Abstract
The Ca2+-stimulated release of cortical vesicle (cortical granule) contents from the cell surface complex (CSC) of the sea urchin egg is an in vitro model for exocytosis. To gain insight into the molecular mechanism of exocytosis we investigated the sensitivity of this model to sulfhydryl modification and proteolytic digestion. Our findings include the following: (a) Proteolytic treatment with trypsin or pronase of CSC prepared from the eggs of Strongylocentrotus purpuratus increased the free Ca2+ concentration required to elicit exocytosis. Although a small increase in the Ca2+ threshold was detected after mild proteolysis, high concentrations of trypsin (0.5 mg/ml) and prolonged incubation (3 h) were required to render the CSC unresponsive to high concentrations of Ca2+ (0.5 mM). Despite the severity of the proteolytic digestions required to inactivate the CSC, the individual cortical vesicles remained intact, as gauged by the latency of ovoperoxidase, a cortical vesicle enzyme. (b) As previously shown (Haggerty, J. C., and R. C. Jackson, 1983, J. Biol. Chem. 258:1819-1825), cortical exocytosis can be blocked by sulfhydryl-modifying reagents such as N-ethylmaleimide (NEM). In this report we demonstrate that NEM inhibits by increasing the Ca2+ threshold required for exocytosis. When CSC that had been completely inactivated by NEM modification was briefly digested, on ice, with a low concentration of trypsin (or several other proteases), exocytotic activity was restored. Although the Ca2+ threshold of the reactivated CSC was slightly higher than that of untreated CSC, it was nearly identical to that of control CSC, which was trypsinized but not treated with NEM. We discuss the significance of these results with regard to the molecular mechanism of exocytosis.
MeSH Terms
Animals
Calcium/pharmacology
Cytoplasmic Granules/physiology
Dose-Response Relationship, Drug
Ethylmaleimide/pharmacology
Exocytosis/drug effects
Female
Membrane Proteins/physiology
Ovum/drug effects,ultrastructure
Sea Urchins
Trypsin/pharmacology
Chemicals
Membrane Proteins
Trypsin
Ethylmaleimide
Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Jackson R C
Ward K K
Haggerty J G
References (19)
19 references, click to expand
-
Peroxidatic activity of catalase in the cortical granules of sea urchin eggs.
Dev Biol. 1974 Oct;40(2):292-7
PMID: 4473390
-
Reversible and irreversible activation of cyclic nucleotide phosphodiesterase: separation of the regulatory and catalytic domains by limited proteolysis.
Adv Cyclic Nucleotide Protein Phosphorylation Res. 1984;16:31-47
PMID: 6326530
-
Isolation and characterization of plasma membrane-associated cortical granules from sea urchin eggs.
J Cell Biol. 1977 Dec;75(3):899-914
PMID: 562888
-
Conversion of calcium-sensitive myosin light chain kinase to a calcium-insensitive form.
FEBS Lett. 1978 Apr 15;88(2):242-6
PMID: 648635
-
Refinement of the coomassie blue method of protein quantitation. A simple and linear spectrophotometric assay for less than or equal to 0.5 to 50 microgram of protein.
Anal Biochem. 1978 May;86(1):142-6
PMID: 655375
-
Influence of ATP and calcium on the cortical reaction in sea urchin eggs.
Nature. 1978 Nov 30;276(5687):513-5
PMID: 364317
-
Metabolic similarities between fertilization and phagocytosis. Conservation of a peroxidatic mechanism.
J Exp Med. 1979 Apr 1;149(4):938-53
PMID: 372484
-
Sperm binding and fertilization envelope formation in a cell surface complex isolated from sea urchin eggs.
J Cell Biol. 1979 Apr;81(1):92-103
PMID: 479292
-
Inhibitory action of chlorpromazine, dibucaine, and other phospholipid-interacting drugs on calcium-activated, phospholipid-dependent protein kinase.
J Biol Chem. 1980 Sep 25;255(18):8378-80
PMID: 7410368
-
Regulatory light-chains and scallop myosin. Full dissociation, reversibility and co-operative effects.
J Mol Biol. 1980 Apr 15;138(3):473-92
PMID: 6251228
-
Calmodulin confers calcium sensitivity on secretory exocytosis.
Nature. 1982 Jan 14;295(5845):154-5
PMID: 7035964
-
L-trans-Epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L.
Biochem J. 1982 Jan 1;201(1):189-98
PMID: 7044372
-
Calcium-dependence of catecholamine release from bovine adrenal medullary cells after exposure to intense electric fields.
J Membr Biol. 1982;68(2):107-40
PMID: 6809949
-
Release of granule contents from sea urchin egg cortices. New assay procedures and inhibition by sulfhydryl-modifying reagents.
J Biol Chem. 1983 Feb 10;258(3):1819-25
PMID: 6822535
-
Calcium-evoked secretion from digitonin-permeabilized adrenal medullary chromaffin cells.
J Biol Chem. 1983 Apr 25;258(8):4994-5000
PMID: 6300108
-
Cortical vesicle exocytosis in isolated cortices of sea urchin eggs: description of a turbidometric assay and its utilization in studying effects of different media on discharge.
Dev Biol. 1983 Aug;98(2):327-37
PMID: 6683684
-
Activation of calcineurin by limited proteolysis.
Proc Natl Acad Sci U S A. 1983 Jul;80(14):4291-5
PMID: 6576338
-
Calcium-mediated release of glucanase activity from cortical granules of sea urchin eggs.
Dev Biol. 1983 Dec;100(2):267-74
PMID: 6686171
-
The isolation of intact cortical granules from sea urchin eggs: calcium lons trigger granule discharge.
Dev Biol. 1975 Mar;43(1):62-74
PMID: 1171035