Mechano- and chemosensitivity of rat nodose neurones - Selective excitatory effects of prostacyclin

Vladislav Snitsarev, Carol A. Whiteis, Mark W. Chapleau, François M. Abboud

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11 Citations (Scopus)

Abstract

Nodose ganglion sensory neurones exert a significant reflex autonomic influence. We contrasted their mechanosensitivity, excitability and chemosensitivity in response to the stable prostacyclin (PGI2) analogue carbacyclin (cPGI) in culture. Under current clamp conditions we measured changes in membrane potential (ΔmV) and action potential (AP) responses to mechanically induced depolarizations and depolarizing current injections before and after superfusion of cPGI (1 μm and 10 μm). Chemosensitivity was indicated by augmentation of AP firing frequency and increased maximum gain of AP frequency (max. dAP/ dΔmV), during superfusion with cPGI. Results indicate that two groups of neurones, A and B, are mechanosensitive (MS) and one group, C, is mechanoinsensitive (MI). Group A shows modest depolarization without AP generation during mechanical stimulation, and no increase in max. dAP/ dΔmV, despite a marked increase in electrical depolarization with cPGI. Group B shows pronounced mechanical depolarization accompanied by enhanced AP discharge with cPGI, and an increase in max. dAP/dΔmV. Group C remains MI after cPGI but is more excitable and markedly chemosensitive (CS) with a pronounced enhancement of max. dAP/dΔmV with cPGI. The effect of cPGI on ionic conductances indicates that it does not sensitize the mechanically gated depolarizing degenerin/ epithelial Na+ channels (DEG/ENaC), but it inhibits two voltage-gated K+ currents, Maxi-K and M-current, causing enhanced AP firing frequency and depolarization, respectively. We conclude that MS nodose neurones may be unimodal MS or bimodal MS/CS, and that MI neurones are unimodal CS, and much more CS to cPGI than MS/ CS neurones. We suggest that the known excitatory effect of PGI2 on baroreceptor and vagal afferent fibres is mediated by inhibition of voltage-gated K+ channels (Maxi-K and M-current) and not by an effect on mechanically gated DEG/ENaC channels.

Original languageEnglish
Pages (from-to)177-194
Number of pages18
JournalJournal of Physiology
Volume582
Issue number1
DOIs
StatePublished - 1 Jul 2007

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Epoprostenol
Action Potentials
Neurons
Degenerin Sodium Channels
Epithelial Sodium Channels
Nodose Ganglion
Voltage-Gated Potassium Channels
Pressoreceptors
Sensory Receptor Cells
Membrane Potentials
Reflex
Injections

Cite this

Snitsarev, Vladislav ; Whiteis, Carol A. ; Chapleau, Mark W. ; Abboud, François M. / Mechano- and chemosensitivity of rat nodose neurones - Selective excitatory effects of prostacyclin. In: Journal of Physiology. 2007 ; Vol. 582, No. 1. pp. 177-194.
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abstract = "Nodose ganglion sensory neurones exert a significant reflex autonomic influence. We contrasted their mechanosensitivity, excitability and chemosensitivity in response to the stable prostacyclin (PGI2) analogue carbacyclin (cPGI) in culture. Under current clamp conditions we measured changes in membrane potential (ΔmV) and action potential (AP) responses to mechanically induced depolarizations and depolarizing current injections before and after superfusion of cPGI (1 μm and 10 μm). Chemosensitivity was indicated by augmentation of AP firing frequency and increased maximum gain of AP frequency (max. dAP/ dΔmV), during superfusion with cPGI. Results indicate that two groups of neurones, A and B, are mechanosensitive (MS) and one group, C, is mechanoinsensitive (MI). Group A shows modest depolarization without AP generation during mechanical stimulation, and no increase in max. dAP/ dΔmV, despite a marked increase in electrical depolarization with cPGI. Group B shows pronounced mechanical depolarization accompanied by enhanced AP discharge with cPGI, and an increase in max. dAP/dΔmV. Group C remains MI after cPGI but is more excitable and markedly chemosensitive (CS) with a pronounced enhancement of max. dAP/dΔmV with cPGI. The effect of cPGI on ionic conductances indicates that it does not sensitize the mechanically gated depolarizing degenerin/ epithelial Na+ channels (DEG/ENaC), but it inhibits two voltage-gated K+ currents, Maxi-K and M-current, causing enhanced AP firing frequency and depolarization, respectively. We conclude that MS nodose neurones may be unimodal MS or bimodal MS/CS, and that MI neurones are unimodal CS, and much more CS to cPGI than MS/ CS neurones. We suggest that the known excitatory effect of PGI2 on baroreceptor and vagal afferent fibres is mediated by inhibition of voltage-gated K+ channels (Maxi-K and M-current) and not by an effect on mechanically gated DEG/ENaC channels.",
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Mechano- and chemosensitivity of rat nodose neurones - Selective excitatory effects of prostacyclin. / Snitsarev, Vladislav; Whiteis, Carol A.; Chapleau, Mark W.; Abboud, François M.

