Skip to main content
Erschienen in: Metabolic Brain Disease 4/2017

12.06.2017 | Original Article

The analgesic effect of trans-resveratrol is regulated by calcium channels in the hippocampus of mice

verfasst von: Weijie Wang, Yingcong Yu, Jing Li, Lin Wang, Zhi Li, Chong Zhang, Linlin Zhen, Lianshu Ding, Gang Wang, Xiaoyang Sun, Ying Xu

Erschienen in: Metabolic Brain Disease | Ausgabe 4/2017

Einloggen, um Zugang zu erhalten

Abstract

Resveratrol has been widely studied in terms of it’s potential to slow the progression of many diseases. But little is known about the mechanism of action in neuropathic pain. Neuropathic pain is the main type of chronic pain associated with tissue injury. Calcium channels and calcium/caffeine-sensitive pools are associated with analgesic pathway involving neuropathic pain. Our previous study suggested that the antinociceptive effect of resveratrol was involved in Ca2+/calmodulin-dependent signaling in the spinal cord of mice. The aim of this study was to explore the involvement of Ca2+ in analgesic effects of trans-resveratrol in neuropathic pain and signal pathway in hippocampus. Hot plate test was used to assess antinociceptive response when mice were treated with trans-resveratrol alone or in combination with Mk 801, nimodipine, CaCl2, ryanodine or EGTA. The effects of trans-resveratrol and the combination on Ca2+/calmodulin-dependent protein kinase II (CaMKII) and BDNF (brain-derived neurotrophic factor) expression in hippocampus were also investigated. The results showed that trans-resveratrol increased paw withdraw latency in the hot plate test. The effect of resveratrol was enhanced by Mk 801 and nimodipine. Central administration of Ca2+, however, abolished the antinociceptive effects of resveratrol. In contrast, centrally administered EGTA or ryanodine improved trans-resveratrol induced antinociception. There was a significant increase in p-CaMKII and BDNF expression in the hippocampus when resveratrol were combined with Mk 801, nimodipine, ryanodine and EGTA. Administration of CaCl2 blocked changes in p-CaMKII and BDNF levels in the hippocampus. These findings suggest that trans-resveratrol exerts the effects of antinociception through regulation of calcium channels and calcium/caffeine-sensitive pools.
Literatur
Zurück zum Zitat Backonja M, Woolf CJ (2010) Future directions in neuropathic pain therapy: closing the translational loop. Oncologist 15:24–29CrossRefPubMed Backonja M, Woolf CJ (2010) Future directions in neuropathic pain therapy: closing the translational loop. Oncologist 15:24–29CrossRefPubMed
Zurück zum Zitat Baron R (2006) Mechanisms of disease: neuropathic pain - a clinical perspective. Nat Clin Pract Neurol 2:95–106CrossRefPubMed Baron R (2006) Mechanisms of disease: neuropathic pain - a clinical perspective. Nat Clin Pract Neurol 2:95–106CrossRefPubMed
Zurück zum Zitat Bennett MK, Erondu NE, Kennedy MB (1983) Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. J Biol Chem 258:12735–12744PubMed Bennett MK, Erondu NE, Kennedy MB (1983) Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. J Biol Chem 258:12735–12744PubMed
Zurück zum Zitat Ben-Sreti MM, Gonzalez JP, Sewell RD (1983) Effects of elevated calcium and calcium antagonists on 6,7-benzomorphan-induced analgesia. Eur J Pharmacol 90:385–391CrossRefPubMed Ben-Sreti MM, Gonzalez JP, Sewell RD (1983) Effects of elevated calcium and calcium antagonists on 6,7-benzomorphan-induced analgesia. Eur J Pharmacol 90:385–391CrossRefPubMed
Zurück zum Zitat Brüggemann I, Schulz S, Wiborny D, Höllt V (2000) Colocalization of the mu-opioid receptor and calcium/calmodulin-dependent kinase II in distinct pain-processing brain regions. Brain Res Mol Brain Res 85:239–250CrossRefPubMed Brüggemann I, Schulz S, Wiborny D, Höllt V (2000) Colocalization of the mu-opioid receptor and calcium/calmodulin-dependent kinase II in distinct pain-processing brain regions. Brain Res Mol Brain Res 85:239–250CrossRefPubMed
Zurück zum Zitat Carlton SM (2002) Localization of CaMKIIalpha in rat primary sensory neurons: increase in inflammation. Brain Res 947:252–259CrossRefPubMed Carlton SM (2002) Localization of CaMKIIalpha in rat primary sensory neurons: increase in inflammation. Brain Res 947:252–259CrossRefPubMed
