Review Article

Effect of Rotenone on the Neurodegeneration among Different Models

Author(s): Iqra Subhan and Yasir Hasan Siddique*

Volume 25, Issue 8, 2024

Published on: 02 May, 2024

Page: [530 - 542] Pages: 13

DOI: 10.2174/0113894501281496231226070459

Price: $65

Abstract

Rotenone is a naturally occurring plant product used as an insecticide, pesticide and piscicide. It is lipophilic in nature and can cross the blood-brain barrier and induce the degeneration of neurons. It inhibits the mitochondrial respiratory chain complex I and stops the transfer of electrons. It induces ROS generation, which impairs mitochondrial activity. Rotenone is a toxic agent which causes the death of neurons. The present review describes the effect of rotenone on neurodegeneration with an emphasis on behavioral, pathological and neuropathological components carried out on various experimental models such as cell lines, Drosophila melanogaster, mice and rats.

Keywords: Rotenone, insecticide, complex-i inhibitor, neurodegeneration, cell lines, Drosophila, mice, rats.

Graphical Abstract
[1]
Tamilselvam K, Braidy N, Manivasagam T, et al. Neuroprotective effects of hesperidin, a plant flavanone, on rotenone-induced oxidative stress and apoptosis in a cellular model for Parkinson’s disease. Oxid Med Cell Longev 2013; 2013: 1-11.
[http://dx.doi.org/10.1155/2013/102741] [PMID: 24205431]
[2]
Höglinger GU, Lannuzel A, Khondiker ME, et al. The mitochondrial complex I inhibitor rotenone triggers a cerebral tauopathy. J Neurochem 2005; 95(4): 930-9.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03493.x] [PMID: 16219024]
[3]
Kumar PP, Bawani SS, Anandhi DU, Prashanth KVH. Rotenone mediated developmental toxicity in Drosophila melanogaster. Environ Toxicol Pharmacol 2022; 93: 103892.
[http://dx.doi.org/10.1016/j.etap.2022.103892] [PMID: 35654372]
[4]
Radad K, Al-Shraim M, Al-Emam A, et al. Rotenone: From modelling to implication in Parkinson’s disease. Folia Neuropathol 2019; 57(4): 317-26.
[http://dx.doi.org/10.5114/fn.2019.89857] [PMID: 32337944]
[5]
Ling N. Rotenone a review of its toxicity and use for fisheries management. Sci Conserv 2002; 211: 40.
[6]
Fukuda T. Neurotoxicity of MPTP. Neuropathology 2001; 21(4): 323-32.
[http://dx.doi.org/10.1046/j.1440-1789.2001.00402.x] [PMID: 11837540]
[7]
Alam M, Schmidt WJ. Rotenone destroys dopaminergic neurons and induces parkinsonian symptoms in rats. Behav Brain Res 2002; 136(1): 317-24.
[http://dx.doi.org/10.1016/S0166-4328(02)00180-8] [PMID: 12385818]
[8]
Testa CM, Sherer TB, Greenamyre JT. Rotenone induces oxidative stress and dopaminergic neuron damage in organotypic substantia nigra cultures. Brain Res Mol Brain Res 2005; 134(1): 109-18.
[http://dx.doi.org/10.1016/j.molbrainres.2004.11.007] [PMID: 15790535]
[9]
Shinomol GK, Mythri RB, Srinivas Bharath MM, Muralidhara . Bacopa monnieri extract offsets rotenone-induced cytotoxicity in dopaminergic cells and oxidative impairments in mice brain. Cell Mol Neurobiol 2012; 32(3): 455-65.
[http://dx.doi.org/10.1007/s10571-011-9776-0] [PMID: 22160863]
[10]
Pereira CS, Teixeira MH, Russell DA, Hirst J, Arantes GM. Mechanism of rotenone binding to respiratory complex I depends on ligand flexibility. Sci Rep 2023; 13(1): 6738.
[http://dx.doi.org/10.1038/s41598-023-33333-6] [PMID: 37185607]
[11]
Koopman WJH, Willems PHGM, Smeitink JAM. Monogenic mitochondrial disorders. N Engl J Med 2012; 366(12): 1132-41.
[http://dx.doi.org/10.1056/NEJMra1012478] [PMID: 22435372]
[12]
Wirth C, Brandt U, Hunte C, Zickermann V. Structure and function of mitochondrial complex I. Biochim Biophys Acta Bioenerg 2016; 1857(7): 902-14.
