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PMID: 2324701 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Compound versus multigranular exocytosis in peritoneal mast cells.

The Journal of general physiology ·Vol. 95 ·No. 3 ·1990-03-00 ·Pages 397-409

Alvarez de Toledo G, Fernandez JM

Abstract

We have used the whole-cell patch-pipette technique to measure the step increases in the cell membrane capacitance (equivalent to the membrane area) caused by the fusion of secretory granules in degranulating murine mast cells. We have observed that up to 30% of the total membrane expansion caused by degranulation results from large fusion events that cannot be explained by the fusion of single secretory granules. These large events are observed mainly in the initial phase of a degranulation. We have developed a simple mathematical model for a mast cell to test whether these large events are caused by a stimulus-induced, granule-to-granule fusion that occurs before their exocytosis (multigranular exocytosis). Our results suggest that the large fusion events are caused by the exocytosis of granule aggregates that existed before stimulation and that are located at the cell's periphery. We propose a novel mechanism by which granule aggregates can be formed at the periphery of the cell. This mechanism relies on the ability of a transiently fused granule ("flicker") to fuse with more internally located granules in a sequential manner. This pattern may result in the formation of larger peripheral granules that later on can fuse with the membrane. The formation of peripheral granule aggregates may potentiate a subsequent secretory response.

MeSH Terms
Animals Biomechanical Phenomena Computer Simulation Electric Conductivity Exocytosis/physiology Mast Cells/physiology Peritoneal Cavity/cytology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Alvarez de Toledo G
Department of Physiology, School of Medicine, University of Pennsylvania, Philadelphia 19104-6085.
Fernandez J M
References (19)
19 references, click to expand
  1. Studies on morphological changes and histamine release induced by bee venom, n-decylamine and hypotonic solutions in rat peritoneal mast cells.
    Acta Physiol Scand. 1967 Dec;71(4):257-69 PMID: 4172483
  2. The events leading to secretory granule fusion.
    Soc Gen Physiol Ser. 1988;43:333-44 PMID: 3269026
  3. Sequential exocytosis of storage granules during antigen-induced histamine release from sensitized rat mast cells in vitro. An electron microscopic study.
    Acta Physiol Scand. 1973 Jul;88(3):359-72 PMID: 4127384
  4. Quantitative analysis of mast cell structure.
    J Microsc. 1974 Apr;100(3):315-21 PMID: 4406770
  5. Anaphylactic degranulation of guinea pig basophilic leukocytes. I. Fusion of granule membranes and cytoplasmic vesicles formation and resolution of degranulation sacs.
    Lab Invest. 1981 Feb;44(2):174-91 PMID: 6162057
  6. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells.
    Proc Natl Acad Sci U S A. 1982 Nov;79(21):6712-6 PMID: 6959149
  7. Freeze-fracture studies of chemotactic peptide-induced exocytosis in neutrophils: evidence for two patterns of secretory granule fusion.
    J Ultrastruct Res. 1983 Feb;82(2):221-32 PMID: 6827649
  8. Periodic, multimodal distribution of granule volumes in mast cells.
    Cell Tissue Res. 1983;228(1):51-9 PMID: 6831525
  9. Capacitance measurements reveal stepwise fusion events in degranulating mast cells.
    Nature. 1984 Nov 29-Dec 5;312(5993):453-5 PMID: 6504157
  10. Differences in the volume distributions of human lung mast cell granules and lipid bodies: evidence that the size of these organelles is regulated by distinct mechanisms.
    J Cell Biol. 1985 May;100(5):1488-92 PMID: 3988795
  11. Ultrastructural characterization and morphometric analysis of human eosinophil degranulation.
    J Cell Sci. 1985 Feb;73:33-48 PMID: 2991305
  12. Multigranular exocytosis induced by phospholipase A2-activators, melittin and mastoparan, in rat anterior pituitary cells.
    Cell Tissue Res. 1986;243(2):311-6 PMID: 3948236
  13. Chemotactic peptide-induced exocytosis in neutrophils: granule fusion patterns depend on the source of messenger calcium.
    J Cell Sci. 1986 Jul;83:293-311 PMID: 3100542
  14. Simultaneous electrical and optical measurements show that membrane fusion precedes secretory granule swelling during exocytosis of beige mouse mast cells.
    Proc Natl Acad Sci U S A. 1987 Mar;84(6):1585-9 PMID: 3470745
  15. Final steps in exocytosis observed in a cell with giant secretory granules.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1945-9 PMID: 3470768
  16. The exocytosis of human blood platelets. A fast freezing and freeze-substitution analysis.
    Eur J Cell Biol. 1987 Apr;43(2):273-82 PMID: 3595636
  17. Currents through the fusion pore that forms during exocytosis of a secretory vesicle.
    Nature. 1987 Aug 27-Sep 2;328(6133):814-7 PMID: 2442614
  18. Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis.
    Biophys J. 1988 Jun;53(6):885-92 PMID: 3395658
  19. Electron microscope observations on compounds 48-80-induced degranulation in rat mast cells. Evidence for sequential exocytosis of storage granules.
    J Cell Biol. 1971 Nov;51(21):465-83 PMID: 4107023
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1990-03-00
Pages
397-409
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2216328
Subset
IM
Grants
NIGMS NIH HHS · GM-38857 · United States
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