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Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line

Year 2019, Volume: 11 Issue: 1, 815 - 824, 18.06.2019
https://doi.org/10.37212/jcnos.653500

Abstract

Cisplatin (CSP) is used treatment of several cancers. However, it has also adverse effect through excessive reactive oxygen species production and activation of TRPV1 channel activation in neurons. Pregabalin (PGAB) has antioxidant and calcium channel blocker actions in neurons. I have investigated protective role of PGAB against the adverse effects of CSP in DBTRG neuronal cells. The neuronal cells were divided into four groups as control group, PGAB group (500 M for 24 1 hrs), CSP group (25 M for 24 hrs), and PGAB+CSP combination group. CISP-induced decrease of cell viability, glutathione peroxidase and glutathione level in the cells were increased in the neurons by PGAB treatment. However, CSP-induced increase of apoptosis, Ca2+ fluorescence intensity, TRPV1 current densities through the increase mitochondrial oxidative stress were decreased in the neurons by PGAB treatment. In conclusion, CSP-induced increases in mitochondrial ROS and cell death levels in the neuronal cells were decreased through the decrease of TRPV1 activation with the effect of PGAB treatment. CSP-induced drug resistance in the neurons might be reduced by PGAB treatment.

Supporting Institution

BSN Health, Analyses, Innovation, Consultancy, Organization, Agriculture, Industry and Trade Limited Company, Göller Bölgesi Teknokenti, Isparta, Turkey

Project Number

Project No: 2018-17

Thanks

The authors wish to thanks technicians Fatih Şahin and Hulusi Gül (BSN Health, Analyses, Innovation, Consultancy, Organization, Agriculture, Industry and Trade Limited Company, Göller Bölgesi Teknokenti, Isparta, Turkey) for helping patch-clamp and laser confocal microscopy analyses.