[http://dx.doi.org/10.1016/j.bbabio.2016.02.013]
[13]
Palmer G, Horgan DJ, Tisdale H, Singer TP, Beinert H. Studies on the respiratory chain-linked reduced nicotinamide adenine dinucleotide dehydrogenase. XIV. Location of the sites of inhibition of rotenone, barbiturates, and piericidin by means of electron paramagnetic resonance spectroscopy. J Biol Chem 1968; 243(4): 844-7.
[http://dx.doi.org/10.1016/S0021-9258(19)81742-8] [PMID: 4295607]
[14]
Li N, Ragheb K, Lawler G, et al. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J Biol Chem 2003; 278(10): 8516-25.
[http://dx.doi.org/10.1074/jbc.M210432200] [PMID: 12496265]
[15]
Sies H. Oxidative stress: Oxidants and antioxidants. Exp Physiol 1997; 82(2): 291-5.
[http://dx.doi.org/10.1113/expphysiol.1997.sp004024] [PMID: 9129943]
[16]
Ighodaro OM, Akinloye OA. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Med 2018; 54(4): 287-93.
[http://dx.doi.org/10.1016/j.ajme.2017.09.001]
[17]
Heinz S, Freyberger A, Lawrenz B, Schladt L, Schmuck G, Ellinger-Ziegelbauer H. Mechanistic investigations of the mitochondrial complex I inhibitor rotenone in the context of pharmacological and safety evaluation. Sci Rep 2017; 7(1): 45465.
[http://dx.doi.org/10.1038/srep45465] [PMID: 28374803]
[18]
Srivastava P, Panda D. Rotenone inhibits mammalian cell proliferation by inhibiting microtubule assembly through tubulin binding. FEBS J 2007; 274(18): 4788-801.
[http://dx.doi.org/10.1111/j.1742-4658.2007.06004.x] [PMID: 17697112]
[19]
Bisbal M, Sanchez M. Neurotoxicity of the pesticide rotenone on neuronal polarization: A mechanistic approach. Neural Regen Res 2019; 14(5): 762-6.
[http://dx.doi.org/10.4103/1673-5374.249847] [PMID: 30688258]
[20]
Passmore JB, Pinho S, Gomez-Lazaro M, Schrader M. The respiratory chain inhibitor rotenone affects peroxisomal dynamics via its microtubule-destabilising activity. Histochem Cell Biol 2017; 148(3): 331-41.
[http://dx.doi.org/10.1007/s00418-017-1577-1] [PMID: 28523458]
[21]
Wu F, Xu HD, Guan JJ, et al. Rotenone impairs autophagic flux and lysosomal functions in Parkinson’s disease. Neuroscience 2015; 284: 900-11.
[http://dx.doi.org/10.1016/j.neuroscience.2014.11.004] [PMID: 25446361]
[22]
Sonia Angeline M, Sarkar A, Anand K, Ambasta RK, Kumar P. Sesamol and naringenin reverse the effect of rotenone-induced PD rat model. Neuroscience 2013; 254: 379-94.
[http://dx.doi.org/10.1016/j.neuroscience.2013.09.029] [PMID: 24070629]
[23]
Matsunaga K, Saitoh T, Tabata K, et al. Two Beclin 1-binding proteins, Atg14L and Rubicon, reciprocally regulate autophagy at different stages. Nat Cell Biol 2009; 11(4): 385-96.
[http://dx.doi.org/10.1038/ncb1846] [PMID: 19270696]
[24]
Ethell DW, Fei Q. Parkinson-linked genes and toxins that affect neuronal cell death through the Bcl-2 family. Antioxid Redox Signal 2009; 11(3): 529-40.
[http://dx.doi.org/10.1089/ars.2008.2228] [PMID: 18715146]
[25]
Xiong N, Long X, Xiong J, et al. Mitochondrial complex I inhibitor rotenone-induced toxicity and its potential mechanisms in Parkinson’s disease models. Crit Rev Toxicol 2012; 42(7): 613-32.
[http://dx.doi.org/10.3109/10408444.2012.680431] [PMID: 22574684]
[26]
Kahle PJ, Waak J, Gasser T. DJ-1 and prevention of oxidative stress in Parkinson’s disease and other age-related disorders. Free Radic Biol Med 2009; 47(10): 1354-61.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.08.003] [PMID: 19686841]
[27]
Lee JM, Johnson JA. An important role of Nrf2-ARE pathway in the cellular defense mechanism. J Biochem Mol Biol 2004; 37(2): 139-43.
