Skip to main content
The EMBO Journal logoLink to The EMBO Journal
. 1994 Feb 15;13(4):816–826. doi: 10.1002/j.1460-2075.1994.tb06324.x

A selective defect in IgM antigen receptor synthesis and transport causes loss of cell surface IgM expression on tolerant B lymphocytes.

S E Bell 1, C C Goodnow 1
PMCID: PMC394880  PMID: 8112296

Abstract

To explore the biochemical basis for maintaining immunological tolerance by functional inactivation of self-reactive B lymphocytes, transgenic mice carrying rearranged anti-lysozyme immunoglobulin transgenes and a lysozyme transgene were used as a source of large numbers of tolerant self-reactive B cells. Antigen receptors of the IgD isotype were expressed at normal levels on tolerant B cells, contained the heterodimeric MB1/B29 signalling component of the receptor complex and were structurally indistinguishable from IgD on nontolerant B cells. In contrast, cell surface expression of IgM receptor complexes on tolerant B cells was greatly reduced, despite normal expression of mRNA encoding the receptor components. Three-fold fewer immunoreactive mu heavy chains were detectable after a short period of biosynthetic labelling and the immunoreactive mu chains produced were paired with kappa light chains and assembled normally into intact receptor complexes containing the MB1/B29 heterodimer. Nascent IgM receptor complexes nevertheless failed to be processed into an endoglycosidase H-resistant form in the tolerant B cells and thus appeared to be selectively blocked in their transport from the endoplasmic reticulum to the medial Golgi. These findings demonstrate that intracellular trafficking of antigen receptor complexes is regulated by exposure to receptor stimuli at the cell surface causing a long-lasting decrease in surface receptor expression on tolerant B cells.

Full text

PDF
816

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahluwalia N., Bergeron J. J., Wada I., Degen E., Williams D. B. The p88 molecular chaperone is identical to the endoplasmic reticulum membrane protein, calnexin. J Biol Chem. 1992 May 25;267(15):10914–10918. [PubMed] [Google Scholar]
  2. Basten A., Brink R., Peake P., Adams E., Crosbie J., Hartley S., Goodnow C. C. Self tolerance in the B-cell repertoire. Immunol Rev. 1991 Aug;122:5–19. doi: 10.1111/j.1600-065x.1991.tb00593.x. [DOI] [PubMed] [Google Scholar]
  3. Blum J. S., Cresswell P. Role for intracellular proteases in the processing and transport of class II HLA antigens. Proc Natl Acad Sci U S A. 1988 Jun;85(11):3975–3979. doi: 10.1073/pnas.85.11.3975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bonifacino J. S., McCarthy S. A., Maguire J. E., Nakayama T., Singer D. S., Klausner R. D., Singer A. Novel post-translational regulation of TCR expression in CD4+CD8+ thymocytes influenced by CD4. Nature. 1990 Mar 15;344(6263):247–251. doi: 10.1038/344247a0. [DOI] [PubMed] [Google Scholar]
  6. Burkhardt A. L., Brunswick M., Bolen J. B., Mond J. J. Anti-immunoglobulin stimulation of B lymphocytes activates src-related protein-tyrosine kinases. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7410–7414. doi: 10.1073/pnas.88.16.7410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cambier J. C., Campbell K. S. Signal transduction by B lymphocyte receptors: structure-function relationships of membrane immunoglobulins and associated molecules. Semin Immunol. 1990 Mar;2(2):139–149. [PubMed] [Google Scholar]
  8. Cambier J. C., Justement L. B., Newell M. K., Chen Z. Z., Harris L. K., Sandoval V. M., Klemsz M. J., Ransom J. T. Transmembrane signals and intracellular "second messengers" in the regulation of quiescent B-lymphocyte activation. Immunol Rev. 1987 Feb;95:37–57. doi: 10.1111/j.1600-065x.1987.tb00499.x. [DOI] [PubMed] [Google Scholar]
  9. Campbell K. S., Cambier J. C. B lymphocyte antigen receptors (mIg) are non-covalently associated with a disulfide linked, inducibly phosphorylated glycoprotein complex. EMBO J. 1990 Feb;9(2):441–448. doi: 10.1002/j.1460-2075.1990.tb08129.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Campbell K. S., Hager E. J., Cambier J. C. Alpha-chains of IgM and IgD antigen receptor complexes are differentially N-glycosylated MB-1-related molecules. J Immunol. 1991 Sep 1;147(5):1575–1580. [PubMed] [Google Scholar]
