-receptors revisited.
    Science. 1975 Sep 19;189(4207):964-9 PMID: 1083069
  24. Regulation of immunoglobulin D synthesis in murine neonatal B lymphocytes.
    Mol Cell Biol. 1986 Apr;6(4):1015-22 PMID: 3491288
  25. Assignment of the human prohibitin gene (PHB) to chromosome 17 and identification of a DNA polymorphism.
    Genomics. 1991 Sep;11(1):228-30 PMID: 1684951
  26. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum.
    Anal Biochem. 1984 Feb;137(1):266-7 PMID: 6329026
  27. B cell tolerance induction by cross-linking of membrane IgM, but not IgD, and synergy by cross-linking of both isotypes.
    J Immunol. 1993 Mar 1;150(5):1663-9 PMID: 8436810
  28. Prohibitin, an evolutionarily conserved intracellular protein that blocks DNA synthesis in normal fibroblasts and HeLa cells.
    Mol Cell Biol. 1991 Mar;11(3):1372-81 PMID: 1996099
  29. Receptor signalling and crosstalk in B lymphocytes.
    Immunol Rev. 1987 Oct;99:19-38 PMID: 2824341
  30. Cellular signalling mechanisms in B lymphocytes.
    Biochem J. 1993 Jun 1;292 ( Pt 2):313-32 PMID: 8503867
  31. A novel germ-line JK transcript starting immediately upstream of JK1.
    Nucleic Acids Res. 1989 Sep 12;17(17):6809-19 PMID: 2506531
  32. Cell cycle activity and expression of prohibitin mRNA.
    J Cell Physiol. 1993 Nov;157(2):289-95 PMID: 8227162
  33. Regulation of surface IgM- and IgD-mediated inositol phosphate formation and Ca2+ mobilization in murine B lymphocytes.
    Eur J Immunol. 1989 Oct;19(10):1933-9 PMID: 2555196
  34. Somatic cell hybrid mapping on mouse chromosome 11 (MMU11): assignment of markers relative to two breakpoints in band D.
    Genomics. 1993 Feb;15(2):323-31 PMID: 8449498
  35. Immunoglobulins D and M mediate signals that are qualitatively different in B cells with an immature phenotype.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6919-23 PMID: 3261870
  36. The B-cell antigen receptor: structure and function of primary, secondary, tertiary and quaternary components.
    Immunol Rev. 1993 Apr;132:85-106 PMID: 8349299
  37. Cloning and sequencing of mouse ribosomal protein S12 cDNA.
    Nucleic Acids Res. 1989 Aug 25;17(16):6722 PMID: 2780296
  38. Blocking of primary in vitro antibody responses to thymus-independent and thymus-dependent antigens with antiserum specific for IgM or IgD.
    Proc Natl Acad Sci U S A. 1978 Jan;75(1):432-5 PMID: 305047
  39. Role of IgD in the immune response and tolerance. II. Precursor analysis of murine B cells separated on the basis of surface IgD or treated with an anti-delta serum.
    Eur J Immunol. 1978 Jan;8(1):13-6 PMID: 416959
  40. The relationship between surface immunoglobulin isotype and immune function of murine B lymphocytes. V. IgD-bearing cells in immunological tolerance.
    Eur J Immunol. 1982 Oct;12(10):838-44 PMID: 6983441
  41. B-cell antigen receptor motifs have redundant signalling capabilities and bind the tyrosine kinases PTK72, Lyn and Fyn.
    Curr Biol. 1993 Oct 1;3(10):645-57 PMID: 15335855
  42. Structure of genes for membrane and secreted murine IgD heavy chains.
    Nature. 1982 Apr 1;296(5856):410-5 PMID: 6801528
  43. Early B cell development requires mu signaling.
    Eur J Immunol. 1993 Oct;23(10):2622-30 PMID: 8405063
  44. The role of DNA rearrangement and alternative RNA processing in the expression of immunoglobulin delta genes.
    Cell. 1981 May;24(2):353-65 PMID: 6786756
  45. Cross-linking of B cell receptor-related MB-1 molecule induces protein tyrosine phosphorylation in early B lineage cells.
    J Immunol. 1993 May 1;150(9):3766-75 PMID: 8473731
  46. Receptor-mediated antigen uptake and its effect on antigen presentation to class II-restricted T lymphocytes.
    Annu Rev Immunol. 1990;8:773-93 PMID: 2188679
  47. Severe progressive erosive arthritis in multicentric reticulohistiocytosis: possible involvement of cytokines in synovial proliferation.
    J Rheumatol. 1992 Oct;19(10):1643-6 PMID: 1464883
  48. B-cell tolerance. III. Effect of papain-mediated cleavage of cell surface IgD on tolerance susceptibility of murine B cells.
    J Exp Med. 1977 Jul 1;146(1):107-17 PMID: 68987
  49. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor.
    J Biol Chem. 1990 Feb 25;265(6):3116-23 PMID: 1968060
  50. Development of the primary antibody repertoire.
    Science. 1987 Nov 20;238(4830):1079-87 PMID: 3317825
  51. Biochemistry of B lymphocyte activation.
    Adv Immunol. 1994;55:221-95 PMID: 8304234
  52. The relationship between surface immunoglobulin isotype and immune function of murine B lymphocytes. IV. Role of IgD-bearing cells in the propagation of immunologic memory.