[PMID: 15469687]
[28]
Ma Q. Role of nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 2013; 53(1): 401-26.
[http://dx.doi.org/10.1146/annurev-pharmtox-011112-140320] [PMID: 23294312]
[29]
Jazwa A, Rojo AI, Innamorato NG, Hesse M, Fernández-Ruiz J, Cuadrado A. Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid Redox Signal 2011; 14(12): 2347-60.
[http://dx.doi.org/10.1089/ars.2010.3731] [PMID: 21254817]
[30]
Yuan Y, Sun J, Wu M, Hu J, Peng S, Chen NH. Rotenone could activate microglia through NFκB associated pathway. Neurochem Res 2013; 38(8): 1553-60.
[http://dx.doi.org/10.1007/s11064-013-1055-7] [PMID: 23645222]
[31]
Denault JB, Salvesen GS. Caspases. Curr Protoc Protein Sci 2001; 26(1): 21-8.
[http://dx.doi.org/10.1002/0471140864.ps2108s26]
[32]
Tada-Oikawa S, Oikawa S, Kawanishi M, Yamada M, Kawanishi S. Generation of hydrogen peroxide precedes loss of mitochondrial membrane potential during DNA alkylation-induced apoptosis. FEBS Lett 1999; 442(1): 65-9.
[http://dx.doi.org/10.1016/S0014-5793(98)01618-4] [PMID: 9923606]
[33]
Tolkovsky AM. Mitophagy. Biochimica et biophysica acta (BBA)-. Molecular Cell Research 2009; 1793(9): 1508-15.
[34]
Jauhari A, Singh T, Mishra S, Shankar J, Yadav S. Coordinated action of miR-146a and parkin gene regulate rotenone-induced neurodegeneration. Toxicol Sci 2020; 176(2): 433-45.
[http://dx.doi.org/10.1093/toxsci/kfaa066] [PMID: 32392329]
[35]
Vives-Bauza C, Zhou C, Huang Y, et al. PINK1-dependent recruitment of parkin to mitochondria in mitophagy. Proc Natl Acad Sci 2010; 107(1): 378-83.
[http://dx.doi.org/10.1073/pnas.0911187107] [PMID: 19966284]
[36]
Wang Y, Liu N, Lu B. Mechanisms and roles of mitophagy in neurodegenerative diseases. CNS Neurosci Ther 2019; 25(7): 859-75.
[http://dx.doi.org/10.1111/cns.13140] [PMID: 31050206]
[37]
Yang X, Qian Y, Xu S, Song Y, Xiao Q. Longitudinal analysis of fecal microbiome and pathologic processes in a rotenone induced mice model of Parkinson’s disease. Front Aging Neurosci 2018; 9: 441.
[http://dx.doi.org/10.3389/fnagi.2017.00441] [PMID: 29358918]
[38]
Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ 2013; 20(1): 31-42.
[http://dx.doi.org/10.1038/cdd.2012.81] [PMID: 22743996]
[39]
Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol 2011; 12(1): 9-14.
[http://dx.doi.org/10.1038/nrm3028] [PMID: 21179058]
[40]
Kim YY, Um JH, Yoon JH, et al. Assessment of mitophagy in mt-Keima Drosophila revealed an essential role of the PINK1-Parkin pathway in mitophagy induction in vivo. FASEB J 2019; 33(9): 9742-51.
[http://dx.doi.org/10.1096/fj.201900073R] [PMID: 31120803]
[41]
Wang N, Zhao J, Liu Q, Diao X, Kong B. Sulforaphane protects human umbilical vein cells against lipotoxicity by stimulating autophagy via an AMPK-mediated pathway. J Funct Foods 2015; 15: 23-34.
[http://dx.doi.org/10.1016/j.jff.2015.03.016]
[42]
Cai Z, Yan LJ. Rapamycin, autophagy, and Alzheimer’s disease. J Biochem Pharmacol Res 2013; 1(2): 84-90.
[PMID: 23826514]
[43]
Yarmohammadi F, Wallace Hayes A, Najafi N, Karimi G. The protective effect of natural compounds against rotenone-induced neurotoxicity. J Biochem Mol Toxicol 2020; 34(12): e22605.