  11. Campbell K. S., Hager E. J., Friedrich R. J., Cambier J. C. IgM antigen receptor complex contains phosphoprotein products of B29 and mb-1 genes. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3982–3986. doi: 10.1073/pnas.88.9.3982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Campbell M. A., Sefton B. M. Association between B-lymphocyte membrane immunoglobulin and multiple members of the Src family of protein tyrosine kinases. Mol Cell Biol. 1992 May;12(5):2315–2321. doi: 10.1128/mcb.12.5.2315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chen J. Z., Stall A. M., Herzenberg L. A., Herzenberg L. A. Differences in glycoprotein complexes associated with IgM and IgD on normal murine B cells potentially enable transduction of different signals. EMBO J. 1990 Jul;9(7):2117–2124. doi: 10.1002/j.1460-2075.1990.tb07380.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Chen S. Z., Evans G. A. A simple screening method for transgenic mice using the polymerase chain reaction. Biotechniques. 1990 Jan;8(1):32–33. [PubMed] [Google Scholar]
  15. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  16. Costa T. E., Franke R. R., Sanchez M., Misulovin Z., Nussenzweig M. C. Functional reconstitution of an immunoglobulin antigen receptor in T cells. J Exp Med. 1992 Jun 1;175(6):1669–1676. doi: 10.1084/jem.175.6.1669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dang L. H., Rock K. L. Stimulation of B lymphocytes through surface Ig receptors induces LFA-1 and ICAM-1-dependent adhesion. J Immunol. 1991 May 15;146(10):3273–3279. [PubMed] [Google Scholar]
  18. David V., Hochstenbach F., Rajagopalan S., Brenner M. B. Interaction with newly synthesized and retained proteins in the endoplasmic reticulum suggests a chaperone function for human integral membrane protein IP90 (calnexin). J Biol Chem. 1993 May 5;268(13):9585–9592. [PubMed] [Google Scholar]
  19. DeFranco A. L. Molecular aspects of B-lymphocyte activation. Annu Rev Cell Biol. 1987;3:143–178. doi: 10.1146/annurev.cb.03.110187.001043. [DOI] [PubMed] [Google Scholar]
  20. Degen E., Williams D. B. Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules. J Cell Biol. 1991 Mar;112(6):1099–1115. doi: 10.1083/jcb.112.6.1099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dorner A. J., Wasley L. C., Kaufman R. J. Protein dissociation from GRP78 and secretion are blocked by depletion of cellular ATP levels. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7429–7432. doi: 10.1073/pnas.87.19.7429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Dunphy W. G., Brands R., Rothman J. E. Attachment of terminal N-acetylglucosamine to asparagine-linked oligosaccharides occurs in central cisternae of the Golgi stack. Cell. 1985 Feb;40(2):463–472. doi: 10.1016/0092-8674(85)90161-8. [DOI] [PubMed] [Google Scholar]
  23. Erikson J., Radic M. Z., Camper S. A., Hardy R. R., Carmack C., Weigert M. Expression of anti-DNA immunoglobulin transgenes in non-autoimmune mice. Nature. 1991 Jan 24;349(6307):331–334. doi: 10.1038/349331a0. [DOI] [PubMed] [Google Scholar]
  24. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  25. Freeman G. J., Freedman A. S., Segil J. M., Lee G., Whitman J. F., Nadler L. M. B7, a new member of the Ig superfamily with unique expression on activated and neoplastic B cells. J Immunol. 1989 Oct 15;143(8):2714–2722. [PubMed] [Google Scholar]
  26. Freiden P. J., Gaut J. R., Hendershot L. M. Interconversion of three differentially modified and assembled forms of BiP. EMBO J. 1992 Jan;11(1):63–70. doi: 10.1002/j.1460-2075.1992.tb05028.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Galvin K., Krishna S., Ponchel F., Frohlich M., Cummings D. E., Carlson R., Wands J. R., Isselbacher K. J., Pillai S., Ozturk M. The major histocompatibility complex class I antigen-binding protein p88 is the product of the calnexin gene. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8452–8456. doi: 10.1073/pnas.89.18.8452. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Gay D., Saunders T., Camper S., Weigert M. Receptor editing: an approach by autoreactive B cells to escape tolerance. J Exp Med. 1993 Apr 1;177(4):999–1008. doi: 10.1084/jem.177.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Germain R. N., Hendrix L. R. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature. 1991 Sep 12;353(6340):134–139. doi: 10.1038/353134a0. [DOI] [PubMed] [Google Scholar]
