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. 1991 Mar;2(3):181–191. doi: 10.1091/mbc.2.3.181

Association of the crosslinked IgE receptor with the membrane skeleton is independent of the known signaling mechanisms in rat basophilic leukemia cells.

J R Apgar 1
PMCID: PMC361749  PMID: 1830493

Abstract

Crosslinking of the IgE receptor on the surface of rat basophilic leukemia (RBL) cells by multivalent antigen induces an association of these receptors with the detergent-insoluble membrane skeleton. Detergent insolubility of the receptor can also be induced on purified plasma membranes isolated from RBL cells by the use of either IgE oligomers or IgE monomers plus multivalent antigen. The critical event in initiating this interaction between the receptor and the membrane skeleton is cross-linking of the receptor. This association is rapid, and, when triggered by multivalent antigen, it is quickly reversed by the addition of excess monovalent antigen. The fact that this association occurs with the use of purified plasma membranes indicates that all of the components necessary for this interaction are present in the plasma membrane and that intracellular components are not required. Although crosslinking of the receptor activates phospholipase C and phospholipase A2 leading to the generation of several second messengers, none of these signaling mechanisms appears to be involved in IgE receptor interaction with the membrane skeleton. This interaction cannot be induced by phorbol 12-myristate 13-acetate (PMA), ionomycin, or a combination of these two reagents, although this will result in degranulation. Furthermore, receptor detergent insolubility is temperature independent when triggered by multivalent antigen, thus indicating that enzyme-catalyzed reactions are not important. This was verified by the fact that a variety of inhibitors that block phosphatidylinositol metabolism, arachidonic acid metabolism, Ca2+ influx, and protein kinase C (PKC) activation had no effect on antigen-induced association of the receptor with the membrane skeleton. These results indicate that the signaling mechanisms leading to the degranulation response are not involved in the association of the crosslinked receptor with the membrane skeleton.

