Omarigliptin Mitigates 6-Hydroxydopamine- or Rotenone-Induced Oxidative Toxicity in PC12 Cells by Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Actions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Cell Culture
2.3. Treatment of Cells
2.4. Measurement of Cell Viability
2.5. Measurement of Intracellular Reactive Oxygen Species (ROS) Levels
2.6. Measurement of DPPH Radical Scavenging Activity
2.7. Measurement of Lipid Peroxidation (LPO) in Rat Forebrain Homogenates
2.8. Measurement of Nitric Oxide (NO) Levels
2.9. Western Blotting
2.10. Transitory Transfection with Small Interfering RNA (siRNA)
2.11. Immunocytochemistry
2.12. Statistical Analysis
3. Results and Discussion
3.1. Effect of OMG on Viability of PC12 Cells
3.2. Effect of OMG on 6-OHDA- or Rotenone-Induced Toxicity in PC12 Cells
3.3. Effect of OMG on 6-OHDA- or Rotenone-Induced ROS Generation in PC12 Cells
3.4. Effects of OMG on DPPH Radical Formation and LPO
3.5. Effect of OMG on the Activation of Nrf2/HO-1 Signaling and Its Role in 6-OHDA- or Rotenone-Induced Toxicity in PC12 Cells
3.6. Effect of OMG on NO Production and iNOS Expression in 6-OHDA- or Rotenone-Treated PC12 Cells
3.7. Effect of OMG on 6-OHDA- or Rotenone-Induced Nuclear Translocation of NF-κB in PC12 Cells
3.8. Effect of OMG on Phosphorylation of Akt and Its Role in NF-κB Signaling in PC12 Cells
3.9. Effects of OMG on Expression of Apoptosis-Related Proteins in 6-OHDA- or Rotenone-Treated PC12 Cells
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mulvaney, C.A.; Duarte, G.S.; Handley, J.; Evans, D.J.; Menon, S.; Wyse, R.; Emsley, H.C. GLP-1 receptor agonists for Parkinson’s disease. Cochrane Database Syst. Rev. 2020, 7, Cd012990. [Google Scholar] [CrossRef]
- Ye, H.; Wei, J.; Tang, K.; Feuers, R.; Hong, H. Drug Repositioning Through Network Pharmacology. Curr. Top. Med. Chem. 2016, 16, 3646–3656. [Google Scholar] [CrossRef]
- Lu, Z.N.; Tian, B.; Guo, X.L. Repositioning of proton pump inhibitors in cancer therapy. Cancer Chemother. Pharmacol. 2017, 80, 925–937. [Google Scholar] [CrossRef]
- Corbett, A.; Williams, G.; Ballard, C. Drug repositioning in Alzheimer’s disease. Front. Biosci. 2015, 7, 184–188. [Google Scholar] [CrossRef]
- Wilkinson, G.F.; Pritchard, K. In vitro screening for drug repositioning. J. Biomol. Screen. 2015, 20, 167–179. [Google Scholar] [CrossRef]
- Kim, T.W. Drug repositioning approaches for the discovery of new therapeutics for Alzheimer’s disease. Neurotherapeutics 2015, 12, 132–142. [Google Scholar] [CrossRef]
- Seufert, J.; Gallwitz, B. The extra-pancreatic effects of GLP-1 receptor agonists: A focus on the cardiovascular, gastrointestinal and central nervous systems. Diabetes Obes. Metab. 2014, 16, 673–688. [Google Scholar] [CrossRef]
- Hong, C.T.; Chen, K.Y.; Wang, W.; Chiu, J.Y.; Wu, D.; Chao, T.Y.; Hu, C.J.; Chau, K.D.; Bamodu, O.A. Insulin Resistance Promotes Parkinson’s Disease through Aberrant Expression of α-Synuclein, Mitochondrial Dysfunction, and Deregulation of the Polo-Like Kinase 2 Signaling. Cells 2020, 9, 740. [Google Scholar] [CrossRef]
- Shannon, R.P. DPP-4 inhibition and neuroprotection: Do mechanisms matter? Diabetes 2013, 62, 1029–1031. [Google Scholar] [CrossRef]