  30. Goodnow C. C., Brink R., Adams E. Breakdown of self-tolerance in anergic B lymphocytes. Nature. 1991 Aug 8;352(6335):532–536. doi: 10.1038/352532a0. [DOI] [PubMed] [Google Scholar]
  31. Goodnow C. C., Crosbie J., Adelstein S., Lavoie T. B., Smith-Gill S. J., Brink R. A., Pritchard-Briscoe H., Wotherspoon J. S., Loblay R. H., Raphael K. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature. 1988 Aug 25;334(6184):676–682. doi: 10.1038/334676a0. [DOI] [PubMed] [Google Scholar]
  32. Goodnow C. C., Crosbie J., Jorgensen H., Brink R. A., Basten A. Induction of self-tolerance in mature peripheral B lymphocytes. Nature. 1989 Nov 23;342(6248):385–391. doi: 10.1038/342385a0. [DOI] [PubMed] [Google Scholar]
  33. Goodnow C. C. Transgenic mice and analysis of B-cell tolerance. Annu Rev Immunol. 1992;10:489–518. doi: 10.1146/annurev.iy.10.040192.002421. [DOI] [PubMed] [Google Scholar]
  34. Guagliardi L. E., Koppelman B., Blum J. S., Marks M. S., Cresswell P., Brodsky F. M. Co-localization of molecules involved in antigen processing and presentation in an early endocytic compartment. Nature. 1990 Jan 11;343(6254):133–139. doi: 10.1038/343133a0. [DOI] [PubMed] [Google Scholar]
  35. Haas I. G., Wabl M. Immunoglobulin heavy chain binding protein. Nature. 1983 Nov 24;306(5941):387–389. doi: 10.1038/306387a0. [DOI] [PubMed] [Google Scholar]
  36. Hardy R. R., Hayakawa K., Haaijman J., Herzenberg L. A. B-cell subpopulations identified by two-colour fluorescence analysis. Nature. 1982 Jun 17;297(5867):589–591. doi: 10.1038/297589a0. [DOI] [PubMed] [Google Scholar]
  37. Hartley S. B., Cooke M. P., Fulcher D. A., Harris A. W., Cory S., Basten A., Goodnow C. C. Elimination of self-reactive B lymphocytes proceeds in two stages: arrested development and cell death. Cell. 1993 Feb 12;72(3):325–335. doi: 10.1016/0092-8674(93)90111-3. [DOI] [PubMed] [Google Scholar]
  38. Hartley S. B., Crosbie J., Brink R., Kantor A. B., Basten A., Goodnow C. C. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature. 1991 Oct 24;353(6346):765–769. doi: 10.1038/353765a0. [DOI] [PubMed] [Google Scholar]
  39. Hendershot L. M. Immunoglobulin heavy chain and binding protein complexes are dissociated in vivo by light chain addition. J Cell Biol. 1990 Sep;111(3):829–837. doi: 10.1083/jcb.111.3.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Hendershot L. M., Kearney J. F. A role for human heavy chain binding protein in the developmental regulation of immunoglobin transport. Mol Immunol. 1988 Jun;25(6):585–595. doi: 10.1016/0161-5890(88)90081-8. [DOI] [PubMed] [Google Scholar]
  41. Hendershot L. M., Ting J., Lee A. S. Identity of the immunoglobulin heavy-chain-binding protein with the 78,000-dalton glucose-regulated protein and the role of posttranslational modifications in its binding function. Mol Cell Biol. 1988 Oct;8(10):4250–4256. doi: 10.1128/mcb.8.10.4250. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Hendershot L., Bole D., Köhler G., Kearney J. F. Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain-binding protein. J Cell Biol. 1987 Mar;104(3):761–767. doi: 10.1083/jcb.104.3.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Hermanson G. G., Eisenberg D., Kincade P. W., Wall R. B29: a member of the immunoglobulin gene superfamily exclusively expressed on beta-lineage cells. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6890–6894. doi: 10.1073/pnas.85.18.6890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Hochstenbach F., David V., Watkins S., Brenner M. B. Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4734–4738. doi: 10.1073/pnas.89.10.4734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Hombach J., Leclercq L., Radbruch A., Rajewsky K., Reth M. A novel 34-kd protein co-isolated with the IgM molecule in surface IgM-expressing cells. EMBO J. 1988 Nov;7(11):3451–3456. doi: 10.1002/j.1460-2075.1988.tb03219.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Hombach J., Tsubata T., Leclercq L., Stappert H., Reth M. Molecular components of the B-cell antigen receptor complex of the IgM class. Nature. 1990 Feb 22;343(6260):760–762. doi: 10.1038/343760a0. [DOI] [PubMed] [Google Scholar]
