Abstract
1. Putrescine has been implicated in modulating cytoplasmic calcium concentration and is correlated with selective neuronal vulnerability in cerebral ischaemia. In order to determine whether putrescine modulates voltage-activated calcium channels, whole-cell and single channel patch clamp experiments were performed with N1E-115 mouse neuroblastoma cells. 2. L-type calcium channel currents showed a 34 +/- 21% increase (n = 6 cells) during external application of 1 mM putrescine. There was no change in the kinetics of the current and no shift in the current-voltage relationship along the voltage axis. 3. T-type calcium channel currents were not affected by 1 mM putrescine. 4. The effect of putrescine on single L-type calcium channels was studied using the cell-attached configuration of the patch clamp technique. Putrescine (5 mM) applied to the bathing solution, but not present in the pipette, caused an increase in open time of the single channel current without changing the conductance of the channel. In 345 depolarizing steps compiled from three cells, the number of channel openings longer than 3 ms increased from six to seventy-six, and the number of channel openings longer than 9 ms increased from zero to twenty-seven. This single channel study supports the hypothesis that putrescine acts on the L-type channel from the inside of the cell. 5. External application of 1 mM spermine and 1 mM spermidine had no effect on T- and L-type calcium channels. Thus, the effect of putrescine is probably not mediated by the higher polyamines. 6. In order to test whether the effect of putrescine is mediated by a second messenger, specific protein kinase C and cyclic AMP-dependent protein kinase inhibitors, staurosporine and KT5720, respectively, were applied prior to putrescine. When cells were preconditioned with 200 nM staurosporine, the increase of the L-type calcium current by 1 mM putrescine was inhibited. By contrast, 200 nM KT5720 did not inhibit the putrescine effect. Therefore, the increase of L-type channel currents by putrescine may be mediated by protein kinase C but not the cyclic AMP-dependent protein kinase. 7. The putrescine-induced enhancement of the L-type calcium channel activity may play an important role in calcium-induced neurotoxicity.
MeSH Terms
Alkaloids/pharmacology
Animals
Calcium Channels/drug effects
Carbazoles
Electric Stimulation
Indoles/pharmacology
Membrane Potentials/physiology
Mice
Neuroblastoma
Polyamines/pharmacology
Protein Kinase C/antagonists & inhibitors
Putrescine/pharmacology
Pyrroles/pharmacology
Staurosporine
Tumor Cells, Cultured/drug effects
Chemicals
Alkaloids
Calcium Channels
Carbazoles
Indoles
Polyamines
Pyrroles
KT 5720
Protein Kinase C
Staurosporine
Putrescine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Herman M D
Department of Pharmacology, Northwestern University Medical School, Chicago, IL 60611.
Reuveny E
Narahashi T
References (29)
29 references, click to expand
-
Maturation of neuroblastoma cells in the presence of dimethylsulfoxide.
Proc Natl Acad Sci U S A. 1976 Feb;73(2):462-6
PMID: 1756
-
Polyamines allosterically modulate [3H]nitrendipine binding to the voltage-sensitive calcium channel in rat brain.
Eur J Pharmacol. 1992 Feb 13;225(2):167-9
PMID: 1312941
-
Ionic currents in cultured mouse neuroblastoma cells under voltage-clamp conditions.
J Physiol. 1978 May;278:265-86
PMID: 671297
-
Transient formation of superoxide radicals in polyunsaturated fatty acid-induced brain swelling.
J Neurochem. 1980 Oct;35(4):1004-7
PMID: 6256498
-
Calcium-dependent proteolysis in living cells.
Life Sci. 1981 Sep 14;29(11):1079-87
PMID: 7026951
-
Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
Pflugers Arch. 1981 Aug;391(2):85-100
PMID: 6270629
-
Brain cortical fatty acids and phospholipids during and following complete and severe incomplete ischemia.
