Abstract
At the entry into mitosis, cells abruptly lose membrane activities such as phagocytosis, pinocytosis, and capping. The present studies test if mitotic cells also resist functional responses to cell surface ligand- receptor interactions. The IgE receptors of RBL-2H3 rat basophilic leukemia cells were labeled with anti-dinitrophenol IgE (anti-DNP-IgE) and then cross-linked with multivalent ligands (DNP-bovine serum albumin [BSA]; DNP-B-phycoerythrin; DNP-BSA-gold). IgE-receptor cross- linking modulates cell surface organization and function and releases serotonin and other mediators of allergic and asthmatic reactions from interphase cells (Pfeiffer, J. R., JC. Seagrave, B. H. Davis, G. G. Deanin, and J. M. Oliver, 1985, J. Cell Biol., 101:2145-2155). It was found that anti-DNP-IgE-receptor complexes are preserved on the cell surface throughout mitosis; they continue to bind DNP-proteins, and the resulting antigen-IgE-receptor complexes can redistribute to coated pits on the cell surface. Furthermore, there is no loss of [3H]serotonin through mitosis. Nevertheless, antigen-stimulated [3H]- serotonin release is strongly impaired in mitotic-enriched as compared with mixed interphase or G1-enriched cell populations. In addition, antigen binding transforms the surface of interphase cells from a microvillous to a plicated topography and stimulates the uptake of fluorescein isothiocyanate-conjugated dextran by fluid pinocytosis. Mitotic cells maintain a microvillous surface topography after antigen treatment, and fluid pinocytosis virtually ceases from prometaphase to telophase. Phorbol myristate acetate, a tumor promoter that activates protein kinase C, restores surface ruffling activity to mitotic cells. Thus, the mitosis-specific freezing of membrane and secretory responses is most likely due to the failure of transmembrane signaling.
Full Text
The Full Text of this article is available as a PDF (1.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- 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]
- Beaven M. A., Rogers J., Moore J. P., Hesketh T. R., Smith G. A., Metcalfe J. C. The mechanism of the calcium signal and correlation with histamine release in 2H3 cells. J Biol Chem. 1984 Jun 10;259(11):7129–7136. [PubMed] [Google Scholar]
- Becker E. L. The relationship of the chemotactic behavior of the complement-derived factors, C3a, C5a, and C567, and a bacterial chemotactic factor to their ability to activate the proesterase 1 of rabbit polymorphonuclear leukocytes. J Exp Med. 1972 Feb 1;135(2):376–387. doi: 10.1084/jem.135.2.376. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berlin R. D., Oliver J. M. Surface functions during mitosis. II. Quantitation of pinocytosis and kinetic characterization of the mitotic cycle with a new fluorescence technique. J Cell Biol. 1980 Jun;85(3):660–671. doi: 10.1083/jcb.85.3.660. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berlin R. D., Oliver J. M., Walter R. J. Surface functions during Mitosis I: phagocytosis, pinocytosis and mobility of surface-bound Con A. Cell. 1978 Oct;15(2):327–341. doi: 10.1016/0092-8674(78)90002-8. [DOI] [PubMed] [Google Scholar]
- Buell D. N., Fowlkes B. J., Metzher H., Isersky C. Cell cycle and morphological changes during growth and differentiation of a rat basophilic leukemia cell line. Cancer Res. 1976 Sep;36(9 PT1):3131–3137. [PubMed] [Google Scholar]
- Carson D. A., Metzger H. Interaction of IgE with rat basophilic leukemia cells. IV. Antibody-induced redistribution of IgE receptors. J Immunol. 1974 Oct;113(4):1271–1277. [PubMed] [Google Scholar]
- Furuichi K., Rivera J., Isersky C. The fate of IgE bound to rat basophilic leukemia cells. III. Relationship between antigen-induced endocytosis and serotonin release. J Immunol. 1984 Sep;133(3):1513–1520. [PubMed] [Google Scholar]