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Selected References

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

  1. Ali H., Collado-Escobar D. M., Beaven M. A. The rise in concentration of free Ca2+ and of pH provides sequential, synergistic signals for secretion in antigen-stimulated rat basophilic leukemia (RBL-2H3) cells. J Immunol. 1989 Oct 15;143(8):2626–2633. [PubMed] [Google Scholar]
  2. Apgar J. R. Antigen-induced cross-linking of the IgE receptor leads to an association with the detergent-insoluble membrane skeleton of rat basophilic leukemia (RBL-2H3) cells. J Immunol. 1990 Dec 1;145(11):3814–3822. [PubMed] [Google Scholar]
  3. Apgar J. R., Herrmann S. H., Robinson J. M., Mescher M. F. Triton X-100 extraction of P815 tumor cells: evidence for a plasma membrane skeleton structure. J Cell Biol. 1985 May;100(5):1369–1378. doi: 10.1083/jcb.100.5.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Apgar J. R., Mescher M. F. Agorins: major structural proteins of the plasma membrane skeleton of P815 tumor cells. J Cell Biol. 1986 Aug;103(2):351–360. doi: 10.1083/jcb.103.2.351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beaven M. A., Moore J. P., Smith G. A., Hesketh T. R., Metcalfe J. C. The calcium signal and phosphatidylinositol breakdown in 2H3 cells. J Biol Chem. 1984 Jun 10;259(11):7137–7142. [PubMed] [Google Scholar]
  6. Berridge M. J., Downes C. P., Hanley M. R. Lithium amplifies agonist-dependent phosphatidylinositol responses in brain and salivary glands. Biochem J. 1982 Sep 15;206(3):587–595. doi: 10.1042/bj2060587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Braun J., Hochman P. S., Unanue E. R. Ligand-induced association of surface immunoglobulin with the detergent-insoluble cytoskeletal matrix of the B lymphocyte. J Immunol. 1982 Mar;128(3):1198–1204. [PubMed] [Google Scholar]
  8. Crews F. T., Morita Y., McGivney A., Hirata F., Siraganian R. P., Axelrod J. IgE-mediated histamine release in rat basophilic leukemia cells: receptor activation, phospholipid methylation, Ca2+ flux, and release of arachidonic acid. Arch Biochem Biophys. 1981 Dec;212(2):561–571. doi: 10.1016/0003-9861(81)90399-4. [DOI] [PubMed] [Google Scholar]
  9. Cunha-Melo J. R., Dean N. M., Moyer J. D., Maeyama K., Beaven M. A. The kinetics of phosphoinositide hydrolysis in rat basophilic leukemia (RBL-2H3) cells varies with the type of IgE receptor cross-linking agent used. J Biol Chem. 1987 Aug 25;262(24):11455–11463. [PubMed] [Google Scholar]
  10. Cunha-Melo J. R., Gonzaga H. M., Ali H., Huang F. L., Huang K. P., Beaven M. A. Studies of protein kinase C in the rat basophilic leukemia (RBL-2H3) cell reveal that antigen-induced signals are not mimicked by the actions of phorbol myristate acetate and Ca2+ ionophore. J Immunol. 1989 Oct 15;143(8):2617–2625. [PubMed] [Google Scholar]
  11. Fewtrell C., Metzger H. Larger oligomers of IgE are more effective than dimers in stimulating rat basophilic leukemia cells. J Immunol. 1980 Aug;125(2):701–710. [PubMed] [Google Scholar]
  12. Fewtrell C., Sherman E. IgE receptor-activated calcium permeability pathway in rat basophilic leukemia cells: measurement of the unidirectional influx of calcium using quin2-buffered cells. Biochemistry. 1987 Nov 3;26(22):6995–7003. doi: 10.1021/bi00396a021. [DOI] [PubMed] [Google Scholar]
  13. Galvin N. J., Stockhausen D., Meyers-Hutchins B. L., Frazier W. A. Association of the cyclic AMP chemotaxis receptor with the detergent-insoluble cytoskeleton of Dictyostelium discoideum. J Cell Biol. 1984 Feb;98(2):584–595. doi: 10.1083/jcb.98.2.584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ishizaka T., Ishizaka K. Activation of mast cells for mediator release through IgE receptors. Prog Allergy. 1984;34:188–235. [PubMed] [Google Scholar]
  15. Jack R. M., Ezzell R. M., Hartwig J., Fearon D. T. Differential interaction of the C3b/C4b receptor and MHC class I with the cytoskeleton of human neutrophils. J Immunol. 1986 Dec 15;137(12):3996–4003. [PubMed] [Google Scholar]
  16. Jesaitis A. J., Naemura J. R., Sklar L. A., Cochrane C. G., Painter R. G. Rapid modulation of N-formyl chemotactic peptide receptors on the surface of human granulocytes: formation of high-affinity ligand-receptor complexes in transient association with cytoskeleton. J Cell Biol. 1984 Apr;98(4):1378–1387. doi: 10.1083/jcb.98.4.1378. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jung G., Helm R. M., Carraway C. A., Carraway K. L. Mechanism of concanavalin A-induced anchorage of the major cell surface glycoproteins to the submembrane cytoskeleton in 13762 ascites mammary adenocarcinoma cells. J Cell Biol. 1984 Jan;98(1):179–187. doi: 10.1083/jcb.98.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kane P. M., Holowka D., Baird B. Cross-linking of IgE-receptor complexes by rigid bivalent antigens greater than 200 A in length triggers cellular degranulation. J Cell Biol. 1988 Sep;107(3):969–980. doi: 10.1083/jcb.107.3.969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kane P., Erickson J., Fewtrell C., Baird B., Holowka D. Cross-linking of IgE-receptor complexes at the cell surface: synthesis and characterization of a long bivalent hapten that is capable of triggering mast cells and rat basophilic leukemia cells. Mol Immunol. 1986 Jul;23(7):783–790. doi: 10.1016/0161-5890(86)90090-8. [DOI] [PubMed] [Google Scholar]