[http://dx.doi.org/10.1002/jbt.22605] [PMID: 32830361]
[44]
Hanna RA, Quinsay MN, Orogo AM, Giang K, Rikka S, Gustafsson ÅB. Microtubule-associated protein 1 light chain 3 (LC3) interacts with Bnip3 protein to selectively remove endoplasmic reticulum and mitochondria via autophagy. J Biol Chem 2012; 287(23): 19094-104.
[http://dx.doi.org/10.1074/jbc.M111.322933] [PMID: 22505714]
[45]
Mader BJ, Pivtoraiko VN, Flippo HM, et al. Rotenone inhibits autophagic flux prior to inducing cell death. ACS Chem Neurosci 2012; 3(12): 1063-72.
[http://dx.doi.org/10.1021/cn300145z] [PMID: 23259041]
[46]
El-Sherbeeny NA, Soliman N, Youssef AM, et al. The protective effect of biochanin A against rotenone-induced neurotoxicity in mice involves enhancing of PI3K/Akt/mTOR signaling and beclin-1 production. Ecotoxicol Environ Saf 2020; 205: 111344.
[http://dx.doi.org/10.1016/j.ecoenv.2020.111344] [PMID: 32977283]
[47]
Jang W, Kim HJ, Li H, Jo KD, Lee MK, Yang HO. The Neuroprotective effect of erythropoietin on rotenone-induced neurotoxicity in SH-SY5Y Cells through the induction of autophagy. Mol Neurobiol 2016; 53(6): 3812-21.
[http://dx.doi.org/10.1007/s12035-015-9316-x] [PMID: 26156288]
[48]
Ravid T, Hochstrasser M. Diversity of degradation signals in the ubiquitin–proteasome system. Nat Rev Mol Cell Biol 2008; 9(9): 679-89.
[http://dx.doi.org/10.1038/nrm2468] [PMID: 18698327]
[49]
Sherer TB, Betarbet R, Testa CM, et al. Mechanism of toxicity in rotenone models of Parkinson’s disease. J Neurosci 2003; 23(34): 10756-64.
[http://dx.doi.org/10.1523/JNEUROSCI.23-34-10756.2003] [PMID: 14645467]
[50]
Chou AP, Li S, Fitzmaurice AG, Bronstein JM. Mechanisms of rotenone-induced proteasome inhibition. Neurotoxicology 2010; 31(4): 367-72.
[http://dx.doi.org/10.1016/j.neuro.2010.04.006] [PMID: 20417232]
[51]
Ebrahimi-Fakhari D, Wahlster L, McLean PJ. Protein degradation pathways in Parkinson’s disease: Curse or blessing. Acta Neuropathol 2012; 124(2): 153-72.
[http://dx.doi.org/10.1007/s00401-012-1004-6] [PMID: 22744791]
[52]
Rocha SM, Bantle CM, Aboellail T, Chatterjee D, Smeyne RJ, Tjalkens RB. Rotenone induces regionally distinct α-synuclein protein aggregation and activation of glia prior to loss of dopaminergic neurons in C57Bl/6 mice. Neurobiol Dis 2022; 167: 105685.
[http://dx.doi.org/10.1016/j.nbd.2022.105685] [PMID: 35257879]
[53]
Chaves RS, Kazi AI, Silva CM, et al. Presence of insoluble Tau following rotenone exposure ameliorates basic pathways associated with neurodegeneration. IBRO Rep 2016; 1: 32-45.
[http://dx.doi.org/10.1016/j.ibror.2016.09.001] [PMID: 30135926]
[54]
Buratta S, Chiaradia E, Tognoloni A, et al. Effect of curcumin on protein damage induced by rotenone in dopaminergic PC12 cells. Int J Mol Sci 2020; 21(8): 2761.
[http://dx.doi.org/10.3390/ijms21082761] [PMID: 32316110]
[55]
Fukami J, Yamamoto I, Casida JE. Metabolism of rotenone in vitro by tissue homogenates from mammals and insects. Science 1967; 155(3763): 713-6.
[http://dx.doi.org/10.1126/science.155.3763.713] [PMID: 4381128]
[56]
Caboni P, Sherer TB, Zhang N, et al. Rotenone, deguelin, their metabolites, and the rat model of Parkinson’s disease. Chem Res Toxicol 2004; 17(11): 1540-8.