  47. Kashiwamura S., Koyama T., Matsuo T., Steinmetz M., Kimoto M., Sakaguchi N. Structure of the murine mb-1 gene encoding a putative sIgM-associated molecule. J Immunol. 1990 Jul 1;145(1):337–343. [PubMed] [Google Scholar]
  48. Kassenbrock C. K., Kelly R. B. Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J. 1989 May;8(5):1461–1467. doi: 10.1002/j.1460-2075.1989.tb03529.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kehry M., Sibley C., Fuhrman J., Schilling J., Hood L. E. Amino acid sequence of a mouse immunoglobulin mu chain. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2932–2936. doi: 10.1073/pnas.76.6.2932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Klausner R. D., Lippincott-Schwartz J., Bonifacino J. S. The T cell antigen receptor: insights into organelle biology. Annu Rev Cell Biol. 1990;6:403–431. doi: 10.1146/annurev.cb.06.110190.002155. [DOI] [PubMed] [Google Scholar]
  51. Koke J. A., Yang M., Henner D. J., Volwerk J. J., Griffith O. H. High-level expression in Escherichia coli and rapid purification of phosphatidylinositol-specific phospholipase C from Bacillus cereus and Bacillus thuringiensis. Protein Expr Purif. 1991 Feb;2(1):51–58. doi: 10.1016/1046-5928(91)90009-8. [DOI] [PubMed] [Google Scholar]
  52. Kosugi A., Weissman A. M., Ogata M., Hamaoka T., Fujiwara H. Instability of assembled T-cell receptor complex that is associated with rapid degradation of zeta chains in immature CD4+CD8+ thymocytes. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9494–9498. doi: 10.1073/pnas.89.20.9494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  54. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature. 1985 Apr 11;314(6011):537–539. doi: 10.1038/314537a0. [DOI] [PubMed] [Google Scholar]
  55. Lin J., Justement L. B. The MB-1/B29 heterodimer couples the B cell antigen receptor to multiple src family protein tyrosine kinases. J Immunol. 1992 Sep 1;149(5):1548–1555. [PubMed] [Google Scholar]
  56. Mason D. Y., van Noesel C. J., Cordell J. L., Comans-Bitter W. M., Micklem K., Tse A. G., van Lier R. A., van Dongen J. J. The B29 and mb-1 polypeptides are differentially expressed during human B cell differentiation. Eur J Immunol. 1992 Oct;22(10):2753–2756. doi: 10.1002/eji.1830221044. [DOI] [PubMed] [Google Scholar]
  57. Matsuuchi L., Gold M. R., Travis A., Grosschedl R., DeFranco A. L., Kelly R. B. The membrane IgM-associated proteins MB-1 and Ig-beta are sufficient to promote surface expression of a partially functional B-cell antigen receptor in a nonlymphoid cell line. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3404–3408. doi: 10.1073/pnas.89.8.3404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. McCarthy S. A., Kruisbeek A. M., Uppenkamp I. K., Sharrow S. O., Singer A. Engagement of the CD4 molecule influences cell surface expression of the T-cell receptor on thymocytes. Nature. 1988 Nov 3;336(6194):76–79. doi: 10.1038/336076a0. [DOI] [PubMed] [Google Scholar]
  59. McDonnell T. J., Deane N., Platt F. M., Nunez G., Jaeger U., McKearn J. P., Korsmeyer S. J. bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 1989 Apr 7;57(1):79–88. doi: 10.1016/0092-8674(89)90174-8. [DOI] [PubMed] [Google Scholar]
  60. Munro S., Pelham H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. doi: 10.1016/0092-8674(86)90746-4. [DOI] [PubMed] [Google Scholar]
  61. Nemazee D. A., Bürki K. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature. 1989 Feb 9;337(6207):562–566. doi: 10.1038/337562a0. [DOI] [PubMed] [Google Scholar]
  62. Nemazee D., Buerki K. Clonal deletion of autoreactive B lymphocytes in bone marrow chimeras. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8039–8043. doi: 10.1073/pnas.86.20.8039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Nguyen Q. V., Knapp W., Humphreys R. E. Inhibition by leupeptin and antipain of the intracellular proteolysis of Ii. Hum Immunol. 1989 Mar;24(3):153–163. doi: 10.1016/0198-8859(89)90056-6. [DOI] [PubMed] [Google Scholar]