- Martin, B.; Golden, E.; Carlson, O.D.; Pistell, P.; Zhou, J.; Kim, W.; Frank, B.P.; Thomas, S.; Chadwick, W.A.; Greig, N.H.; et al. Exendin-4 improves glycemic control, ameliorates brain and pancreatic pathologies, and extends survival in a mouse model of Huntington’s disease. Diabetes 2009, 58, 318–328. [Google Scholar] [CrossRef] [Green Version]
- Perry, T.; Lahiri, D.K.; Chen, D.; Zhou, J.; Shaw, K.T.; Egan, J.M.; Greig, N.H. A novel neurotrophic property of glucagon-like peptide 1: A promoter of nerve growth factor-mediated differentiation in PC12 cells. J. Pharmacol. Exp. Ther. 2002, 300, 958–966. [Google Scholar] [CrossRef]
- Erbil, D.; Eren, C.Y.; Demirel, C.; Küçüker, M.U.; Solaroğlu, I.; Eser, H.Y. GLP-1’s role in neuroprotection: A systematic review. Brain Inj. 2019, 33, 734–819. [Google Scholar] [CrossRef]
- Al-Badri, G.; Leggio, G.M.; Musumeci, G.; Marzagalli, R.; Drago, F.; Castorina, A. Tackling dipeptidyl peptidase IV in neurological disorders. Neural Regen. Res. 2018, 13, 26–34. [Google Scholar] [CrossRef]
- Chalichem, N.S.S.; Sai Kiran, P.S.S.; Basavan, D. Possible role of DPP4 inhibitors to promote hippocampal neurogenesis in Alzheimer’s disease. J. Drug Target. 2018, 26, 670–675. [Google Scholar] [CrossRef]
- Nassar, N.N.; Al-Shorbagy, M.Y.; Arab, H.H.; Abdallah, D.M. Saxagliptin: A novel antiparkinsonian approach. Neuropharmacology 2015, 89, 308–317. [Google Scholar] [CrossRef] [PubMed]
- Mima, A. Incretin-Based Therapy for Prevention of Diabetic Vascular Complications. J. Diabetes Res. 2016, 2016, 1379274. [Google Scholar] [CrossRef]
- Ashraghi, M.R.; Pagano, G.; Polychronis, S.; Niccolini, F.; Politis, M. Parkinson’s Disease, Diabetes and Cognitive Impairment. Recent Pat. Endocr. Metab. Immune Drug Discov. 2016, 10, 11–21. [Google Scholar] [CrossRef]
- DellaValle, B.; Brix, G.S.; Brock, B.; Gejl, M.; Rungby, J.; Larsen, A. Oral Administration of Sitagliptin Activates CREB and Is Neuroprotective in Murine Model of Brain Trauma. Front. Pharmacol. 2016, 7, 450. [Google Scholar] [CrossRef]
- Badawi, G.A.; Abd El Fattah, M.A.; Zaki, H.F.; El Sayed, M.I. Sitagliptin and liraglutide reversed nigrostriatal degeneration of rodent brain in rotenone-induced Parkinson’s disease. Inflammopharmacology 2017, 25, 369–382. [Google Scholar] [CrossRef]
- Nader, M.A.; Ateyya, H.; El-Shafey, M.; El-Sherbeeny, N.A. Sitagliptin enhances the neuroprotective effect of pregabalin against pentylenetetrazole-induced acute epileptogenesis in mice: Implication of oxidative, inflammatory, apoptotic and autophagy pathways. Neurochem. Int. 2018, 115, 11–23. [Google Scholar] [CrossRef]
- Abdelsalam, R.M.; Safar, M.M. Neuroprotective effects of vildagliptin in rat rotenone Parkinson’s disease model: Role of RAGE-NFκB and Nrf2-antioxidant signaling pathways. J. Neurochem. 2015, 133, 700–707. [Google Scholar] [CrossRef] [PubMed]
- Lin, C.L.; Huang, C.N. The neuroprotective effects of the anti-diabetic drug linagliptin against Aβ-induced neurotoxicity. Neural Regen. Res. 2016, 11, 236–237. [Google Scholar] [CrossRef] [PubMed]
- Duarte, A.I.; Candeias, E.; Correia, S.C.; Santos, R.X.; Carvalho, C.; Cardoso, S.; Plácido, A.; Santos, M.S.; Oliveira, C.R.; Moreira, P.I. Crosstalk between diabetes and brain: Glucagon-like peptide-1 mimetics as a promising therapy against neurodegeneration. Biochim. Biophys. Acta 2013, 1832, 527–541. [Google Scholar] [CrossRef] [PubMed]
