Abstract
1. We have measured the breakdown of [3H]phosphatidylinositol in rabbit neutrophils prelabelled with [3H]glycerol by a pulse-chase procedure. With a view to defining a possible causal relationship between phosphatidylinositol breakdown and enzyme secretion in these cells, we have compared the characteristics of both these processes induced by either the receptor-directed agonist formylmethionyl-leucylphenylalanine (fMet-Leu-Phe) or the Ca2+-ionophore ionomycin. 2. The dependence on fMet-Leu-Phe concentration of phosphatidylinositol breakdown and secretion is identical (half-maximal at 0.3 nM). This is 30-fold less than that required for half-maximal occupation of receptors. 3. Both secretion and breakdown of phosphatidylinositol due to fMet-Leu-Phe are modulated by extracellular Ca2+. The sensitivity to Ca2+ of both processes is enhanced by pretreatment to deplete cell Ca2+. The concentration of Ca2+ required to cause half-maximal effects of both processes in Ca2+-depleted cells on stimulation with 1nM-fMet-Leu-Phe is 100 microM. Ionomycin-stimulated secretion and breakdown of phosphatidylinositol are completely dependent on extracellular Ca2+ over similar concentration ranges. 4. Both secretion and phosphatidylinositol breakdown due to fMet-Leu-Phe approach completion by 10s. With ionomycin these processes are slower, terminating by 2 min. 5. In the presence of [32P]Pi, labelling of [32P]phosphatidic acid reaches a maximum 15 min after stimulation with either fMet-Leu-Phe or ionomycin. This precedes the labelling of [32P]phosphatidylinositol and shows the expected precursor-product relationship. 6. We conclude from these results that in rabbit neutrophils a rise in cytosol [Ca2+] is both sufficient and necessary to cause secretion and phosphatidylinositol breakdown. In cells depleted of Ca2+, the occupation of receptors by fMet-Leu-Phe is without effect on these two processes.
MeSH Terms
Animals
Calcium/pharmacology
Chemotactic Factors/pharmacology
Ethers/pharmacology
In Vitro Techniques
Ionomycin
Ionophores/pharmacology
Methionine/analogs & derivatives
N-Formylmethionine/analogs & derivatives,pharmacology
N-Formylmethionine Leucyl-Phenylalanine
Neutrophils/drug effects,enzymology,metabolism
Oligopeptides/pharmacology
Phosphatidylinositols/metabolism
Rabbits
Time Factors
Chemicals
Chemotactic Factors
Ethers
Ionophores
Oligopeptides
Phosphatidylinositols
N-Formylmethionine
Ionomycin
N-Formylmethionine Leucyl-Phenylalanine
Methionine
Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Cockcroft S
Bennett J P
Gomperts B D
References (21)
21 references, click to expand
-
The possible involvement of phosphatidylinositol breakdown in the mechanism of stimulus-response coupling at receptors which control cell-surface calcium gates.
Adv Exp Med Biol. 1977;83:447-64
PMID: 335830
-
A comparison of the effects of phytohaemagglutinin and of calcium ionophore A23187 on the metabolism of glycerolipids in small lymphocytes.
Biochem J. 1977 May 15;164(2):389-97
PMID: 328012
-
Evidence for a role of phosphatidylinositol turnover in stimulus-secretion coupling. Studies with rat peritoneal mast cells.
Biochem J. 1979 Mar 15;178(3):681-7
PMID: 88219
-
Receptor-mediated internalization of fluorescent chemotactic peptide by human neutrophils.
Science. 1979 Sep 28;205(4413):1412-4
PMID: 472759
-
Ionomycin stimulates mast cell histamine secretion by forming a lipid-soluble calcium complex.
Nature. 1979 Dec 20-27;282(5741):851-3
PMID: 92764
-
f-MetLeuPhe-induced phosphatidylinositol turnover in rabbit neutrophils is dependent on extracellular calcium.
FEBS Lett. 1980 Jan 28;110(1):115-8
PMID: 7353657
-
Proposed mechanism of cholinergic action in smooth muscle.
Nature. 1980 Mar 27;284(5754):344-5
PMID: 6767193
-
Is phosphatidic acid a calcium ionophore under neurohumoral control?
Nature. 1980 Mar 27;284(5754):345-7
PMID: 6244502
-
Stimulus-secretion coupling in rabbit neutrophils is not mediated by phosphatidylinositol breakdown.
Nature. 1980 Nov 20;288(5788):275-7
PMID: 7432525
-
The accumulation of calcium by the polymorphonuclear leucocyte treated with staphylococcal leucocidin and its significance in the extrusion of protein.
Biochem J. 1963 Jun;87:487-95
PMID: 14001785
-
Quantitative analysis of phospholipids by thin-layer chromatography.
Biochem J. 1964 Feb;90(2):374-8
PMID: 4284220
-
Mechanisms of lysosomal enzyme release from human leukocytes: microtubule assembly and membrane fusion induced by a component of complement.
Proc Natl Acad Sci U S A. 1973 Oct;70(10):2916-20
PMID: 4355374
-
The ability of chemotactic factors to induce lysosomal enzyme release. II. The mechanism of release.
J Immunol. 1974 Jun;112(6):2055-62
PMID: 4825785
-
The bacterial factors which stimulate neutrophils may be derived from procaryote signal peptides.
FEBS Lett. 1980 Jul 11;116(1):57-61
PMID: 6967828
-
Inositol phospholipids and cell surface receptor function.
Biochim Biophys Acta. 1975 Mar 25;415(1):81-47
PMID: 164246
-
Bioregulation of lysosomal enzyme secretion from human neutrophils: roles of guanosine 3':5'-monophosphate and calcium in stimulus-secretion coupling.
Proc Natl Acad Sci U S A. 1975 Jan;72(1):108-12
PMID: 164009
-
Use of cytochalasin B to distinguish between early and late events in neutrophil activation.
Biochim Biophys Acta. 1980 Oct 2;601(3):584-91
PMID: 6251879
-
The structure-activity relations of synthetic peptides as chemotactic factors and inducers of lysosomal secretion for neutrophils.
J Exp Med. 1976 May 1;143(5):1154-69
PMID: 1262785
-
Receptor occupancy dose--response curve suggests that phosphatidyl-inositol breakdown may be intrinsic to the mechanism of the muscarinic cholinergic receptor.
FEBS Lett. 1976 Oct 15;69(1):1-5
PMID: 992019
-
Transport of sodium, potassium, and calcium across rabbit polymorphonuclear leukocyte membranes. Effect of chemotactic factor.
J Cell Biol. 1977 May;73(2):428-44
PMID: 558197
-
Desensitization of the neutrophil aggregation response to chemotactic factors.
Am J Pathol. 1978 Dec;93(3):693-706
PMID: 717543