In: Journal of Physiology, Vol. 582, No. 1, 01.07.2007, p. 177-194.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Mechano- and chemosensitivity of rat nodose neurones - Selective excitatory effects of prostacyclin

AU - Snitsarev, Vladislav

AU - Whiteis, Carol A.

AU - Chapleau, Mark W.

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N2 - Nodose ganglion sensory neurones exert a significant reflex autonomic influence. We contrasted their mechanosensitivity, excitability and chemosensitivity in response to the stable prostacyclin (PGI2) analogue carbacyclin (cPGI) in culture. Under current clamp conditions we measured changes in membrane potential (ΔmV) and action potential (AP) responses to mechanically induced depolarizations and depolarizing current injections before and after superfusion of cPGI (1 μm and 10 μm). Chemosensitivity was indicated by augmentation of AP firing frequency and increased maximum gain of AP frequency (max. dAP/ dΔmV), during superfusion with cPGI. Results indicate that two groups of neurones, A and B, are mechanosensitive (MS) and one group, C, is mechanoinsensitive (MI). Group A shows modest depolarization without AP generation during mechanical stimulation, and no increase in max. dAP/ dΔmV, despite a marked increase in electrical depolarization with cPGI. Group B shows pronounced mechanical depolarization accompanied by enhanced AP discharge with cPGI, and an increase in max. dAP/dΔmV. Group C remains MI after cPGI but is more excitable and markedly chemosensitive (CS) with a pronounced enhancement of max. dAP/dΔmV with cPGI. The effect of cPGI on ionic conductances indicates that it does not sensitize the mechanically gated depolarizing degenerin/ epithelial Na+ channels (DEG/ENaC), but it inhibits two voltage-gated K+ currents, Maxi-K and M-current, causing enhanced AP firing frequency and depolarization, respectively. We conclude that MS nodose neurones may be unimodal MS or bimodal MS/CS, and that MI neurones are unimodal CS, and much more CS to cPGI than MS/ CS neurones. We suggest that the known excitatory effect of PGI2 on baroreceptor and vagal afferent fibres is mediated by inhibition of voltage-gated K+ channels (Maxi-K and M-current) and not by an effect on mechanically gated DEG/ENaC channels.

AB - Nodose ganglion sensory neurones exert a significant reflex autonomic influence. We contrasted their mechanosensitivity, excitability and chemosensitivity in response to the stable prostacyclin (PGI2) analogue carbacyclin (cPGI) in culture. Under current clamp conditions we measured changes in membrane potential (ΔmV) and action potential (AP) responses to mechanically induced depolarizations and depolarizing current injections before and after superfusion of cPGI (1 μm and 10 μm). Chemosensitivity was indicated by augmentation of AP firing frequency and increased maximum gain of AP frequency (max. dAP/ dΔmV), during superfusion with cPGI. Results indicate that two groups of neurones, A and B, are mechanosensitive (MS) and one group, C, is mechanoinsensitive (MI). Group A shows modest depolarization without AP generation during mechanical stimulation, and no increase in max. dAP/ dΔmV, despite a marked increase in electrical depolarization with cPGI. Group B shows pronounced mechanical depolarization accompanied by enhanced AP discharge with cPGI, and an increase in max. dAP/dΔmV. Group C remains MI after cPGI but is more excitable and markedly chemosensitive (CS) with a pronounced enhancement of max. dAP/dΔmV with cPGI. The effect of cPGI on ionic conductances indicates that it does not sensitize the mechanically gated depolarizing degenerin/ epithelial Na+ channels (DEG/ENaC), but it inhibits two voltage-gated K+ currents, Maxi-K and M-current, causing enhanced AP firing frequency and depolarization, respectively. We conclude that MS nodose neurones may be unimodal MS or bimodal MS/CS, and that MI neurones are unimodal CS, and much more CS to cPGI than MS/ CS neurones. We suggest that the known excitatory effect of PGI2 on baroreceptor and vagal afferent fibres is mediated by inhibition of voltage-gated K+ channels (Maxi-K and M-current) and not by an effect on mechanically gated DEG/ENaC channels.

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