Inhibition of CaV3.2 T-type calcium channels in peripheral sensory neurons contributes to analgesic properties of epipregnanolone
Rationale T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce poten...
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| Published in | Psychopharmacology Vol. 231; no. 17; pp. 3503 - 3515 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Berlin/Heidelberg
Springer Berlin Heidelberg
01.09.2014
Springer Springer Nature B.V |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0033-3158 1432-2072 1432-2072 |
| DOI | 10.1007/s00213-014-3588-0 |
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| Abstract | Rationale
T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223–1235,
2004
).
Objectives
Here, we investigated the effects of the endogenous 5β-reduced neuroactive steroid molecule, epipregnanolone [(3β,5β)-3-hydroxypregnan-20-one], on peripheral nociception.
Methods
We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels.
Results
We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC
50
) of 2 μM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 μM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of Ca
V
3.2 knockout mice.
Conclusions
We conclude that the inhibition of peripheral Ca
V
3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. |
|---|---|
| AbstractList | Rationale: T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5 beta -reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004). Objectives: Here, we investigated the effects of the endogenous 5 beta -reduced neuroactive steroid molecule, epipregnanolone [(3 beta ,5 beta )-3-hydroxypregnan-20-one], on peripheral nociception. Methods: We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels. Results: We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC sub(50)) of 2 mu M and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 mu M. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of Ca sub(V)3.2 knockout mice. Conclusions: We conclude that the inhibition of peripheral Ca sub(V)3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. Rationale T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5 β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004). Objectives Here, we investigated the effects of the endogenous 5 β-reduced neuroactive steroid molecule, epipregnanolone [(3β, 5β)-3-hydroxypregnan-20-one], on peripheral nociception. Methods We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels. Results We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration ([IC.sub.50]) of 2 µM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 µM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of [Ca.sub.V]3.2 knockout mice. Conclusions We conclude that the inhibition of peripheral [Ca.sub.V]3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. Keywords Low-voltage-activated * [Ca.sup.2+] * Pain * Dorsal root * Hyperalgesia T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004). Here, we investigated the effects of the endogenous 5β-reduced neuroactive steroid molecule, epipregnanolone [(3β,5β)-3-hydroxypregnan-20-one], on peripheral nociception. We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels. We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC50) of 2 μM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 μM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of CaV3.2 knockout mice. We conclude that the inhibition of peripheral CaV3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. Rationale T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223–1235, 2004 ). Objectives Here, we investigated the effects of the endogenous 5β-reduced neuroactive steroid molecule, epipregnanolone [(3β,5β)-3-hydroxypregnan-20-one], on peripheral nociception. Methods We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels. Results We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC 50 ) of 2 μM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 μM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of Ca V 3.2 knockout mice. Conclusions We conclude that the inhibition of peripheral Ca V 3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. Issue Title: Neuroactive Steroids in the CNS in Memory of Robert H. Purdy' T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5[beta]-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004 ). Here, we investigated the effects of the endogenous 5[beta]-reduced neuroactive steroid molecule, epipregnanolone [(3[beta],5[beta])-3-hydroxypregnan-20-one], on peripheral nociception. We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels. We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC^sub 50^) of 2 [mu]M and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 [mu]M. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of Ca^sub V^3.2 knockout mice. We conclude that the inhibition of peripheral Ca^sub V^3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone.[PUBLICATION ABSTRACT] T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004).RATIONALET-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of 5β-reduced steroids induce a voltage-dependent blockade of T-currents in rat dorsal root ganglia (DRG) cells in vitro and induce potent analgesia to thermal stimuli in rats in vivo (Mol Pharmacol 66:1223-1235, 2004).Here, we investigated the effects of the endogenous 5β-reduced neuroactive steroid molecule, epipregnanolone [(3β,5β)-3-hydroxypregnan-20-one], on peripheral nociception.OBJECTIVESHere, we investigated the effects of the endogenous 5β-reduced neuroactive steroid molecule, epipregnanolone [(3β,5β)-3-hydroxypregnan-20-one], on peripheral nociception.We used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels.METHODSWe used acutely dissociated DRG cells in vitro from adult rats as well as in vivo pain studies in mice and rats to investigate the effects of epipregnanolone on DRG T-channels.We found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC50) of 2 μM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 μM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of CaV3.2 knockout mice.RESULTSWe found that epipregnanolone reversibly blocked DRG T-currents with a half-maximal inhibitory concentration (IC50) of 2 μM and stabilized the channel in the inactive state. However, sodium, potassium, and gamma-aminobutyric acid (GABA)-gated ionic currents were not sensitive to the blocking effects of epipregnanolone even at 10 μM. In ensuing in vivo studies, we found that intraplantar (i.pl.) injections of epipregnanolone directly into peripheral receptive fields reduced responses to nociceptive heat stimuli in rats in a dose-dependent fashion. Furthermore, i.pl. epipregnanolone injections effectively reduced responses to peripheral nociceptive thermal and mechanical stimuli in wild-type mice but had no effect on the responses of CaV3.2 knockout mice.We conclude that the inhibition of peripheral CaV3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone.CONCLUSIONSWe conclude that the inhibition of peripheral CaV3.2 T-channels contributes to the potent analgesic effect of the endogenous steroid epipregnanolone. |