[http://dx.doi.org/10.1021/tx049867r] [PMID: 15540952]
[57]
Barreca D, Currò M, Bellocco E, et al. Neuroprotective effects of phloretin and its glycosylated derivative on rotenone-induced toxicity in human SH-SY5Y neuronal-like cells. Biofactors 2017; 43(4): 549-57.
[http://dx.doi.org/10.1002/biof.1358] [PMID: 28401997]
[58]
Pakrashi S, Chakraborty J, Bandyopadhyay J. Neuroprotective role of quercetin on rotenone-induced toxicity in SH-SY5Y cell line through modulation of apoptotic and autophagic pathways. Neurochem Res 2020; 45(8): 1962-73.
[http://dx.doi.org/10.1007/s11064-020-03061-8] [PMID: 32488468]
[59]
Sun W, Li H, Shen Y, Xiao H. Resveratrol attenuates rotenone-induced inflammation and oxidative stress via STAT1 and Nrf2/Keap1/SLC7A11 pathway in a microglia cell line. Pathol Res Pract 2021; 225: 153576.
[http://dx.doi.org/10.1016/j.prp.2021.153576] [PMID: 34391968]
[60]
Abdalkader M, Lampinen R, Kanninen KM, Malm TM, Liddell JR. Targeting Nrf2 to suppress ferroptosis and mitochondrial dysfunction in neurodegeneration. Front Neurosci 2018; 12: 466.
[http://dx.doi.org/10.3389/fnins.2018.00466] [PMID: 30042655]
[61]
Molina-Jiménez MF, Sánchez-Reus MI, Andres D, Cascales M, Benedi J. Neuroprotective effect of fraxetin and myricetin against rotenone-induced apoptosis in neuroblastoma cells. Brain Res 2004; 1009(1-2): 9-16.
[http://dx.doi.org/10.1016/j.brainres.2004.02.065] [PMID: 15120578]
[62]
Ahlawat J, Deemer EM, Narayan M. Chitosan nanoparticles rescue rotenone-mediated cell death. Materials 2019; 12(7): 1176.
[http://dx.doi.org/10.3390/ma12071176] [PMID: 30978909]
[63]
Condello S, Currò M, Ferlazzo N, Caccamo D, Satriano J, Ientile R. Agmatine effects on mitochondrial membrane potential andNF-κB activation protect against rotenone-induced cell damage in human neuronal-like SH-SY5Y cells. J Neurochem 2011; 116(1): 67-75.
[http://dx.doi.org/10.1111/j.1471-4159.2010.07085.x] [PMID: 21044082]
[64]
Swarnkar S, Singh S, Goswami P, Mathur R, Patro IK, Nath C. Astrocyte activation: A key step in rotenone induced cytotoxicity and DNA damage. Neurochem Res 2012; 37(10): 2178-89.
[http://dx.doi.org/10.1007/s11064-012-0841-y] [PMID: 22846965]
[65]
Feng Y, Liu T, Dong SY, et al. Rotenone affects p53 transcriptional activity and apoptosis via targeting SIRT 1 and H3K9 acetylation in SH-SY 5Y cells. J Neurochem 2015; 134(4): 668-76.
[http://dx.doi.org/10.1111/jnc.13172] [PMID: 25991017]
[66]
Marella M, Seo BB, Matsuno-Yagi A, Yagi T. Mechanism of cell death caused by complex I defects in a rat dopaminergic cell line. J Biol Chem 2007; 282(33): 24146-56.
[http://dx.doi.org/10.1074/jbc.M701819200] [PMID: 17581813]
[67]
Bollimpelli VS, Kumar P, Kumari S, Kondapi AK. Neuroprotective effect of curcumin-loaded lactoferrin nano particles against rotenone induced neurotoxicity. Neurochem Int 2016; 95: 37-45.
[http://dx.doi.org/10.1016/j.neuint.2016.01.006] [PMID: 26826319]
[68]
Chen YY, Chen G, Fan Z, Luo J, Ke ZJ. GSK3β and endoplasmic reticulum stress mediate rotenone-induced death of SK-N-MC neuroblastoma cells. Biochem Pharmacol 2008; 76(1): 128-38.
[http://dx.doi.org/10.1016/j.bcp.2008.04.010] [PMID: 18508033]
[69]
Sherer TB, Betarbet R, Stout AK, et al. An in vitro model of Parkinson’s disease: Linking mitochondrial impairment to altered α-synuclein metabolism and oxidative damage. J Neurosci 2002; 22(16): 7006-15.