Zurück zum Zitat Chapman DB, Way EL (1982) Modification of endorphine/enkephalin analgesia and stress-induced analgesia by divalent cations, a cation chelator and an ionophore. Br J Pharmacol 75:389–396CrossRefPubMedPubMedCentral Chapman DB, Way EL (1982) Modification of endorphine/enkephalin analgesia and stress-induced analgesia by divalent cations, a cation chelator and an ionophore. Br J Pharmacol 75:389–396CrossRefPubMedPubMedCentral
Zurück zum Zitat Chen JQ, Zhang YQ, Dai J, Luo ZM, Liang SP (2005) Antinociceptive effects of intrathecally administered huwentoxin-I, a selective N-type calcium channel blocker, in the formalin test in conscious rats. Toxicon 45:15–20CrossRefPubMed Chen JQ, Zhang YQ, Dai J, Luo ZM, Liang SP (2005) Antinociceptive effects of intrathecally administered huwentoxin-I, a selective N-type calcium channel blocker, in the formalin test in conscious rats. Toxicon 45:15–20CrossRefPubMed
Zurück zum Zitat Del Pozo E, Rouiz-Garcia C, Bayens JM (1990) Analgesic effects of diltiazem and verapamil after central and peripheral administration in the hot-plate test. Gen Pharmacol 21:681–685CrossRefPubMed Del Pozo E, Rouiz-Garcia C, Bayens JM (1990) Analgesic effects of diltiazem and verapamil after central and peripheral administration in the hot-plate test. Gen Pharmacol 21:681–685CrossRefPubMed
Zurück zum Zitat Eaton MJ, Santiago DI, Dancausse HA, Whittemore SR (1997) Lumbar transplants of immortalized serotonergic neurons alleviates chronic neuropathic pain. Pain 72:59–69CrossRefPubMed Eaton MJ, Santiago DI, Dancausse HA, Whittemore SR (1997) Lumbar transplants of immortalized serotonergic neurons alleviates chronic neuropathic pain. Pain 72:59–69CrossRefPubMed
Zurück zum Zitat Eddy NB, Leimbach D (1953) Synthetic analgesics II Dithienylbutenyland dithienylbutylamines. J Pharmacol Exp Ther 107:385–393PubMed Eddy NB, Leimbach D (1953) Synthetic analgesics II Dithienylbutenyland dithienylbutylamines. J Pharmacol Exp Ther 107:385–393PubMed
Zurück zum Zitat Eisenach JC, Zhang Y, Duflo F (2005) Alpha2-adrenoceptors inhibit the intracellular Ca2+ response to electrical stimulation in normal and injured sensory neurons, with increased inhibition of calcitonin gene-related peptide expressing neurons after injury. Neuroscience 131:187–197CrossRef Eisenach JC, Zhang Y, Duflo F (2005) Alpha2-adrenoceptors inhibit the intracellular Ca2+ response to electrical stimulation in normal and injured sensory neurons, with increased inhibition of calcitonin gene-related peptide expressing neurons after injury. Neuroscience 131:187–197CrossRef
Zurück zum Zitat Evans RC, Morera-Herreras T, Cui Y, Du K, Sheehan T, Kotaleski JH, Venance L, Blackwell KT (2012) The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium neruons. PLoS Comput Biol 8:e1002493CrossRefPubMedPubMedCentral Evans RC, Morera-Herreras T, Cui Y, Du K, Sheehan T, Kotaleski JH, Venance L, Blackwell KT (2012) The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium neruons. PLoS Comput Biol 8:e1002493CrossRefPubMedPubMedCentral
Zurück zum Zitat Friel DD, Tsien RW (1992) A caffeine- and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurones modulates effects of Ca2+ entry on [Ca2+]i. J Physiol 450:217–246CrossRefPubMedPubMedCentral Friel DD, Tsien RW (1992) A caffeine- and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurones modulates effects of Ca2+ entry on [Ca2+]i. J Physiol 450:217–246CrossRefPubMedPubMedCentral
Zurück zum Zitat Galeotti N, Bartolini A, Ghelardini C (2004) Role of intracellular calcium in acute thermal pain perception. Neuropharmacology 47:935–944CrossRefPubMed Galeotti N, Bartolini A, Ghelardini C (2004) Role of intracellular calcium in acute thermal pain perception. Neuropharmacology 47:935–944CrossRefPubMed
Zurück zum Zitat Ghosh A, Carnahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618–1623CrossRefPubMed Ghosh A, Carnahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618–1623CrossRefPubMed