    J Immunol. 1979 Aug;123(2):925-30 PMID: 313424
  53. Dual role of the tyrosine activation motif of the Ig-alpha protein during signal transduction via the B cell antigen receptor.
    EMBO J. 1994 Jan 1;13(1):83-9 PMID: 8306975
  54. Induction of murine B cell proliferation by insolubilized anti-immunoglobulins.
    J Immunol. 1980 Sep;125(3):1240-2 PMID: 6967895
  55. Immunoglobulin D (IgD)-deficient mice reveal an auxiliary receptor function for IgD in antigen-mediated recruitment of B cells.
    J Exp Med. 1993 Jan 1;177(1):45-55 PMID: 8418208
  56. Cell surface immunoglobulin. XI. The appearance of an IgD-like molecule on murine lymphoid cells during ontogeny.
    J Exp Med. 1975 Jan 1;141(1):206-15 PMID: 1090697
  57. Cloning of B cells positive or negative for surface IgD. I. Triggering and tolerance in T-independent systems.
    J Immunol. 1979 Aug;123(2):702-8 PMID: 379215
  58. Synthesis of secreted and membrane-bound immunoglobulin mu heavy chains is directed by mRNAs that differ at their 3' ends.
    Cell. 1980 Jun;20(2):293-301 PMID: 6771018
  59. The syntaxin family of vesicular transport receptors.
    Cell. 1993 Sep 10;74(5):863-73 PMID: 7690687
  60. Activation of V kappa gene rearrangement in pre-B cells follows the expression of membrane-bound immunoglobulin heavy chains.
    EMBO J. 1987 Nov;6(11):3299-305 PMID: 3123216
  61. Expression of prohibitin in rat seminiferous epithelium.
    Biol Reprod. 1993 Aug;49(2):300-10 PMID: 8373953
  62. The B cell antigen receptor complex: association of Ig-alpha and Ig-beta with distinct cytoplasmic effectors.
    Science. 1992 Oct 2;258(5079):123-6 PMID: 1439759
  63. Differentiation of growth signal requirement of B lymphocyte precursor is directed by expression of immunoglobulin.
    EMBO J. 1991 Feb;10(2):337-42 PMID: 1899373
  64. A role for immunoglobulin D: interference with tolerance induction.
    Eur J Immunol. 1993 Jan;23(1):168-78 PMID: 8419167
  65. The murine B cell response to TNP-polyacrylamide beads: the relationship between the epitope density of the antigen and the requirements for T cell help and surface IgD.
    J Immunol. 1980 Jul;125(1):420-7 PMID: 6155404
  66. Allele losses in the region 17q12-21 in familial breast and ovarian cancer involve the wild-type chromosome.
    Nat Genet. 1992 Oct;2(2):128-31 PMID: 1303261
  67. Antigen receptor tail clue.
    Nature. 1989 Mar 30;338(6214):383-4 PMID: 2927501
  68. Acylation of viral and eukaryotic proteins.
    Biochem J. 1989 Mar 15;258(3):625-38 PMID: 2658970
  69. Differential signaling through the Ig-alpha and Ig-beta components of the B cell antigen receptor.
    Eur J Immunol. 1993 Apr;23(4):911-6 PMID: 7681402
  70. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  71. Two mRNAs can be produced from a single immunoglobulin mu gene by alternative RNA processing pathways.
    Cell. 1980 Jun;20(2):313-9 PMID: 6771020
  72. Cell surface immunoglobulin. X. Identification of an IgD-like molecule on the surface of murine splenocytes.
    J Exp Med. 1974 Nov 1;140(5):1427-31 PMID: 4417345
  73. Immunoglobulin D-deficient mice can mount normal immune responses to thymus-independent and -dependent antigens.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1887-91 PMID: 8446604
  74. Growth inhibition of a B cell clone mediated by ligation of IL-4 receptors or membrane IgM.
    J Immunol. 1993 Apr 1;150(7):2565-74 PMID: 8454843
  75. Two mRNAs with different 3' ends encode membrane-bound and secreted forms of immunoglobulin mu chain.
    Cell. 1980 Jun;20(2):303-12 PMID: 6771019
  76. Antigen receptors on B lymphocytes.
    Annu Rev Immunol. 1992;10:97-121 PMID: 1591006
  77. Endogenous expression of delta on the surface of WEHI-231. Characterization of its expression and signaling properties.
    J Immunol. 1993 Nov 1;151(9):4681-93 PMID: 8409428
  78. Polyclonal activation of the murine immune system by an antibody to IgD. I. Increase in cell size and DNA synthesis.
    J Immunol. 1982 Aug;129(2):629-37 PMID: 6177772
  79. Candidate for immunoglobulin D present on murine B lymphocytes.
    Nature. 1974 Dec 13;252(5484):600-2 PMID: 4215039
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1994-08-15
Pages
3782-92
Language
English
Region
England
NLM ID
8208664
PMCID
PMC395291
Subset
IM
Databases
GENBANK
X78682, X78683, X78684
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]