References

  • Al-Massri KF, Ahmed LA, El-Abhar HS. (2018). Pregabalin and lacosamide ameliorate paclitaxel-induced peripheral neuropathy via inhibition of JAK/STAT signaling pathway and Notch-1 receptor. Neurochem Internat 120:164-171.
  • Aslankoc R, Savran M, Ozmen O, Asci S. (2018). Hippocampus and cerebellum damage in sepsis induced by lipopolysaccharide in aged rats - Pregabalin can prevent damage. Biomedicine and Pharmacotherapy 108:1384-1392.
  • Ataizi ZS, Ertilav K, Nazıroğlu M. 2019. Mitochondrial oxidative stress-induced brain and hippocampus apoptosis decrease through modulation of caspase activity, Ca(2+) influx and inflammatory cytokine molecular pathways in the docetaxel-treated mice by melatonin and selenium treatments. Metab Brain Dis. 34(4):1077-1089.
  • Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816-24.
  • Chen C, Zhang H, Xu H, Zheng Y, Wu T, Lian Y. (2019). Ginsenoside Rb1 ameliorates cisplatin-induced learning and memory impairments. J Ginseng Res. 43(4):499-507.
  • Clapham DE. (2003). TRP channels as cellular sensors. Nature 426(6966):517-524.
  • Gavva NR, Tamir R, Qu Y, Klionsky L, Zhang TJ, Immke D, Wang J, Zhu D, Vanderah TW, Porreca F, Doherty EM, Norman MH, Wild KD, Bannon AW, Louis JC, Treanor JJ. (2005). AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. J Pharmacol Exp Ther. 313(1):474-484.
  • Gökçe Kütük S, Gökçe Kütük M, Gürses Cila HE, Nazıroğlu M. (2019). Curcumin enhances cisplatin-induced human laryngeal squamous cancer cell death through activation of TRPM2 channel and mitochondrial oxidative stress. Sci Rep. 28;9(1):17784. Han FY, Kuo A, Nicholson JR, Corradinni L, Smith MT. (2018). Comparative analgesic efficacy of pregabalin administered according to either a prevention protocol or an intervention protocol in rats with cisplatin-induced peripheral neuropathy. Clin Exp Pharmacol Physiol. 45(10):1067-1075. Ho KW, Ward NJ, Calkins DJ. (2012). TRPV1: a stress response protein in the central nervous system. Am J Neurodegener Dis. 1(1):1-14. Joshi DC, Bakowska JC. 2011. Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Vis Exp 51: 2704. Kaur S, Muthuraman A. (2019). Ameliorative effect of gallic acid in paclitaxel-induced neuropathic pain in mice. Toxicol Rep 6:505-513. Kazanci B, Ozdogan S, Kahveci R, Gokce EC, Yigitkanli K, Gokce A, Erdogan B. (2017). Neuroprotective effects of pregabalin against spinal cord ischemia-reperfusion injury in rats. Turk Neurosurg. 27(6):952-961. Keil VC, Funke F, Zeug A, Schild D, Müller M. 2011. Ratiometric high-resolution imaging of JC-1 fluorescence reveals the subcellular heterogeneity of astrocytic mitochondria. Pflugers Arch. 462:693-708. Khasabova IA, Khasabov SG, Olson JK, Uhelski ML, Kim AH, Albino-Ramírez AM, Wagner CL, Seybold VS, Simone DA. (2019). Pioglitazone, a PPARγ agonist, reduces cisplatin-evoked neuropathic pain by protecting against oxidative stress. Pain 160(3):688-701. Lawrence RA, Burk RF. 1976. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952-958. Marmolino D, Manto M. (2010). Pregabalin antagonizes copper-induced toxicity in the brain: in vitro and in vivo studies. Neurosignals 18(4):210-222. Marwaha L, Bansal Y, Singh R, Saroj P, Sodhi RK, Kuhad A. (2016). Niflumic acid, a TRPV1 channel modulator, ameliorates stavudine-induced neuropathic pain. Inflammopharm. 24(6):319-334. Nam E, Han J, Suh JM, Yi Y, Lim MH. (2018). Link of impaired metal ion homeostasis to mitochondrial dysfunction in neurons. Curr Opin Chem Biol. 43:8-14. Nazıroğlu M, Braidy N. (2017). Thermo-sensitive TRP channels: Novel targets for treating chemotherapy-induced peripheral pain. Front Physiol. 