  64. Okamoto M., Murakami M., Shimizu A., Ozaki S., Tsubata T., Kumagai S., Honjo T. A transgenic model of autoimmune hemolytic anemia. J Exp Med. 1992 Jan 1;175(1):71–79. doi: 10.1084/jem.175.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Parkhouse R. M. Three B-cell surface molecules associating with membrane immunoglobulin. Immunology. 1990 Feb;69(2):298–302. [PMC free article] [PubMed] [Google Scholar]
  66. Reth M. Antigen receptors on B lymphocytes. Annu Rev Immunol. 1992;10:97–121. doi: 10.1146/annurev.iy.10.040192.000525. [DOI] [PubMed] [Google Scholar]
  67. Sakaguchi N., Kashiwamura S., Kimoto M., Thalmann P., Melchers F. B lymphocyte lineage-restricted expression of mb-1, a gene with CD3-like structural properties. EMBO J. 1988 Nov;7(11):3457–3464. doi: 10.1002/j.1460-2075.1988.tb03220.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Schüppel R., Wilke J., Weiler E. Monoclonal anti-allotype antibody towards BALB/c IgM. Analysis of specificity and site of a V-C crossover in recombinant strain BALB-Igh-Va/Igh-Cb. Eur J Immunol. 1987 May;17(5):739–741. doi: 10.1002/eji.1830170527. [DOI] [PubMed] [Google Scholar]
  69. Sitia R., Neuberger M. S., Milstein C. Regulation of membrane IgM expression in secretory B cells: translational and post-translational events. EMBO J. 1987 Dec 20;6(13):3969–3977. doi: 10.1002/j.1460-2075.1987.tb02739.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Staddon J. M., Bouzyk M. M., Rozengurt E. Interconversion of GRP78/BiP. A novel event in the action of Pasteurella multocida toxin, bombesin, and platelet-derived growth factor. J Biol Chem. 1992 Dec 15;267(35):25239–25245. [PubMed] [Google Scholar]
  71. Stall A. M., Loken M. R. Allotypic specificities of murine IgD and IgM recognized by monoclonal antibodies. J Immunol. 1984 Feb;132(2):787–795. [PubMed] [Google Scholar]
  72. Strasser A., Whittingham S., Vaux D. L., Bath M. L., Adams J. M., Cory S., Harris A. W. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8661–8665. doi: 10.1073/pnas.88.19.8661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tarentino A. L., Plummer T. H., Jr, Maley F. The release of intact oligosaccharides from specific glycoproteins by endo-beta-N-acetylglucosaminidase H. J Biol Chem. 1974 Feb 10;249(3):818–824. [PubMed] [Google Scholar]
  74. Tokunaga K., Takeda K., Kamiyama K., Kageyama H., Takenaga K., Sakiyama S. Isolation of cDNA clones for mouse cytoskeletal gamma-actin and differential expression of cytoskeletal actin mRNAs in mouse cells. Mol Cell Biol. 1988 Sep;8(9):3929–3933. doi: 10.1128/mcb.8.9.3929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Tucker P. W., Liu C. P., Mushinski J. F., Blattner F. R. Mouse immunoglobulin D: messenger RNA and genomic DNA sequences. Science. 1980 Sep 19;209(4463):1353–1360. doi: 10.1126/science.6968091. [DOI] [PubMed] [Google Scholar]
  76. Van Noesel C. J., Brouns G. S., van Schijndel G. M., Bende R. J., Mason D. Y., Borst J., van Lier R. A. Comparison of human B cell antigen receptor complexes: membrane-expressed forms of immunoglobulin (Ig)M, IgD, and IgG are associated with structurally related heterodimers. J Exp Med. 1992 Jun 1;175(6):1511–1519. doi: 10.1084/jem.175.6.1511. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Venkitaraman A. R., Williams G. T., Dariavach P., Neuberger M. S. The B-cell antigen receptor of the five immunoglobulin classes. Nature. 1991 Aug 29;352(6338):777–781. doi: 10.1038/352777a0. [DOI] [PubMed] [Google Scholar]
  78. Wada I., Rindress D., Cameron P. H., Ou W. J., Doherty J. J., 2nd, Louvard D., Bell A. W., Dignard D., Thomas D. Y., Bergeron J. J. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem. 1991 Oct 15;266(29):19599–19610. [PubMed] [Google Scholar]
  79. Watts C., Davidson H. W. Endocytosis and recycling of specific antigen by human B cell lines. EMBO J. 1988 Jul;7(7):1937–1945. doi: 10.1002/j.1460-2075.1988.tb03031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Wienands J., Reth M. Glycosyl-phosphatidylinositol linkage as a mechanism for cell-surface expression of immunoglobulin D. Nature. 1992 Mar 19;356(6366):246–248. doi: 10.1038/356246a0. [DOI] [PubMed] [Google Scholar]
  81. Yamanashi Y., Kakiuchi T., Mizuguchi J., Yamamoto T., Toyoshima K. Association of B cell antigen receptor with protein tyrosine kinase Lyn. Science. 1991 Jan 11;251(4990):192–194. doi: 10.1126/science.1702903. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES