Abstract
1. The whole cell variant of the patch clamp technique was used to record high voltage-activated Ca2+ currents and Ca(2+)-activated Cl- tail currents from cultured neonatal rat dorsal root ganglion neurones. The aim of the project was to use these currents as physiological indices of intracellular Ca2+ regulation under control conditions and in the presence of metabolic inhibitors. 2. Carbonyl cyanide p-trifluoromethoxyphenylhydrazone (5 microM) and sodium cyanide (1 microM) inhibited Ca2+ currents within 20 s, even when ATP was present in the patch pipette solution, suggesting a direct action on Ca2+ channels. These metabolic inhibitors did not affect Ca2+ current 'run down' or inactivation kinetics. 3. Cultured neonatal dorsal root ganglion neurones of the rat were relatively insensitive to the removal of glucose and ATP from the recording solutions for up to 3 h. These data suggest that the Ca2+ homeostatic mechanisms in these cells are highly resistant to metabolic insult. 4. However 2-deoxy-D-glucose (5 mM) in the extracellular recording medium with no ATP or glucose present did prolong the deactivation time of Ca(2+)-activated Cl- tail currents and increase the total charge flow following activation of a 500 ms voltage-activated Ca2+ current. This effect was prevented by inclusion of D-fructose 1,6-diphosphate (500 microM) in the patch pipette solution. 5. We conclude that some agents used to induce chemical hypoxia, such as carbonyl cyanide p-trifluoromethoxyphenylhydrazone and sodium cyanide, may interact directly with voltage-activated Ca2+ channels and are therefore not appropriate for use in studying disturbed neuronal Ca2+ homeostasis. However, the use of 2-deoxy-D-glucose in the absence of glucose and ATP does represent a model of disturbed Ca2+ homeostasis in cultured dorsal root ganglion neurones. In this study we have combined the whole cell recording technique with cultured neurones under conditions which produce a degree of metabolic stress as reflected by prolonged Ca(2+)-activated Cl- tail currents. The reduced efficiency of handling of intracellular Ca2+ loads may be an important factor contributing to the onset of neuronal damage during hypoxia and ischaemia.
MeSH Terms
Adenosine Triphosphate/metabolism
Animals
Animals, Newborn
Calcium/metabolism
Calcium Channels/drug effects
Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone/pharmacology
Cells, Cultured
Deoxyglucose/metabolism
Electrophysiology
Fructosediphosphates/metabolism
Ganglia, Spinal/cytology
Glycolysis/drug effects
Neurons, Afferent/drug effects,physiology
Oxidative Phosphorylation/drug effects
Rats
Rats, Wistar
Sodium Cyanide/pharmacology
Chemicals
Calcium Channels
Fructosediphosphates
Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone
Adenosine Triphosphate
Deoxyglucose
fructose-1,6-diphosphate
Sodium Cyanide
Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Stapleton S R
Department of Physiology, St George's Hospital Medical School, London.
Scott R H
Bell B A
References (29)
29 references, click to expand
-
Transport of protons across membranes by weak acids.
Physiol Rev. 1980 Jul;60(3):825-63
PMID: 6248908
-
Calcium currents in aged rat dorsal root ganglion neurones.
J Physiol. 1993 Feb;461:467-83
PMID: 8394426
-
Cell damage in the brain: a speculative synthesis.
J Cereb Blood Flow Metab. 1981;1(2):155-85
PMID: 6276420
-
The calcium pump and sodium-calcium exchange in squid axons.
Annu Rev Physiol. 1983;45:313-24
PMID: 6303203
-
Calcium overload in selectively vulnerable neurons of the hippocampus during and after ischemia: an electron microscopy study in the rat.
J Cereb Blood Flow Metab. 1984 Sep;4(3):350-61
PMID: 6470053
-
A Ca-dependent Cl- conductance in cultured mouse spinal neurones.
Nature. 1984 Oct 11-17;311(5986):567-70
PMID: 6482969
-
Ischaemic brain damage: the role of excitatory activity and of calcium entry.
Br J Anaesth. 1985 Jan;57(1):44-6
PMID: 3966963
-
A calcium-activated chloride current generates the after-depolarization of rat sensory neurones in culture.
J Physiol. 1985 Jul;364:217-39
PMID: 2411915
-
An enzymatic mechanism for calcium current inactivation in dialysed Helix neurones.
J Physiol. 1986 Sep;378:31-51
PMID: 2432251
-
In squid axons, ATP modulates Na+-Ca2+ exchange by a Ca2+i-dependent phosphorylation.
Biochim Biophys Acta. 1987 Mar 12;897(3):347-54
PMID: 3814592
-
Voltage-activated calcium channels that must be phosphorylated to respond to membrane depolarization.
Proc Natl Acad Sci U S A. 1987 Apr;84(8):2518-22
PMID: 2436233
-
Effects of hypoxia on rat hippocampal neurones in vitro.
J Physiol. 1987 Mar;384:131-51
PMID: 2443657
-
Calcium-activated chloride current in cultured sensory and parasympathetic quail neurones.
J Physiol. 1987 Dec;394:125-48
PMID: 3502143
-
Calcium transport and buffering in neurons.
Trends Neurosci. 1988 Oct;11(10):438-43
PMID: 2469161
-
Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage.
Trends Neurosci. 1988 Oct;11(10):465-9
PMID: 2469166
-
Changes in membrane currents of hippocampal neurons evoked by brief anoxia.
J Neurophysiol. 1989 Jul;62(1):15-30
PMID: 2754469
-
Anoxia on slow inward currents of immature hippocampal neurons.
J Neurophysiol. 1989 Oct;62(4):896-906
PMID: 2553881
-
Protection of hippocampal slices from young rats against anoxic transmission damage is due to better maintenance of ATP.
J Physiol. 1989 Jun;413:1-11
PMID: 2557434
-
Electrogenic properties of the Na:Ca exchange.
J Membr Biol. 1990 Feb;113(3):177-91
PMID: 2186169
-
Calcium-dependent chloride current in neurones of the rabbit pelvic parasympathetic ganglia.
J Physiol. 1990 Mar;422:303-20
PMID: 1693681
-
Effects of metabolic inhibition on the membrane properties of isolated mouse primary sensory neurones.
J Physiol. 1990 May;424:387-409
PMID: 2391654
-
Effects of metabolic blockade on the regulation of intracellular calcium in dissociated mouse sensory neurones.
J Physiol. 1990 May;424:411-26
PMID: 2391656
-
The control of neuronal Ca2+ homeostasis.
Prog Neurobiol. 1991;37(3):255-85
PMID: 1947178
-
Mechanisms of excitation-contraction coupling failure during metabolic inhibition in guinea-pig ventricular myocytes.
J Physiol. 1991 Nov;443:371-86
PMID: 1822531
-
Calcium-activated currents in cultured neurones from rat dorsal root ganglia.
Br J Pharmacol. 1992 Jul;106(3):593-602
PMID: 1324075
-
Palmitoyl-DL-carnitine has calcium-dependent effects on cultured neurones from rat dorsal root ganglia.
Br J Pharmacol. 1992 Dec;107(4):1192-7
PMID: 1334752
-
Ca2+ efflux mechanisms following depolarization evoked calcium transients in cultured rat sensory neurones.
J Physiol. 1992 Sep;455:567-83
PMID: 1484362
-
Major differences in Ca2+i response to anoxia between neonatal and adult rat CA1 neurons: role of Ca2+o and Na+o.
J Neurosci. 1993 Jan;13(1):63-72
PMID: 8093716
-
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