- Gillespie E., Lichtenstein L. M. Histamine release from human leukocytes: studies with deuterium oxide, colchicine, and cytochalasin B. J Clin Invest. 1972 Nov;51(11):2941–2947. doi: 10.1172/JCI107118. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hesketh T. R., Beaven M. A., Rogers J., Burke B., Warren G. B. Stimulated release of histamine by a rat mast cell line is inhibited during mitosis. J Cell Biol. 1984 Jun;98(6):2250–2254. doi: 10.1083/jcb.98.6.2250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Howard R. F., Sheppard J. R. Cell cycle changes in the adenylate cyclase of C6 glioma cells. J Cell Biol. 1981 Jul;90(1):169–175. doi: 10.1083/jcb.90.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isersky C., Metzger H., Buell D. N. Cell cycle-associated changes in receptors for IgE during growth and differentiation of a rat basophilic leukemia cell line. J Exp Med. 1975 May 1;141(5):1147–1162. doi: 10.1084/jem.141.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Isersky C., Rivera J., Segal D. M., Triche T. The fate of IgE bound to rat basophilic leukemia cells. II. Endocytosis of IgE oligomers and effect on receptor turnover. J Immunol. 1983 Jul;131(1):388–396. [PubMed] [Google Scholar]
- 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]
- Menon A. K., Holowka D., Baird B. Small oligomers of immunoglobulin E (IgE) cause large-scale clustering of IgE receptors on the surface of rat basophilic leukemia cells. J Cell Biol. 1984 Feb;98(2):577–583. doi: 10.1083/jcb.98.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meyer C., Wahl L. M., Stadler B. M., Siraganian R. P. Cell cycle associated changes in histamine release from rat basophilic leukemia cells separated by counterflow centrifugal elutriation. J Immunol. 1983 Aug;131(2):911–914. [PubMed] [Google Scholar]
- Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984 Apr 19;308(5961):693–698. doi: 10.1038/308693a0. [DOI] [PubMed] [Google Scholar]
- Oliver J. M., Berlin R. D. Mechanisms that regulate the structural and functional architecture of cell surfaces. Int Rev Cytol. 1982;74:55–94. doi: 10.1016/s0074-7696(08)61169-9. [DOI] [PubMed] [Google Scholar]
- Pfeiffer J. R., Seagrave J. C., Davis B. H., Deanin G. G., Oliver J. M. Membrane and cytoskeletal changes associated with IgE-mediated serotonin release from rat basophilic leukemia cells. J Cell Biol. 1985 Dec;101(6):2145–2155. doi: 10.1083/jcb.101.6.2145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Radley J. M., Hodgson G. S. Effect of isoprenaline on cells in different phases of the mitotic cycle. Exp Cell Res. 1971 Nov;69(1):148–160. doi: 10.1016/0014-4827(71)90320-x. [DOI] [PubMed] [Google Scholar]
- Sager P. R., Brown P. A., Berlin R. D. Analysis of transferrin recycling in mitotic and interphase HeLa cells by quantitative fluorescence microscopy. Cell. 1984 Dec;39(2 Pt 1):275–282. doi: 10.1016/0092-8674(84)90005-9. [DOI] [PubMed] [Google Scholar]
- Tobey R. A., Anderson E. C., Petersen D. F. Properties of mitotic cells prepared by mechanically shaking monolayer cultures of Chinese hamster cells. J Cell Physiol. 1967 Aug;70(1):63–68. doi: 10.1002/jcp.1040700109. [DOI] [PubMed] [Google Scholar]
- Warren G., Featherstone C., Griffiths G., Burke B. Newly synthesized G protein of vesicular stomatitis virus is not transported to the cell surface during mitosis. J Cell Biol. 1983 Nov;97(5 Pt 1):1623–1628. doi: 10.1083/jcb.97.5.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zeligs J. D., Wollman S. H. Mitosis in rat thyroid epithelial cells in vivo. I. Ultrastructural changes in cytoplasmic organelles during the mitotic cycle. J Ultrastruct Res. 1979 Jan;66(1):53–77. doi: 10.1016/s0022-5320(79)80065-9. [DOI] [PubMed] [Google Scholar]