J Neurochem. 1982 Jan;38(1):84-93
PMID: 7108537
-
Polyamines inhibit phospholipid-sensitive and calmodulin-sensitive Ca2+-dependent protein kinases.
Biochem J. 1983 Aug 1;213(2):281-8
PMID: 6615435
-
Different modes of Ca channel gating behaviour favoured by dihydropyridine Ca agonists and antagonists.
Nature. 1984 Oct 11-17;311(5986):538-44
PMID: 6207437
-
Putrescine distribution in Escherichia coli studied in vivo by 13C nuclear magnetic resonance.
Biochim Biophys Acta. 1984 Dec 11;805(4):337-44
PMID: 6391557
-
Polyamines appear to be second messengers in mediating Ca2+ fluxes and neurotransmitter release in potassium-depolarized synaptosomes.
Biochem Biophys Res Commun. 1985 Dec 17;133(2):563-73
PMID: 2867766
-
Polyamines contribute to calcium-stimulated release of aspartate from brain particulate fractions.
Brain Res. 1986 Apr 16;371(1):96-100
PMID: 2871896
-
An inhibitory role for polyamines in protein kinase C activation and insulin secretion in mouse pancreatic islets.
Biochem J. 1986 Jul 1;237(1):131-8
PMID: 3541895
-
Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia.
J Cereb Blood Flow Metab. 1987 Feb;7(1):89-95
PMID: 3805166
-
K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases.
Biochem Biophys Res Commun. 1987 Jan 30;142(2):436-40
PMID: 3028414
-
Ionic dependence of glutamate neurotoxicity.
J Neurosci. 1987 Feb;7(2):369-79
PMID: 2880938
-
Characterization of two types of calcium channels in mouse neuroblastoma cells.
J Physiol. 1987 Feb;383:231-49
PMID: 2443646
-
Inhibitory action of polyamines on protein kinase C association to membranes.
Biochem J. 1987 Oct 1;247(1):175-80
PMID: 3479981
-
Relationship between putrescine content and density of ischemic cell damage in the brain of mongolian gerbils: effect of nimodipine and barbiturate.
Acta Neuropathol. 1988;76(4):388-94
PMID: 3176904
-
Polyamines in cerebral ischemia.
Neurochem Pathol. 1988 Jul-Dec;9:1-20
PMID: 2907781
-
Staurosporine, K-252 and UCN-01: potent but nonspecific inhibitors of protein kinases.
Trends Pharmacol Sci. 1989 Jun;10(6):218-20
PMID: 2672462
-
cis-Fatty acids, which activate protein kinase C, attenuate Na+ and Ca2+ currents in mouse neuroblastoma cells.
J Physiol. 1989 Dec;419:95-119
PMID: 2559978
-
Putrescine content and structural defects in isolated fractions of rat brain after reversible cerebral ischemia.
Exp Neurol. 1990 Mar;107(3):249-55
PMID: 2307203
-
Excitatory amino acids activate calpain I and induce structural protein breakdown in vivo.
Neuron. 1988 Jun;1(4):279-87
PMID: 2856162
-
Ethanol effects on two types of voltage-activated calcium channels.
J Pharmacol Exp Ther. 1990 Sep;254(3):1029-37
PMID: 2168482
-
The polyamine spermine affects omega-conotoxin binding and function at N-type voltage-sensitive calcium channels.
J Auton Pharmacol. 1990 Aug;10(4):213-9
PMID: 2172254
-
Polyamines potentiate responses of N-methyl-D-aspartate receptors expressed in xenopus oocytes.
Proc Natl Acad Sci U S A. 1990 Dec;87(24):9971-4
PMID: 1702227
-
Polyamine uptake, binding and release in rat brain.
Eur J Pharmacol. 1991 Jan 25;193(1):41-6
PMID: 2050191
-
Inactivation of the sodium channel. I. Sodium current experiments.
J Gen Physiol. 1977 Nov;70(5):549-66
PMID: 591911