Zurück zum Zitat Granados-Soto V, Argüelles CF, Ortiz MI (2002) The peripheral antinociceptive effect of resveratrol is associated with activation of potassium channels. Neuropharmacology 43:917–923CrossRefPubMed Granados-Soto V, Argüelles CF, Ortiz MI (2002) The peripheral antinociceptive effect of resveratrol is associated with activation of potassium channels. Neuropharmacology 43:917–923CrossRefPubMed
Zurück zum Zitat Guo ZY, Li CZ, Li XJ, Wang YL, Mattson MP, Lu CB (2013) The developmental regulation of glutamate receptor-mediated calcium signaling inprimary cultured rat hippocampal neurons. Neuroreport 24:492–497CrossRefPubMed Guo ZY, Li CZ, Li XJ, Wang YL, Mattson MP, Lu CB (2013) The developmental regulation of glutamate receptor-mediated calcium signaling inprimary cultured rat hippocampal neurons. Neuroreport 24:492–497CrossRefPubMed
Zurück zum Zitat Hafeshjani ZK, Karami M, Biglarnia M (2012) Nitric oxide in the hippocampal cortical area interacts with naloxone in inducing pain. Indian J Pharmacol 44:443–447CrossRefPubMedPubMedCentral Hafeshjani ZK, Karami M, Biglarnia M (2012) Nitric oxide in the hippocampal cortical area interacts with naloxone in inducing pain. Indian J Pharmacol 44:443–447CrossRefPubMedPubMedCentral
Zurück zum Zitat Haley TJ, McCormick WG (1957) Pharmacological effects produced by interacerebral injections of drugs in the conscious mouse. Br J Pharmacol 12(1):12–15 Haley TJ, McCormick WG (1957) Pharmacological effects produced by interacerebral injections of drugs in the conscious mouse. Br J Pharmacol 12(1):12–15
Zurück zum Zitat Han J, Kwon M, Cha M, Tanioka M, Hong SK, Bai SJ, Lee BH (2015) Plasticity-related PKMζ signaling in the insular cortex is involved in the modulation of neuropathic pain after nerve injury. Neural Plast 2015:601767PubMedPubMedCentral Han J, Kwon M, Cha M, Tanioka M, Hong SK, Bai SJ, Lee BH (2015) Plasticity-related PKMζ signaling in the insular cortex is involved in the modulation of neuropathic pain after nerve injury. Neural Plast 2015:601767PubMedPubMedCentral
Zurück zum Zitat Harden RN (2005) Chronic neuropathic pain. Mechanisms, diagnosis, and treatment. Neurologist 11:111–122CrossRefPubMed Harden RN (2005) Chronic neuropathic pain. Mechanisms, diagnosis, and treatment. Neurologist 11:111–122CrossRefPubMed
Zurück zum Zitat Harris RA, Loh HH, Way EL (1975) Effects of divalent cations, cation chelators and an ionophore on morphine analgesia and tolerance. J Pharmcol Exp Ther 195:488–498 Harris RA, Loh HH, Way EL (1975) Effects of divalent cations, cation chelators and an ionophore on morphine analgesia and tolerance. J Pharmcol Exp Ther 195:488–498
Zurück zum Zitat Heinke B, Balzer E, Sandkuhler J (2004) Pre- and postsynaptic contributions of voltage-dependent Ca2+ channels to nociceptive transmission in rat spinal lamina I neurons. Eur J Neurosci 19:103–111CrossRefPubMed Heinke B, Balzer E, Sandkuhler J (2004) Pre- and postsynaptic contributions of voltage-dependent Ca2+ channels to nociceptive transmission in rat spinal lamina I neurons. Eur J Neurosci 19:103–111CrossRefPubMed
Zurück zum Zitat Horiguchi N, Ago Y, Asada K, Kita Y, Hiramatsu N, Takuma K, Matsuda T (2013) Involvement of spinal 5-HT1A receptors in isolation rearing-induced hypoalgesia in mice. Psychopharmacology (Berl) 227:251–261CrossRef Horiguchi N, Ago Y, Asada K, Kita Y, Hiramatsu N, Takuma K, Matsuda T (2013) Involvement of spinal 5-HT1A receptors in isolation rearing-induced hypoalgesia in mice. Psychopharmacology (Berl) 227:251–261CrossRef
Zurück zum Zitat Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275:218–220CrossRefPubMed Jang M, Cai L, Udeani GO, Slowing KV, Thomas CF, Beecher CW, Fong HH, Farnsworth NR, Kinghorn AD, Mehta RG, Moon RC, Pezzuto JM (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275:218–220CrossRefPubMed
Zurück zum Zitat Kakunaga T, Kaneto H, Hano K (1966) Pharmacologic studies on analgesics. VII. Significance of the calcium ion in morphine analgesia. J Pharmacol Exp Ther 153:134–141PubMed Kakunaga T, Kaneto H, Hano K (1966) Pharmacologic studies on analgesics. VII. Significance of the calcium ion in morphine analgesia. J Pharmacol Exp Ther 153:134–141PubMed