8:1040. Nazıroğlu M, Ciğ B, Ozgül C. (2013). Neuroprotection induced by N-acetylcysteine against cytosolic glutathione depletion-induced Ca2+ influx in dorsal root ganglion neurons of mice: role of TRPV1 channels. Neuroscience 242:151-160. Nazıroğlu M. (2012). Molecular role of catalase on oxidative stress-induced Ca(2+) signaling and TRP cation channel activation in nervous system. J Recept Signal Transduct Res. 32(3):134-141. Nazıroğlu M. (2015). TRPV1 channel: A potential drug target for treating epilepsy. Current Neuropharmacology 13:239-247. Nur G, Nazıroğlu M, Deveci HA. (2017). Synergic prooxidant, apoptotic and TRPV1 channel activator effects of alpha-lipoic acid and cisplatin in MCF-7 breast cancer cells. J Recept Signal Transduct Res. 37(6):569-577. Övey IS, Naziroğlu M. (2015). Homocysteine and cytosolic GSH depletion induce apoptosis and oxidative toxicity through cytosolic calcium overload in the hippocampus of aged mice: involvement of TRPM2 and TRPV1 channels. Neuroscience 284:225-233. Piccolini VM, Bottone MG, Bottiroli G, De Pascali SA, Fanizzi FP, Bernocchi G. (2013). Platinum drugs and neurotoxicity: effects on intracellular calcium homeostasis. Cell Biol Toxicol. 29(5):339-353. Placer ZA, Cushman L, Johnson BC. 1966. Estimation of products of lipid peroxidation (malonyl dialdehyde) in biological fluids. Anal Biochem 16:359-364. Popović J, Klajn A, Paunesku T, Ma Q, Chen S, Lai B, Stevanović M, Woloschak GE. (2019). Neuroprotective role of selected antioxidant agents in preventing cisplatin-induced damage of human neurons In Vitro. Cell Mol Neurobiol. 39(5):619-636. Sakallı Çetin E, Nazıroğlu M, Çiğ B, Övey İS, Aslan Koşar P. (2017). Selenium potentiates the anticancer effect of cisplatin against oxidative stress and calcium ion signaling-induced intracellular toxicity in MCF-7 breast cancer cells: Involvement of the TRPV1 channel. J Recept Signal Transduct Res. 37:84-93. Sasaki A, Mizoguchi S, Kagaya K, Shiro M, Sakai A, Andoh T, Kino Y, Taniguchi H, Saito Y, Takahata H, Kuraishi Y. (2014). A mouse model of peripheral postischemic dysesthesia: involvement of reperfusion-induced oxidative stress and TRPA1 channel. J Pharm Sci. 351(3):568-575. Schweizer U, Bräuer AU, Köhrle J, Nitsch R, Savaskan NE. (2004). Selenium and brain function: a poorly recognized liaison. Brain Res Brain Res Rev. 45(3):164-178. Sedlak J, Lindsay RHC. 1968. Estimation of total, protein bound and non-protein sulfhydryl groups in tissue with Ellmann' s reagent. Anal Biochem 25:192-205. Seto Y, Takase M, Tsuji Y, To H. (2017). Pregabalin reduces cisplatin-induced mechanical allodynia in rats. J Pharmacol Sci. 134(3):175-180. Shim HS, Bae C, Wang J, Lee KH, Hankerd KM, Kim HK, Chung JM, La JH. (2019). Peripheral and central oxidative stress in chemotherapy-induced neuropathic pain. Mol Pain 15:1744806919840098. Staff NP, Cavaletti G, Islam B, Lustberg M, Psimaras D, Tamburin S. (2019). Platinum-induced peripheral neurotoxicity: From pathogenesis to treatment. J Peripher Nerv Syst 24 Suppl 2:S26-S39. Tomić M, Pecikoza U, Micov A, Vučković S, Stepanović-Petrović R. (2018). Antiepileptic drugs as analgesics/adjuvants in inflammatory pain: current preclinical evidence. Pharm Ther 192:42-64. Xie Q, Xu Y, Gao W, Zhang Y, Su J, Liu Y, Guo Y, Dou M, Hu K, Sun L. (2018). TAT fused IP3R derived peptide enhances cisplatin sensitivity of ovarian cancer cells by increasing ER Ca2+ release. Int J Mol Med. 41(2):809-817. Yakubov E, Buchfelder M, Eyüpoglu IY, Savaskan NE. 2014. Selenium action in neuro-oncology. Biol Trace Elem Res. 161(3):246-254. Yüksel E, Nazıroğlu M, Şahin M, Çiğ B. (2017). Involvement of TRPM2 and TRPV1 channels on hyperalgesia, apoptosis and oxidative stress in rat fibromyalgia model: Protective role of selenium. Sci Rep 7(1):17543.
Year 2019, Volume: 11 Issue: 1, 815 - 824, 18.06.2019
https://doi.org/10.37212/jcnos.653500