- Shantikumar, S.; Satheeshkumar, N.; Srinivas, R. Pharmacokinetic and protein binding profile of peptidomimetic DPP-4 inhibitor—Teneligliptin in rats using liquid chromatography-tandem mass spectrometry. J. Chromatogr. B 2015, 1002, 194–200. [Google Scholar] [CrossRef]
- Evans, P.M.; Bain, S.C. Omarigliptin for the treatment of type 2 diabetes mellitus. Expert Opin. Pharmacother. 2016, 17, 1947–1952. [Google Scholar] [CrossRef]
- Ayoub, B.M.; Mowaka, S.; Safar, M.M.; Ashoush, N.; Arafa, M.G.; Michel, H.E.; Tadros, M.M.; Elmazar, M.M.; Mousa, S.A. Repositioning of Omarigliptin as a once-weekly intranasal Anti-parkinsonian Agent. Sci. Rep. 2018, 8, 8959. [Google Scholar] [CrossRef]
- Burness, C.B. Omarigliptin: First global approval. Drugs 2015, 75, 1947–1952. [Google Scholar] [CrossRef]
- Li, X.; Yin, Y.; Li, W.; Li, S.; Zhang, D.; Liu, Z. Omarigliptin alleviates cognitive dysfunction in Streptozotocin-induced diabetic mouse. Bioengineered 2022, 13, 9387–9396. [Google Scholar] [CrossRef]
- Kabel, A.M.; Arab, H.H.; Atef, A.; Estfanous, R.S. Omarigliptin/galangin combination mitigates lipopolysaccharide-induced neuroinflammation in rats: Involvement of glucagon-like peptide-1, toll-like receptor-4, apoptosis and Akt/GSK-3β signaling. Life Sci. 2022, 295, 120396. [Google Scholar] [CrossRef]
- Elkamhawy, A.; Woo, J.; Gouda, N.A.; Kim, J.; Nada, H.; Roh, E.J.; Park, K.D.; Cho, J.; Lee, K. Melatonin Analogues Potently Inhibit MAO-B and Protect PC12 Cells against Oxidative Stress. Antioxidants 2021, 10, 1604. [Google Scholar] [CrossRef]
- Walkinshaw, G.; Waters, C.M. Neurotoxin-induced cell death in neuronal PC12 cells is mediated by induction of apoptosis. Neuroscience 1994, 63, 975–987. [Google Scholar] [CrossRef]
- Nisticò, R.; Mehdawy, B.; Piccirilli, S.; Mercuri, N. Paraquat- and rotenone-induced models of Parkinson’s disease. Int. J. Immunopathol. Pharmacol. 2011, 24, 313–322. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Cao, L.; Ren, Y.; Jiang, Y.; Xie, W.; Li, D. GLP-1 receptor regulates cell growth through regulating IDE expression level in Aβ1-42-treated PC12 cells. Biosci. Rep. 2018, 38, BSR20171284. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Chen, S.; Xu, Z.; Chen, S.; Yao, W.; Gao, X. GLP-1 receptor agonists downregulate aberrant GnT-III expression in Alzheimer’s disease models through the Akt/GSK-3β/β-catenin signaling. Neuropharmacology 2018, 131, 190–199. [Google Scholar] [CrossRef]
- Elsherbeny, M.H.; Kim, J.; Gouda, N.A.; Gotina, L.; Cho, J.; Pae, A.N.; Lee, K.; Park, K.D.; Elkamhawy, A.; Roh, E.J. Highly Potent, Selective, and Competitive Indole-Based MAO-B Inhibitors Protect PC12 Cells against 6-Hydroxydopamine- and Rotenone-Induced Oxidative Stress. Antioxidants 2021, 10, 1641. [Google Scholar] [CrossRef]
- Lee, J.; Song, K.; Huh, E.; Oh, M.S.; Kim, Y.S. Neuroprotection against 6-OHDA toxicity in PC12 cells and mice through the Nrf2 pathway by a sesquiterpenoid from Tussilago farfara. Redox Biol. 2018, 18, 6–15. [Google Scholar] [CrossRef]