Zurück zum Zitat Kolarow R, Brigadski T, Lessmann V (2007) Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J Neurosci 27:10350–10364CrossRefPubMed Kolarow R, Brigadski T, Lessmann V (2007) Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J Neurosci 27:10350–10364CrossRefPubMed
Zurück zum Zitat Liang JH, Wang XH, Liu RK, Sun HL, Ye XF, Zheng JW (2003) Buspirone-induced antinociception is mediated by L-type calcium channels and calcium/caffeine-sensitive pools in mice. Psychopharmacology (Berl) 166:276–283CrossRef Liang JH, Wang XH, Liu RK, Sun HL, Ye XF, Zheng JW (2003) Buspirone-induced antinociception is mediated by L-type calcium channels and calcium/caffeine-sensitive pools in mice. Psychopharmacology (Berl) 166:276–283CrossRef
Zurück zum Zitat Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175–190CrossRefPubMed Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci 3:175–190CrossRefPubMed
Zurück zum Zitat MacCarrone M, Lorenzon T, Guerrieri P, Agro AF (1999) Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity. Eur J Biochem 265:27–34CrossRefPubMed MacCarrone M, Lorenzon T, Guerrieri P, Agro AF (1999) Resveratrol prevents apoptosis in K562 cells by inhibiting lipoxygenase and cyclooxygenase activity. Eur J Biochem 265:27–34CrossRefPubMed
Zurück zum Zitat Mahani SE, Motamedi F, Ahmadiani A (2006) Involvement of hypothalamic pituitary adrenal axis on the nifedipine-induced antinociception and tolerance in rats. Pharmacol Biochem Behav 85:422–427CrossRefPubMed Mahani SE, Motamedi F, Ahmadiani A (2006) Involvement of hypothalamic pituitary adrenal axis on the nifedipine-induced antinociception and tolerance in rats. Pharmacol Biochem Behav 85:422–427CrossRefPubMed
Zurück zum Zitat da Matta CB, de Souza ET, de Queiroz AC, de Lira DP, de Araújo MV, Cavalcante-Silva LH, de Miranda GE, de Araújo-Júnior JX, Barbosa-Filho JM, de Oliveira Santos BV, Alexandre-Moreira MS (2011) Antinociceptive and anti-inflammatory activity from algae of the genus Caulerpa. Mar Drugs 9:307–318CrossRefPubMedPubMedCentral da Matta CB, de Souza ET, de Queiroz AC, de Lira DP, de Araújo MV, Cavalcante-Silva LH, de Miranda GE, de Araújo-Júnior JX, Barbosa-Filho JM, de Oliveira Santos BV, Alexandre-Moreira MS (2011) Antinociceptive and anti-inflammatory activity from algae of the genus Caulerpa. Mar Drugs 9:307–318CrossRefPubMedPubMedCentral
Zurück zum Zitat McPherson PS, Kim YK, Valdivia H, Knudson CM, Takekura H, Franzini-Armstrong C, Coronado R, Campbell KP (1991) The brain ryanodine receptor: a caffeine-sensitive Caclium release channel. Neuron 7:17–25CrossRefPubMed McPherson PS, Kim YK, Valdivia H, Knudson CM, Takekura H, Franzini-Armstrong C, Coronado R, Campbell KP (1991) The brain ryanodine receptor: a caffeine-sensitive Caclium release channel. Neuron 7:17–25CrossRefPubMed
Zurück zum Zitat Miranda HF, Pelissier T, Sierralta F (1993) Analgesic effects of intracerebroventricular administration of calcium channel blockers in mice. Gen Pharmacol 24:201–204CrossRefPubMed Miranda HF, Pelissier T, Sierralta F (1993) Analgesic effects of intracerebroventricular administration of calcium channel blockers in mice. Gen Pharmacol 24:201–204CrossRefPubMed
Zurück zum Zitat Mullin GE (2011) Red wine, grapes, and better health-resveratrol. Nutr Clin Pract 26:722–723CrossRefPubMed Mullin GE (2011) Red wine, grapes, and better health-resveratrol. Nutr Clin Pract 26:722–723CrossRefPubMed
Zurück zum Zitat Ogawa A, Dai Y, Yamanaka H, Iwata K, Niwa H, Noguchi K (2005) Ca(2+)/calmodulin-protein kinase IIalpha in the trigeminal subnucleus caudalis contributes to neuropathic pain following inferior alveolar nerve transection. Exp Neurol 192:310–319CrossRefPubMed Ogawa A, Dai Y, Yamanaka H, Iwata K, Niwa H, Noguchi K (2005) Ca(2+)/calmodulin-protein kinase IIalpha in the trigeminal subnucleus caudalis contributes to neuropathic pain following inferior alveolar nerve transection. Exp Neurol 192:310–319CrossRefPubMed
Zurück zum Zitat Orallo F (2006) Comparative studies of the antioxidant effects of cis- and trans-resveratrol. Curr Med Chem 13:87–98CrossRefPubMed Orallo F (2006) Comparative studies of the antioxidant effects of cis- and trans-resveratrol. Curr Med Chem 13:87–98CrossRefPubMed