Abstract

Project Number

Project No: 2018-17

References

  • Al-Massri KF, Ahmed LA, El-Abhar HS. (2018). Pregabalin and lacosamide ameliorate paclitaxel-induced peripheral neuropathy via inhibition of JAK/STAT signaling pathway and Notch-1 receptor. Neurochem Internat 120:164-171.
  • Aslankoc R, Savran M, Ozmen O, Asci S. (2018). Hippocampus and cerebellum damage in sepsis induced by lipopolysaccharide in aged rats - Pregabalin can prevent damage. Biomedicine and Pharmacotherapy 108:1384-1392.
  • Ataizi ZS, Ertilav K, Nazıroğlu M. 2019. Mitochondrial oxidative stress-induced brain and hippocampus apoptosis decrease through modulation of caspase activity, Ca(2+) influx and inflammatory cytokine molecular pathways in the docetaxel-treated mice by melatonin and selenium treatments. Metab Brain Dis. 34(4):1077-1089.
  • Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. (1997). The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389(6653):816-24.
  • Chen C, Zhang H, Xu H, Zheng Y, Wu T, Lian Y. (2019). Ginsenoside Rb1 ameliorates cisplatin-induced learning and memory impairments. J Ginseng Res. 43(4):499-507.
  • Clapham DE. (2003). TRP channels as cellular sensors. Nature 426(6966):517-524.
  • Gavva NR, Tamir R, Qu Y, Klionsky L, Zhang TJ, Immke D, Wang J, Zhu D, Vanderah TW, Porreca F, Doherty EM, Norman MH, Wild KD, Bannon AW, Louis JC, Treanor JJ. (2005). AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. J Pharmacol Exp Ther. 313(1):474-484.
  • Gökçe Kütük S, Gökçe Kütük M, Gürses Cila HE, Nazıroğlu M. (2019). Curcumin enhances cisplatin-induced human laryngeal squamous cancer cell death through activation of TRPM2 channel and mitochondrial oxidative stress. Sci Rep. 28;9(1):17784. Han FY, Kuo A, Nicholson JR, Corradinni L, Smith MT. (2018). Comparative analgesic efficacy of pregabalin administered according to either a prevention protocol or an intervention protocol in rats with cisplatin-induced peripheral neuropathy. Clin Exp Pharmacol Physiol. 45(10):1067-1075. Ho KW, Ward NJ, Calkins DJ. (2012). TRPV1: a stress response protein in the central nervous system. Am J Neurodegener Dis. 1(1):1-14. Joshi DC, Bakowska JC. 2011. Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Vis Exp 51: 2704. Kaur S, Muthuraman A. (2019). Ameliorative effect of gallic acid in paclitaxel-induced neuropathic pain in mice. Toxicol Rep 6:505-513. Kazanci B, Ozdogan S, Kahveci R, Gokce EC, Yigitkanli K, Gokce A, Erdogan B. (2017). Neuroprotective effects of pregabalin against spinal cord ischemia-reperfusion injury in rats. Turk Neurosurg. 27(6):952-961. Keil VC, Funke F, Zeug A, Schild D, Müller M. 2011. Ratiometric high-resolution imaging of JC-1 fluorescence reveals the subcellular heterogeneity of astrocytic mitochondria. Pflugers Arch. 462:693-708. Khasabova IA, Khasabov SG, Olson JK, Uhelski ML, Kim AH, Albino-Ramírez AM, Wagner CL, Seybold VS, Simone DA. (2019). Pioglitazone, a PPARγ agonist, reduces cisplatin-evoked neuropathic pain by protecting against oxidative stress. Pain 160(3):688-701. Lawrence RA, Burk RF. 1976. Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952-958. Marmolino D, Manto M. (2010). Pregabalin antagonizes copper-induced toxicity in the brain: in vitro and in vivo studies. Neurosignals 18(4):210-222. Marwaha L, Bansal Y, Singh R, Saroj P, Sodhi RK, Kuhad A. (2016). Niflumic acid, a TRPV1 channel modulator, ameliorates stavudine-induced neuropathic pain. Inflammopharm. 24(6):319-334. Nam E, Han J, Suh JM, Yi Y, Lim MH. (2018). Link of impaired metal ion homeostasis to mitochondrial dysfunction in neurons. Curr Opin Chem Biol. 43:8-14. Nazıroğlu M, Braidy N. (2017). Thermo-sensitive TRP channels: Novel targets for treating chemotherapy-induced peripheral pain. Front Physiol. 8:1040. Nazıroğlu M, Ciğ B, Ozgül C. (2013). Neuroprotection induced by N-acetylcysteine against cytosolic glutathione depletion-induced Ca2+ influx in dorsal root ganglion neurons of mice: role of TRPV1 channels. Neuroscience 242:151-160. Nazıroğlu M. (2012). Molecular role of catalase on oxidative stress-induced Ca(2+) signaling and TRP cation channel activation in nervous system. J Recept Signal Transduct Res. 32(3):134-141. Nazıroğlu M. (2015). TRPV1 channel: A potential drug target for treating epilepsy. Current Neuropharmacology 13:239-247. Nur G, Nazıroğlu M, Deveci HA. (2017). Synergic prooxidant, apoptotic and TRPV1 channel activator effects of alpha-lipoic acid and cisplatin in MCF-7 breast cancer cells. J Recept Signal Transduct Res. 37(6):569-577. Övey IS, Naziroğlu M. (2015). Homocysteine and cytosolic GSH depletion induce apoptosis and oxidative toxicity through cytosolic calcium overload in the hippocampus of aged mice: involvement of TRPM2 and TRPV1 channels. Neuroscience 284:225-233. Piccolini VM, Bottone MG, Bottiroli G, De Pascali SA, Fanizzi FP, Bernocchi G. (2013). Platinum drugs and neurotoxicity: effects on intracellular calcium homeostasis. Cell Biol Toxicol. 29(5):339-353. Placer ZA, Cushman L, Johnson BC. 1966. Estimation of products of lipid peroxidation (malonyl dialdehyde) in biological fluids. Anal Biochem 16:359-364. Popović J, Klajn A, Paunesku T, Ma Q, Chen S, Lai B, Stevanović M, Woloschak GE. (2019). Neuroprotective role of selected antioxidant agents in preventing cisplatin-induced damage of human neurons In Vitro. Cell Mol Neurobiol. 39(5):619-636. Sakallı Çetin E, Nazıroğlu M, Çiğ B, Övey İS, Aslan Koşar P. (2017). Selenium potentiates the anticancer effect of cisplatin against oxidative stress and calcium ion signaling-induced intracellular toxicity in MCF-7 breast cancer cells: Involvement of the TRPV1 channel. J Recept Signal Transduct Res. 37:84-93. Sasaki A, Mizoguchi S, Kagaya K, Shiro M, Sakai A, Andoh T, Kino Y, Taniguchi H, Saito Y, Takahata H, Kuraishi Y. (2014). A mouse model of peripheral postischemic dysesthesia: involvement of reperfusion-induced oxidative stress and TRPA1 channel. J Pharm Sci. 351(3):568-575. Schweizer U, Bräuer AU, Köhrle J, Nitsch R, Savaskan NE. (2004). Selenium and brain function: a poorly recognized liaison. Brain Res Brain Res Rev. 45(3):164-178. Sedlak J, Lindsay RHC. 1968. Estimation of total, protein bound and non-protein sulfhydryl groups in tissue with Ellmann' s reagent. Anal Biochem 25:192-205. Seto Y, Takase M, Tsuji Y, To H. (2017). Pregabalin reduces cisplatin-induced mechanical allodynia in rats. J Pharmacol Sci. 134(3):175-180. Shim HS, Bae C, Wang J, Lee KH, Hankerd KM, Kim HK, Chung JM, La JH. (2019). Peripheral and central oxidative stress in chemotherapy-induced neuropathic pain. Mol Pain 15:1744806919840098. Staff NP, Cavaletti G, Islam B, Lustberg M, Psimaras D, Tamburin S. (2019). Platinum-induced peripheral neurotoxicity: From pathogenesis to treatment. J Peripher Nerv Syst 24 Suppl 2:S26-S39. Tomić M, Pecikoza U, Micov A, Vučković S, Stepanović-Petrović R. (2018). Antiepileptic drugs as analgesics/adjuvants in inflammatory pain: current preclinical evidence. Pharm Ther 192:42-64. Xie Q, Xu Y, Gao W, Zhang Y, Su J, Liu Y, Guo Y, Dou M, Hu K, Sun L. (2018). TAT fused IP3R derived peptide enhances cisplatin sensitivity of ovarian cancer cells by increasing ER Ca2+ release. Int J Mol Med. 41(2):809-817. Yakubov E, Buchfelder M, Eyüpoglu IY, Savaskan NE. 2014. Selenium action in neuro-oncology. Biol Trace Elem Res. 161(3):246-254. Yüksel E, Nazıroğlu M, Şahin M, Çiğ B. (2017). Involvement of TRPM2 and TRPV1 channels on hyperalgesia, apoptosis and oxidative stress in rat fibromyalgia model: Protective role of selenium. Sci Rep 7(1):17543.
There are 8 citations in total.