- Oh, Y.; Do, H.T.T.; Kim, S.; Kim, Y.M.; Chin, Y.W.; Cho, J. Memory-Enhancing Effects of Mangosteen Pericarp Water Extract through Antioxidative Neuroprotection and Anti-Apoptotic Action. Antioxidants 2020, 10, 34. [Google Scholar] [CrossRef]
- Lee, K.; Park, C.; Oh, Y.; Lee, H.; Cho, J. Antioxidant and Neuroprotective Effects of N-((3,4-Dihydro-2H-benzo[h]chromen-2-yl)methyl)-4-methoxyaniline in Primary Cultured Rat Cortical Cells: Involvement of ERK-CREB Signaling. Molecules 2018, 23, 669. [Google Scholar] [CrossRef]
- Lee, Y.; Kim, S.; Oh, Y.; Kim, Y.M.; Chin, Y.W.; Cho, J. Inhibition of Oxidative Neurotoxicity and Scopolamine-Induced Memory Impairment by γ-Mangostin: In Vitro and In Vivo Evidence. Oxid. Med. Cell. Longev. 2019, 2019, 3640753. [Google Scholar] [CrossRef]
- Nguyen, P.L.; Bui, B.P.; Duong, M.T.H.; Lee, K.; Ahn, H.C.; Cho, J. Suppression of LPS-Induced Inflammation and Cell Migration by Azelastine through Inhibition of JNK/NF-κB Pathway in BV2 Microglial Cells. Int. J. Mol. Sci. 2021, 22, 9061. [Google Scholar] [CrossRef]
- Do, H.T.T.; Bui, B.P.; Sim, S.; Jung, J.K.; Lee, H.; Cho, J. Anti-Inflammatory and Anti-Migratory Activities of Isoquinoline-1-Carboxamide Derivatives in LPS-Treated BV2 Microglial Cells via Inhibition of MAPKs/NF-κB Pathway. Int. J. Mol. Sci. 2020, 21, 2319. [Google Scholar] [CrossRef] [PubMed]
- Do, H.T.T.; Cho, J. Involvement of the ERK/HIF-1α/EMT Pathway in XCL1-Induced Migration of MDA-MB-231 and SK-BR-3 Breast Cancer Cells. Int. J. Mol. Sci. 2020, 22, 89. [Google Scholar] [CrossRef] [PubMed]
- Tang, C.; Hu, Y.; Lyu, H.; Gao, J.; Jiang, J.; Qin, X.; Wu, Y.; Wang, J.; Chai, X. Neuroprotective effects of 1-O-hexyl-2,3,5-trimethylhydroquinone on ischaemia/reperfusion-induced neuronal injury by activating the Nrf2/HO-1 pathway. J. Cell. Mol. Med. 2020, 24, 10468–10477. [Google Scholar] [CrossRef] [PubMed]
- Bernstein, A.I.; Garrison, S.P.; Zambetti, G.P.; O’Malley, K.L. 6-OHDA generated ROS induces DNA damage and p53- and PUMA-dependent cell death. Mol. Neurodegener. 2011, 6, 2. [Google Scholar] [CrossRef] [PubMed]
- Tayarani-Najaran, Z.; Hadipour, E.; Seyed Mousavi, S.M.; Emami, S.A.; Mohtashami, L.; Javadi, B. Protective effects of Lavandula stoechas L. methanol extract against 6-OHDA-induced apoptosis in PC12 cells. J. Ethnopharmacol. 2021, 273, 114023. [Google Scholar] [CrossRef] [PubMed]
- Betarbet, R.; Sherer, T.B.; MacKenzie, G.; Garcia-Osuna, M.; Panov, A.V.; Greenamyre, J.T. Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat. Neurosci. 2000, 3, 1301–1306. [Google Scholar] [CrossRef] [PubMed]
- Rai, S.N.; Singh, P. Advancement in the modelling and therapeutics of Parkinson’s disease. J. Chem. Neuroanat. 2020, 104, 101752. [Google Scholar] [CrossRef]
- Uversky, V.N. Neurotoxicant-induced animal models of Parkinson’s disease: Understanding the role of rotenone, maneb and paraquat in neurodegeneration. Cell Tissue Res. 2004, 318, 225–241. [Google Scholar] [CrossRef]
- Jing, X.; Shi, Q.; Bi, W.; Zeng, Z.; Liang, Y.; Wu, X.; Xiao, S.; Liu, J.; Yang, L.; Tao, E. Rifampicin Protects PC12 Cells from Rotenone-Induced Cytotoxicity by Activating GRP78 via PERK-eIF2α-ATF4 Pathway. PLoS ONE 2014, 9, e92110. [Google Scholar] [CrossRef]
- Xiong, Y.-j.; Song, Y.-z.; Zhu, Y.; Zuo, W.-q.; Zhao, Y.-f.; Shen, X.; Wang, W.-j.; Liu, Y.-l.; Wu, J.-c.; Liang, Z.-q. Neuroprotective effects of olanzapine against rotenone-induced toxicity in PC12 cells. Acta Pharmacol. Sin. 2020, 41, 508–515. [Google Scholar] [CrossRef]