| Audience | Academic |
| Author | Rose, Kirstin E. Hong, Sung Jun Bozic, Neda Jevtovic-Todorovic, Vesna Todorovic, Slobodan M. DiGruccio, Michael R. Ayoola, Christine Boyd, Christopher Osuru, Hari Prasad Covey, Douglas F. Park, Ji-Yong Hwang, Sung Mi |
| AuthorAffiliation | e Department of Neuroscience, University of Virginia Health System, Charlottesville, VA g Department of Anesthesiology and Pain Medicine, College of Medicine, Korea University, Seoul, Republic of Korea c Department of Anesthesiology and Pain Medicine, Chuncheon Sacred Heart Hospital, College of Medicine, Hallym University, Seoul, Republic of Korea f Department of Neuroscience Graduate Program, University of Virginia Health System, Charlottesville, VA d Department of Anesthesiology and Pain Medicine, Kangdong Sacred Heart Hospital, College of Medicine, Hallym University Seoul, Republic of Korea a Department of Anesthesiology, University of Virginia Health System, Charlottesville, VA b Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO |
| AuthorAffiliation_xml | – name: a Department of Anesthesiology, University of Virginia Health System, Charlottesville, VA – name: g Department of Anesthesiology and Pain Medicine, College of Medicine, Korea University, Seoul, Republic of Korea – name: b Department of Developmental Biology, Washington University School of Medicine, St. Louis, MO – name: c Department of Anesthesiology and Pain Medicine, Chuncheon Sacred Heart Hospital, College of Medicine, Hallym University, Seoul, Republic of Korea – name: f Department of Neuroscience Graduate Program, University of Virginia Health System, Charlottesville, VA – name: d Department of Anesthesiology and Pain Medicine, Kangdong Sacred Heart Hospital, College of Medicine, Hallym University Seoul, Republic of Korea – name: e Department of Neuroscience, University of Virginia Health System, Charlottesville, VA |
| Author_xml | – sequence: 1 givenname: Christine surname: Ayoola fullname: Ayoola, Christine organization: Department of Anesthesiology, University of Virginia Health System – sequence: 2 givenname: Sung Mi surname: Hwang fullname: Hwang, Sung Mi organization: Department of Anesthesiology, University of Virginia Health System, Department of Anesthesiology and Pain Medicine, Chuncheon Sacred Heart Hospital, College of Medicine, Hallym University – sequence: 3 givenname: Sung Jun surname: Hong fullname: Hong, Sung Jun organization: Department of Anesthesiology, University of Virginia Health System, Department of Anesthesiology and Pain Medicine, Kangdong Sacred Heart Hospital, College of Medicine, Hallym University – sequence: 4 givenname: Kirstin E. surname: Rose fullname: Rose, Kirstin E. organization: Department of Anesthesiology, University of Virginia Health System – sequence: 5 givenname: Christopher surname: Boyd fullname: Boyd, Christopher organization: Department of Anesthesiology, University of Virginia Health System – sequence: 6 givenname: Neda surname: Bozic fullname: Bozic, Neda organization: Department of Anesthesiology, University of Virginia Health System – sequence: 7 givenname: Ji-Yong surname: Park fullname: Park, Ji-Yong organization: Department of Anesthesiology and Pain Medicine, College of Medicine, Korea University – sequence: 8 givenname: Hari Prasad surname: Osuru fullname: Osuru, Hari Prasad organization: Department of Anesthesiology, University of Virginia Health System – sequence: 9 givenname: Michael R. surname: DiGruccio fullname: DiGruccio, Michael R. organization: Department of Anesthesiology, University of Virginia Health System, Neuroscience Graduate Program, University of Virginia Health System – sequence: 10 givenname: Douglas F. surname: Covey fullname: Covey, Douglas F. organization: Department of Developmental Biology, School of Medicine, Washington University – sequence: 11 givenname: Vesna surname: Jevtovic-Todorovic fullname: Jevtovic-Todorovic, Vesna organization: Department of Anesthesiology, University of Virginia Health System, Department of Neuroscience, University of Virginia Health System, Neuroscience Graduate Program, University of Virginia Health System – sequence: 12 givenname: Slobodan M. surname: Todorovic fullname: Todorovic, Slobodan M. email: st9d@virginia.edu organization: Department of Anesthesiology, University of Virginia Health System, Department of Neuroscience, University of Virginia Health System, Neuroscience Graduate Program, University of Virginia Health System |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24800894$$D View this record in MEDLINE/PubMed |
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T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic... T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic series of... Rationale T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic... Issue Title: Neuroactive Steroids in the CNS in Memory of Robert H. Purdy' T-type calcium channels (T-channels) play an important role in controlling... Rationale: T-type calcium channels (T-channels) play an important role in controlling excitability of nociceptors. We have previously shown that a synthetic... |
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| SubjectTerms | Analgesics Analgesics - pharmacology Animals Behavior, Animal - drug effects Biomedical and Life Sciences Biomedicine Calcium Calcium Channel Blockers - pharmacology Calcium channels Calcium Channels, T-Type - drug effects Calcium Channels, T-Type - genetics Dosage and administration Drug interactions Female Health aspects Identification and classification Male Mice Mice, Knockout Neurons Neurosciences Nociceptors - drug effects Original Investigation Pain management Pain Measurement - drug effects Patch-Clamp Techniques Peripheral Nerves - drug effects Pharmacology/Toxicology Pregnanolone - pharmacology Psychiatry Psychopharmacology Rats Sensory Receptor Cells - drug effects Sensory receptors Steroids (Drugs) |
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| Title | Inhibition of CaV3.2 T-type calcium channels in peripheral sensory neurons contributes to analgesic properties of epipregnanolone |
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