[http://dx.doi.org/10.1523/JNEUROSCI.22-16-07006.2002] [PMID: 12177198]
[70]
Cabezas R, Avila MF, González J, El-Bachá RS, Barreto GE. PDGF-BB protects mitochondria from rotenone in T98G cells. Neurotox Res 2015; 27(4): 355-67.
[http://dx.doi.org/10.1007/s12640-014-9509-5] [PMID: 25516121]
[71]
Kiseleva LN, Kartashev AV, Vartanyan NL, Pinevich AA, Samoilovich MP. A172 and T98G cell lines characteristics. Cell Tissue Biol 2016; 10(5): 341-8.
[http://dx.doi.org/10.1134/S1990519X16050072] [PMID: 30188626]
[72]
Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 2001; 11(6): 1114-25.
[http://dx.doi.org/10.1101/gr.169101] [PMID: 11381037]
[73]
Siddique YH, Naz F, Jyoti S, Ali F, Fatima A, Khanam S. Protective effect of Geraniol on the transgenic Drosophila model of Parkinson’s diseases. Environ Toxicol Pharamcol 2016; 43: 225-31.
[74]
Beg T, Jyoti S, Naz F, et al. Protective effect of kaempferol on the transgenic Drosophila model of Alzheimer's disease. CNS & Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders 2018; 17(6): 421-9.
[http://dx.doi.org/10.2174/1871527317666180508123050]
[75]
Siddique YH, Rahul , Ara G, et al. Beneficial effects of apigenin on the transgenic Drosophila model of Alzheimer’s disease. Chem Biol Interact 2022; 366: 110120.
[http://dx.doi.org/10.1016/j.cbi.2022.110120] [PMID: 36027948]
[76]
Naz F, Jyoti S, Siddique YH. Effect of kaempferol on the transgenic Drosophila model of Parkinson’s disease. Sci Rep 2020; 10(1): 1-14.
[PMID: 31913322]
[77]
Ali F, Rahul , Jyoti S, et al. Therapeutic potential of luteolin in transgenic Drosophila model of Alzheimer’s disease. Neurosci Lett 2019; 692: 90-9.
[http://dx.doi.org/10.1016/j.neulet.2018.10.053] [PMID: 30420334]
[78]
Siddique YH, Naz F, Jyoti S. Effect of curcumin on lifespan, activity pattern, oxidative stress, and apoptosis in the brains of transgenic Drosophila model of Parkinson’s disease. BioMed Res Int 2014; 2014: 1-6.
[http://dx.doi.org/10.1155/2014/606928] [PMID: 24860828]
[79]
Siddique YH, Khan W, Singh BR, Naqvi AH. Synthesis of alginate-curcumin nanocomposite and its protective role in transgenic Drosophila model of Parkinson’s disease. ISRN Pharmacol 2013; 2013: 1-8.
[http://dx.doi.org/10.1155/2013/794582] [PMID: 24171120]
[80]
Siddique YH, Jyoti S, Naz F. Effect of epicatechin gallate dietary supplementation on transgenic Drosophila model of Parkinson’s disease. J Diet Suppl 2014; 11(2): 121-30.
[http://dx.doi.org/10.3109/19390211.2013.859207] [PMID: 24670116]
[81]
Subhan I, Siddique YH. Modulation of huntington’s disease in Drosophila. CNS & Neurological Disorders-Drug Targets 2021; 20(10): 894-903.
[http://dx.doi.org/10.2174/1871527320666210412155508]
[82]
Coulom H, Birman S. Chronic exposure to rotenone models sporadic Parkinson’s disease in Drosophila melanogaster. J Neurosci 2004; 24(48): 10993-8.
[http://dx.doi.org/10.1523/JNEUROSCI.2993-04.2004] [PMID: 15574749]
[83]
Sudati JH, Vieira FA, Pavin SS, et al. Valeriana officinalis attenuates the rotenone-induced toxicity in Drosophila melanogaster. Neurotoxicology 2013; 37: 118-26.
[http://dx.doi.org/10.1016/j.neuro.2013.04.006] [PMID: 23639798]
[84]
Hosamani R, Muralidhara . Neuroprotective efficacy of Bacopa monnieri against rotenone induced oxidative stress and neurotoxicity in Drosophila melanogaster. Neurotoxicology 2009; 30(6): 977-85.