- Zhang, H.; Davies, K.J.A.; Forman, H.J. Oxidative stress response and Nrf2 signaling in aging. Free Radic. Biol. Med. 2015, 88, 314–336. [Google Scholar] [CrossRef] [PubMed]
- Gureev, A.P.; Popov, V.N. Nrf2/ARE Pathway as a Therapeutic Target for the Treatment of Parkinson Diseases. Neurochem. Res. 2019, 44, 2273–2279. [Google Scholar] [CrossRef]
- Maines, M.D. The heme oxygenase system: A regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 1997, 37, 517–554. [Google Scholar] [CrossRef] [PubMed]
- Araujo, J.A.; Zhang, M.; Yin, F. Heme oxygenase-1, oxidation, inflammation, and atherosclerosis. Front. Pharmacol. 2012, 3, 119. [Google Scholar] [CrossRef] [PubMed]
- Yoon, G.; Kim, Y.K.; Song, J. Glucagon-like peptide-1 suppresses neuroinflammation and improves neural structure. Pharmacol. Res. 2020, 152, 104615. [Google Scholar] [CrossRef]
- De Virgilio, A.; Greco, A.; Fabbrini, G.; Inghilleri, M.; Rizzo, M.I.; Gallo, A.; Conte, M.; Rosato, C.; Ciniglio Appiani, M.; de Vincentiis, M. Parkinson’s disease: Autoimmunity and neuroinflammation. Autoimmun. Rev. 2016, 15, 1005–1011. [Google Scholar] [CrossRef] [PubMed]
- Gelders, G.; Baekelandt, V.; Van der Perren, A. Linking Neuroinflammation and Neurodegeneration in Parkinson’s Disease. J. Immunol. Res. 2018, 2018, 4784268. [Google Scholar] [CrossRef]
- Gouda, N.A.; Elkamhawy, A.; Cho, J. Emerging Therapeutic Strategies for Parkinson’s Disease and Future Prospects: A 2021 Update. Biomedicines 2022, 10, 371. [Google Scholar] [CrossRef]
- Torreilles, F.; Salman-Tabcheh, S.; Guérin, M.; Torreilles, J. Neurodegenerative disorders: The role of peroxynitrite. Brain Res. Brain Res. Rev. 1999, 30, 153–163. [Google Scholar] [CrossRef]
- Boje, K.M. Nitric oxide neurotoxicity in neurodegenerative diseases. Front. Biosci. 2004, 9, 763–776. [Google Scholar] [CrossRef]
- Tao, L.; Li, X.; Zhang, L.; Tian, J.; Li, X.; Sun, X.; Li, X.; Jiang, L.; Zhang, X.; Chen, J. Protective effect of tetrahydroxystilbene glucoside on 6-OHDA-induced apoptosis in PC12 cells through the ROS-NO pathway. PLoS ONE 2011, 6, e26055. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.K.; Kim, S.C.; Kang, J.I.; Hyun, J.H.; Boo, H.J.; Eun, S.Y.; Park, D.B.; Yoo, E.S.; Kang, H.K.; Kang, J.H. 6-Hydroxydopamine-induced PC12 cell death is mediated by MEF2D down-regulation. Neurochem. Res. 2011, 36, 223–231. [Google Scholar] [CrossRef] [PubMed]
- Gao, B.; Chang, C.; Zhou, J.; Zhao, T.; Wang, C.; Li, C.; Gao, G. Pycnogenol Protects Against Rotenone-Induced Neurotoxicity in PC12 Cells Through Regulating NF-κB-iNOS Signaling Pathway. DNA Cell Biol. 2015, 34, 643–649. [Google Scholar] [CrossRef] [PubMed]
- Tieu, K. A guide to neurotoxic animal models of Parkinson’s disease. Cold Spring Harb. Perspect Med. 2011, 1, a009316. [Google Scholar] [CrossRef] [PubMed]
- Park, M.H.; Hong, J.T. Roles of NF-κB in Cancer and Inflammatory Diseases and Their Therapeutic Approaches. Cells 2016, 5, 15. [Google Scholar] [CrossRef]
- Soromou, L.W.; Zhang, Z.; Li, R.; Chen, N.; Guo, W.; Huo, M.; Guan, S.; Lu, J.; Deng, X. Regulation of inflammatory cytokines in lipopolysaccharide-stimulated RAW 264.7 murine macrophage by 7-O-methyl-naringenin. Molecules 2012, 17, 3574–3585. [Google Scholar] [CrossRef]