Zurück zum Zitat Prado WA (2001) Involvement of calcium in pain and antinociception. Braz J Med Biol Res 34:449–461CrossRefPubMed Prado WA (2001) Involvement of calcium in pain and antinociception. Braz J Med Biol Res 34:449–461CrossRefPubMed
Zurück zum Zitat Rousseau E, Smith JS, Meissner G (1987) Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Phys 253:C364–C368 Rousseau E, Smith JS, Meissner G (1987) Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Phys 253:C364–C368
Zurück zum Zitat Russo GL (2007) Ins and outs of dietary phytochemicals in cancer chemoprevention. Biochem Pharmacol 74:533–544CrossRefPubMed Russo GL (2007) Ins and outs of dietary phytochemicals in cancer chemoprevention. Biochem Pharmacol 74:533–544CrossRefPubMed
Zurück zum Zitat Saeki K, Obi I, Ogiku N, Hakamata Y, Matsumoto T (1998) Characterization of brain-type ryanodine receptor permanently expressed in Chinese hamster ovary cells. Life Sci 63:575–588CrossRefPubMed Saeki K, Obi I, Ogiku N, Hakamata Y, Matsumoto T (1998) Characterization of brain-type ryanodine receptor permanently expressed in Chinese hamster ovary cells. Life Sci 63:575–588CrossRefPubMed
Zurück zum Zitat Sałat K, Jakubowska A, Kulig K (2014) Zucapsaicin for the treatment of neuropathic pain. Expert Opin Investig Drugs 23:1433–1440CrossRefPubMed Sałat K, Jakubowska A, Kulig K (2014) Zucapsaicin for the treatment of neuropathic pain. Expert Opin Investig Drugs 23:1433–1440CrossRefPubMed
Zurück zum Zitat Schmidt WK, Way EL (1980) Hyperalgesic effects of divalent cations and antinociceptive effects of a calcium chelator in naive and morphine-dependent mice. J Pharmacol Exp Ther 212:22–27PubMed Schmidt WK, Way EL (1980) Hyperalgesic effects of divalent cations and antinociceptive effects of a calcium chelator in naive and morphine-dependent mice. J Pharmacol Exp Ther 212:22–27PubMed
Zurück zum Zitat Sharma S, Kulkarni SK, Chopra K (2007) Effect of resveratrol, a polyphenolic phytoalexin, on thermal hyperalgesia in a mouse model of diabetic neuropathic pain. Fundam Clin Pharmacol 21:89–94CrossRefPubMed Sharma S, Kulkarni SK, Chopra K (2007) Effect of resveratrol, a polyphenolic phytoalexin, on thermal hyperalgesia in a mouse model of diabetic neuropathic pain. Fundam Clin Pharmacol 21:89–94CrossRefPubMed
Zurück zum Zitat Shirahama M, Ushio S, Egashira N, Yamamoto S, Sada H, Masuguchi K, Kawashiri T, Oishi R (2012) Inhibition of Ca2+/calmodulin-dependent protein kinase II reverses oxaliplatin-induced mechanical allodynia in rats. Mol Pain 8:26CrossRefPubMedPubMedCentral Shirahama M, Ushio S, Egashira N, Yamamoto S, Sada H, Masuguchi K, Kawashiri T, Oishi R (2012) Inhibition of Ca2+/calmodulin-dependent protein kinase II reverses oxaliplatin-induced mechanical allodynia in rats. Mol Pain 8:26CrossRefPubMedPubMedCentral
Zurück zum Zitat Smith FL, Stevens DL (1995) Calcium modulation of morphine analgesia: role of calcium channels and intracellular pool calcium. J Pharmacol Exp Ther 272:290–299PubMed Smith FL, Stevens DL (1995) Calcium modulation of morphine analgesia: role of calcium channels and intracellular pool calcium. J Pharmacol Exp Ther 272:290–299PubMed
Zurück zum Zitat Subbaramaiah K, Chung WJ, Michaluart P, Telang N, Tanabe T, Inoue H, Jang M, Pezzuto JM, Dannenberg AJ (1998) Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J Biol Chem 273:21875–21882CrossRefPubMed Subbaramaiah K, Chung WJ, Michaluart P, Telang N, Tanabe T, Inoue H, Jang M, Pezzuto JM, Dannenberg AJ (1998) Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J Biol Chem 273:21875–21882CrossRefPubMed
Zurück zum Zitat Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726CrossRefPubMed Tao X, Finkbeiner S, Arnold DB, Shaywitz AJ, Greenberg ME (1998) Ca2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 20:709–726CrossRefPubMed
Zurück zum Zitat Todorovic SM, Pathirathna S, Meyenburg A, Jevtovic-Todorovic V (2004) Mechanical and thermal anti-nociception in rats after systemic administration of verapamil. Neurosci Lett 360:57–60CrossRefPubMed Todorovic SM, Pathirathna S, Meyenburg A, Jevtovic-Todorovic V (2004) Mechanical and thermal anti-nociception in rats after systemic administration of verapamil. Neurosci Lett 360:57–60CrossRefPubMed