  20. Kanner B. I., Metzger H. Crosslinking of the receptors for immunoglobulin E depolarizes the plasma membrane of rat basophilic leukemia cells. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5744–5748. doi: 10.1073/pnas.80.18.5744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Landreth G. E., Williams L. K., Rieser G. D. Association of the epidermal growth factor receptor kinase with the detergent-insoluble cytoskeleton of A431 cells. J Cell Biol. 1985 Oct;101(4):1341–1350. doi: 10.1083/jcb.101.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Liu F. T., Bohn J. W., Ferry E. L., Yamamoto H., Molinaro C. A., Sherman L. A., Klinman N. R., Katz D. H. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980 Jun;124(6):2728–2737. [PubMed] [Google Scholar]
  23. Maeyama K., Hohman R. J., Ali H., Cunha-Melo J. R., Beaven M. A. Assessment of IgE-receptor function through measurement of hydrolysis of membrane inositol phospholipids. New insights on the phenomena of biphasic antigen concentration-response curves and desensitization. J Immunol. 1988 Jun 1;140(11):3919–3927. [PubMed] [Google Scholar]
  24. Marano N., Holowka D., Baird B. Bivalent binding of an anti-CD3 antibody to Jurkat cells induces association of the T cell receptor complex with the cytoskeleton. J Immunol. 1989 Aug 1;143(3):931–938. [PubMed] [Google Scholar]
  25. Mescher M. F., Jose M. J., Balk S. P. Actin-containing matrix associated with the plasma membrane of murine tumour and lymphoid cells. Nature. 1981 Jan 15;289(5794):139–144. doi: 10.1038/289139a0. [DOI] [PubMed] [Google Scholar]
  26. Metzger H., Alcaraz G., Hohman R., Kinet J. P., Pribluda V., Quarto R. The receptor with high affinity for immunoglobulin E. Annu Rev Immunol. 1986;4:419–470. doi: 10.1146/annurev.iy.04.040186.002223. [DOI] [PubMed] [Google Scholar]
  27. Metzger H. The receptor on mast cells and related cells with high affinity for IgE. Contemp Top Mol Immunol. 1983;9:115–145. doi: 10.1007/978-1-4684-4517-6_4. [DOI] [PubMed] [Google Scholar]
  28. Mohr F. C., Fewtrell C. The relative contributions of extracellular and intracellular calcium to secretion from tumor mast cells. Multiple effects of the proton ionophore carbonyl cyanide m-chlorophenylhydrazone. J Biol Chem. 1987 Aug 5;262(22):10638–10643. [PubMed] [Google Scholar]
  29. Narasimhan V., Holowka D., Baird B. A guanine nucleotide-binding protein participates in IgE receptor-mediated activation of endogenous and reconstituted phospholipase A2 in a permeabilized cell system. J Biol Chem. 1990 Jan 25;265(3):1459–1464. [PubMed] [Google Scholar]
  30. Narasimhan V., Holowka D., Fewtrell C., Baird B. Cholera toxin increases the rate of antigen-stimulated calcium influx in rat basophilic leukemia cells. J Biol Chem. 1988 Dec 25;263(36):19626–19632. [PubMed] [Google Scholar]
  31. Oliver J. M., Seagrave J., Stump R. F., Pfeiffer J. R., Deanin G. G. Signal transduction and cellular response in RBL-2H3 mast cells. Prog Allergy. 1988;42:185–245. [PubMed] [Google Scholar]
  32. Ranscht B., Moss D. J., Thomas C. A neuronal surface glycoprotein associated with the cytoskeleton. J Cell Biol. 1984 Nov;99(5):1803–1813. doi: 10.1083/jcb.99.5.1803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Robertson D., Holowka D., Baird B. Cross-linking of immunoglobulin E-receptor complexes induces their interaction with the cytoskeleton of rat basophilic leukemia cells. J Immunol. 1986 Jun 15;136(12):4565–4572. [PubMed] [Google Scholar]
  34. Sagi-Eisenberg R., Pecht I. Membrane potential changes during IgE-mediated histamine release from rat basophilic leukemia cells. J Membr Biol. 1983;75(2):97–104. doi: 10.1007/BF01995629. [DOI] [PubMed] [Google Scholar]
  35. Seagrave J., Oliver J. M. Antigen-dependent transition of IgE to a detergent-insoluble form is associated with reduced IgE receptor-dependent secretion from RBL-2H3 mast cells. J Cell Physiol. 1990 Jul;144(1):128–136. doi: 10.1002/jcp.1041440117. [DOI] [PubMed] [Google Scholar]
  36. Stump R. F., Oliver J. M., Cragoe E. J., Jr, Deanin G. G. The control of mediator release from RBL-2H3 cells: roles for Ca2+, Na+, and protein kinase C1. J Immunol. 1987 Aug 1;139(3):881–886. [PubMed] [Google Scholar]
  37. Suchard S. J., Boxer L. A. Characterization and cytoskeletal association of a major cell surface glycoprotein, GP 140, in human neutrophils. J Clin Invest. 1989 Aug;84(2):484–492. doi: 10.1172/JCI114190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vale R. D., Shooter E. M. Alteration of binding properties and cytoskeletal attachment of nerve growth factor receptors in PC12 cells by wheat germ agglutinin. J Cell Biol. 1982 Sep;94(3):710–717. doi: 10.1083/jcb.94.3.710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vale R. D., Shooter E. M. Conversion of nerve growth factor-receptor complexes to a slowly dissociating, Triton X-100 insoluble state by anti nerve growth factor antibodies. Biochemistry. 1983 Oct 11;22(21):5022–5028. doi: 10.1021/bi00290a022. [DOI] [PubMed] [Google Scholar]
  40. Wheeler M. E., Gerrard J. M., Carroll R. C. Reciprocal transmembranous receptor-cytoskeleton interactions in concanavalin A-activated platelets. J Cell Biol. 1985 Sep;101(3):993–1000. doi: 10.1083/jcb.101.3.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wilson B. S., Deanin G. G., Standefer J. C., Vanderjagt D., Oliver J. M. Depletion of guanine nucleotides with mycophenolic acid suppresses IgE receptor-mediated degranulation in rat basophilic leukemia cells. J Immunol. 1989 Jul 1;143(1):259–265. [PubMed] [Google Scholar]
  42. Woda B. A., McFadden M. L. Ligand-induced association of rat lymphocyte membrane proteins with the detergent-insoluble lymphocyte cytoskeletal matrix. J Immunol. 1983 Oct;131(4):1917–1919. [PubMed] [Google Scholar]
  43. Woda B. A., Woodin M. B. The interaction of lymphocyte membrane proteins with the lymphocyte cytoskeletal matrix. J Immunol. 1984 Nov;133(5):2767–2772. [PubMed] [Google Scholar]

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