- Khasnavis, S.; Jana, A.; Roy, A.; Mazumder, M.; Bhushan, B.; Wood, T.; Ghosh, S.; Watson, R.; Pahan, K. Suppression of nuclear factor-κB activation and inflammation in microglia by physically modified saline. J. Biol. Chem. 2012, 287, 29529–29542. [Google Scholar] [CrossRef]
- Athauda, D.; Foltynie, T. The glucagon-like peptide 1 (GLP) receptor as a therapeutic target in Parkinson’s disease: Mechanisms of action. Drug Discov. Today 2016, 21, 802–818. [Google Scholar] [CrossRef]
- Hoesel, B.; Schmid, J.A. The complexity of NF-κB signaling in inflammation and cancer. Mol. Cancer 2013, 12, 86. [Google Scholar] [CrossRef]
- Hoeflich, K.P.; Luo, J.; Rubie, E.A.; Tsao, M.S.; Jin, O.; Woodgett, J.R. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 2000, 406, 86–90. [Google Scholar] [CrossRef]
- Tang, Q.L.; Xie, X.B.; Wang, J.; Chen, Q.; Han, A.J.; Zou, C.Y.; Yin, J.Q.; Liu, D.W.; Liang, Y.; Zhao, Z.Q.; et al. Glycogen synthase kinase-3β, NF-κB signaling, and tumorigenesis of human osteosarcoma. J. Natl. Cancer Inst. 2012, 104, 749–763. [Google Scholar] [CrossRef] [PubMed]
- Jope, R.S.; Yuskaitis, C.J.; Beurel, E. Glycogen synthase kinase-3 (GSK3): Inflammation, diseases, and therapeutics. Neurochem. Res. 2007, 32, 577–595. [Google Scholar] [CrossRef] [PubMed]
- Lin, M.T.; Beal, M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443, 787–795. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Gao, S.S.; Yang, H.J.; Wang, M.; Cheng, B.F.; Feng, Z.W.; Wang, L. Neuroprotective Effects of Proanthocyanidins, Natural Flavonoids Derived From Plants, on Rotenone-Induced Oxidative Stress and Apoptotic Cell Death in Human Neuroblastoma SH-SY5Y Cells. Front. Neurosci. 2018, 12, 369. [Google Scholar] [CrossRef] [PubMed]
- Ramazani, E.; YazdFazeli, M.; Emami, S.A.; Mohtashami, L.; Javadi, B.; Asili, J.; Tayarani-Najaran, Z. Protective effects of Cinnamomum verum, Cinnamomum cassia and cinnamaldehyde against 6-OHDA-induced apoptosis in PC12 cells. Mol. Biol. Rep. 2020, 47, 2437–2445. [Google Scholar] [CrossRef]
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Gouda, N.A.; Cho, J. Omarigliptin Mitigates 6-Hydroxydopamine- or Rotenone-Induced Oxidative Toxicity in PC12 Cells by Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Actions. Antioxidants 2022, 11, 1940. https://doi.org/10.3390/antiox11101940
Gouda NA, Cho J. Omarigliptin Mitigates 6-Hydroxydopamine- or Rotenone-Induced Oxidative Toxicity in PC12 Cells by Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Actions. Antioxidants. 2022; 11(10):1940. https://doi.org/10.3390/antiox11101940
Chicago/Turabian StyleGouda, Noha A., and Jungsook Cho. 2022. "Omarigliptin Mitigates 6-Hydroxydopamine- or Rotenone-Induced Oxidative Toxicity in PC12 Cells by Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Actions" Antioxidants 11, no. 10: 1940. https://doi.org/10.3390/antiox11101940
APA StyleGouda, N. A., & Cho, J. (2022). Omarigliptin Mitigates 6-Hydroxydopamine- or Rotenone-Induced Oxidative Toxicity in PC12 Cells by Antioxidant, Anti-Inflammatory, and Anti-Apoptotic Actions. Antioxidants, 11(10), 1940. https://doi.org/10.3390/antiox11101940