Zurück zum Zitat Venegas H, Schaible H (2000) Effects of antagonists to high threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85:9–18CrossRef Venegas H, Schaible H (2000) Effects of antagonists to high threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85:9–18CrossRef
Zurück zum Zitat Vocci FJ, Welch SP, Dewey WL (1980) Differential effects of divalent cation, cation chelators and an ionophore (A23187) on morphine and dibutyryl guanosine 3′: 5′-cyclic monophosphate antinociception. J Pharmacol Exp Ther 214:463–466PubMed Vocci FJ, Welch SP, Dewey WL (1980) Differential effects of divalent cation, cation chelators and an ionophore (A23187) on morphine and dibutyryl guanosine 3′: 5′-cyclic monophosphate antinociception. J Pharmacol Exp Ther 214:463–466PubMed
Zurück zum Zitat Wang JF, Han SP, Lu Z, Wang XJ, Han JS, Ren MF (1989) Effect of calcium ion on analgesia of opioid peptides. Int J Neurosci 47(3–4):279–285CrossRefPubMed Wang JF, Han SP, Lu Z, Wang XJ, Han JS, Ren MF (1989) Effect of calcium ion on analgesia of opioid peptides. Int J Neurosci 47(3–4):279–285CrossRefPubMed
Zurück zum Zitat Weiss N, De Waard M (2006) Voltage-dependent calcium channels at the heart of pain perception. Med Sci (Paris) 22:396–404CrossRef Weiss N, De Waard M (2006) Voltage-dependent calcium channels at the heart of pain perception. Med Sci (Paris) 22:396–404CrossRef
Zurück zum Zitat Wigestrand MB, Fonnum F, Ivar WS (2012) Subunit-specific modulation of [(3)H]MK-801 binding to NMDA receptors mediated by dopamine receptor ligands in rodent brain. Neurochem Int 61:266–276CrossRefPubMed Wigestrand MB, Fonnum F, Ivar WS (2012) Subunit-specific modulation of [(3)H]MK-801 binding to NMDA receptors mediated by dopamine receptor ligands in rodent brain. Neurochem Int 61:266–276CrossRefPubMed
Zurück zum Zitat Wong CH, Wu WH, Zbuzek VK (1998) Hypotension does not alter the antinociceptive effect of nifedipine. Life Sci 63:343–348CrossRef Wong CH, Wu WH, Zbuzek VK (1998) Hypotension does not alter the antinociceptive effect of nifedipine. Life Sci 63:343–348CrossRef
Zurück zum Zitat Xu Y, Wang Z, You W, Zhang X, Li S, Barish PA, Vernon MM, Du X, Li G, Pan J, Ogle WO (2010) Antidepressant-like effect of trans-resveratrol: involvement of serotonin and noradrenaline system. Eur Neuropsychopharmacol 20:405–413CrossRefPubMed Xu Y, Wang Z, You W, Zhang X, Li S, Barish PA, Vernon MM, Du X, Li G, Pan J, Ogle WO (2010) Antidepressant-like effect of trans-resveratrol: involvement of serotonin and noradrenaline system. Eur Neuropsychopharmacol 20:405–413CrossRefPubMed
Zurück zum Zitat Yin Q, Lu FF, Zhao Y, Cheng MY, Fan Q, Cui J, Liu L, Cheng W, Yan CD (2013) Resveratrol facilitates pain attenuation in a rat model of neuropathic pain through the activation of spinal Sirt1. Reg Anesth Pain Med 38:93–99CrossRefPubMed Yin Q, Lu FF, Zhao Y, Cheng MY, Fan Q, Cui J, Liu L, Cheng W, Yan CD (2013) Resveratrol facilitates pain attenuation in a rat model of neuropathic pain through the activation of spinal Sirt1. Reg Anesth Pain Med 38:93–99CrossRefPubMed
Zurück zum Zitat Zhao X, Xu Y, Zhao Q, Chen CR, Liu AM, Huang ZL (2012) Curcumin exerts antinociceptive effects in a mouse model of neuropathic pain: descending monoamine system and opioid receptors are differentially involved. Neuropharmacology 62:843–854CrossRefPubMed Zhao X, Xu Y, Zhao Q, Chen CR, Liu AM, Huang ZL (2012) Curcumin exerts antinociceptive effects in a mouse model of neuropathic pain: descending monoamine system and opioid receptors are differentially involved. Neuropharmacology 62:843–854CrossRefPubMed
Metadaten
Titel
The analgesic effect of trans-resveratrol is regulated by calcium channels in the hippocampus of mice
verfasst von
Weijie Wang
Yingcong Yu
Jing Li
Lin Wang
Zhi Li
Chong Zhang
Linlin Zhen
Lianshu Ding
Gang Wang
Xiaoyang Sun
Ying Xu
Publikationsdatum
12.06.2017
Verlag
Springer US
Erschienen in
Metabolic Brain Disease / Ausgabe 4/2017
Print ISSN: 0885-7490
Elektronische ISSN: 1573-7365
DOI
https://doi.org/10.1007/s11011-017-0033-1