Details

Primary Language English
Subjects Neurosciences
Journal Section Original Articles
Authors

Kemal Ertilav

Project Number Project No: 2018-17
Publication Date June 18, 2019
Published in Issue Year 2019 Volume: 11 Issue: 1

Cite

APA Ertilav, K. (2019). Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line. Journal of Cellular Neuroscience and Oxidative Stress, 11(1), 815-824. https://doi.org/10.37212/jcnos.653500
AMA Ertilav K. Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line. J Cell Neurosci Oxid Stress. June 2019;11(1):815-824. doi:10.37212/jcnos.653500
Chicago Ertilav, Kemal. “Pregabalin Protected Cisplatin-Induced Oxidative Neurotoxicity in Neuronal Cell Line”. Journal of Cellular Neuroscience and Oxidative Stress 11, no. 1 (June 2019): 815-24. https://doi.org/10.37212/jcnos.653500.
EndNote Ertilav K (June 1, 2019) Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line. Journal of Cellular Neuroscience and Oxidative Stress 11 1 815–824.
IEEE K. Ertilav, “Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line”, J Cell Neurosci Oxid Stress, vol. 11, no. 1, pp. 815–824, 2019, doi: 10.37212/jcnos.653500.
ISNAD Ertilav, Kemal. “Pregabalin Protected Cisplatin-Induced Oxidative Neurotoxicity in Neuronal Cell Line”. Journal of Cellular Neuroscience and Oxidative Stress 11/1 (June 2019), 815-824. https://doi.org/10.37212/jcnos.653500.
JAMA Ertilav K. Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line. J Cell Neurosci Oxid Stress. 2019;11:815–824.
MLA Ertilav, Kemal. “Pregabalin Protected Cisplatin-Induced Oxidative Neurotoxicity in Neuronal Cell Line”. Journal of Cellular Neuroscience and Oxidative Stress, vol. 11, no. 1, 2019, pp. 815-24, doi:10.37212/jcnos.653500.
Vancouver Ertilav K. Pregabalin protected cisplatin-induced oxidative neurotoxicity in neuronal cell line. J Cell Neurosci Oxid Stress. 2019;11(1):815-24.

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