Weitere Artikel der Ausgabe 4/2017

Metabolic Brain Disease 4/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Akuter Schwindel: Wann lohnt sich eine MRT?

28.04.2024 Schwindel Nachrichten

Akuter Schwindel stellt oft eine diagnostische Herausforderung dar. Wie nützlich dabei eine MRT ist, hat eine Studie aus Finnland untersucht. Immerhin einer von sechs Patienten wurde mit akutem ischämischem Schlaganfall diagnostiziert.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Frühe Alzheimertherapie lohnt sich

25.04.2024 AAN-Jahrestagung 2024 Nachrichten

Ist die Tau-Last noch gering, scheint der Vorteil von Lecanemab besonders groß zu sein. Und beginnen Erkrankte verzögert mit der Behandlung, erreichen sie nicht mehr die kognitive Leistung wie bei einem früheren Start. Darauf deuten neue Analysen der Phase-3-Studie Clarity AD.

Viel Bewegung in der Parkinsonforschung

25.04.2024 Parkinson-Krankheit Nachrichten

Neue arznei- und zellbasierte Ansätze, Frühdiagnose mit Bewegungssensoren, Rückenmarkstimulation gegen Gehblockaden – in der Parkinsonforschung tut sich einiges. Auf dem Deutschen Parkinsonkongress ging es auch viel um technische Innovationen.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.