[http://dx.doi.org/10.1016/j.neuro.2009.08.012] [PMID: 19744517]
[85]
Hosamani R, Ramesh SR, Muralidhara . Attenuation of rotenone-induced mitochondrial oxidative damage and neurotoxicty in Drosophila melanogaster supplemented with creatine. Neurochem Res 2010; 35(9): 1402-12.
[http://dx.doi.org/10.1007/s11064-010-0198-z] [PMID: 20514516]
[86]
Akinade TC, Babatunde OO, Adedara AO, et al. Protective capacity of carotenoid trans-astaxanthin in rotenone-induced toxicity in Drosophila melanogaster. Sci Rep 2022; 12(1): 4594.
[http://dx.doi.org/10.1038/s41598-022-08409-4] [PMID: 35301354]
[87]
Adedara AO, Otenaike TA, Olabiyi AA, Adedara IA, Abolaji AO. Neurotoxic and behavioral deficit in Drosophila melanogaster co-exposed to rotenone and iron. Metab Brain Dis 2023; 38(1): 349-60.
[http://dx.doi.org/10.1007/s11011-022-01104-3] [PMID: 36308588]
[88]
Levine RL, Stadtman ER. Oxidative modification of proteins during aging. Exp Gerontol 2001; 36(9): 1495-502.
[http://dx.doi.org/10.1016/S0531-5565(01)00135-8] [PMID: 11525872]
[89]
Yun J, Puri R, Yang H, et al. MUL1 acts in parallel to the PINK1/parkin pathway in regulating mitofusin and compensates for loss of PINK1/parkin. elife 2014; 3: 01958.
[90]
Doktór B, Damulewicz M, Pyza E. Overexpression of mitochondrial ligases reverses rotenone-induced effects in a Drosophila model of Parkinson’s disease. Front Neurosci 2019; 13: 94.
[http://dx.doi.org/10.3389/fnins.2019.00094] [PMID: 30837828]
[91]
Inden M, Kitamura Y, Abe M, Tamaki A, Takata K, Taniguchi T. Parkinsonian rotenone mouse model: Reevaluation of long-term administration of rotenone in C57BL/6 mice. Biol Pharm Bull 2011; 34(1): 92-6.
[http://dx.doi.org/10.1248/bpb.34.92] [PMID: 21212524]
[92]
Zhang D, Li S, Hou L, et al. Microglial activation contributes to cognitive impairments in rotenone-induced mouse Parkinson’s disease model. J Neuroinflammation 2021; 18(1): 4.
[http://dx.doi.org/10.1186/s12974-020-02065-z] [PMID: 33402167]
[93]
Thiffault C, Langston JW, Di Monte DA. Increased striatal dopamine turnover following acute administration of rotenone to mice. Brain Res 2000; 885(2): 283-8.
[http://dx.doi.org/10.1016/S0006-8993(00)02960-7] [PMID: 11102582]
[94]
Pan-Montojo F, Anichtchik O, Dening Y, et al. Progression of Parkinson’s disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One 2010; 5(1): e8762.
[http://dx.doi.org/10.1371/journal.pone.0008762] [PMID: 20098733]
[95]
Miyazaki I, Isooka N, Imafuku F, et al. Chronic systemic exposure to low-dose rotenone induced central and peripheral neuropathology and motor deficits in mice: reproducible animal model of Parkinson’s disease. Int J Mol Sci 2020; 21(9): 3254.
[http://dx.doi.org/10.3390/ijms21093254] [PMID: 32375371]
[96]
Hasan W, Kori RK, Jain J, Yadav RS, Jat D. Neuroprotective effects of mitochondria-targeted curcumin against rotenone-induced oxidative damage in cerebellum of mice. J Biochem Mol Toxicol 2020; 34(1): e22416.
[http://dx.doi.org/10.1002/jbt.22416] [PMID: 31714633]
[97]
Singh S, Ganguly U, Pal S, et al. Protective effects of cyclosporine A on neurodegeneration and motor impairment in rotenone-induced experimental models of Parkinson’s disease. Eur J Pharmacol 2022; 929: 175129.
[http://dx.doi.org/10.1016/j.ejphar.2022.175129] [PMID: 35777442]
[98]
Fleming S, Zhu C, Fernagut PO, et al. Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone. Exp Neurol 2004; 187(2): 418-29.
[http://dx.doi.org/10.1016/j.expneurol.2004.01.023] [PMID: 15144868]
[99]
Damier P, Hirsch EC, Agid Y, Graybiel AM. The substantia nigra of the human brain. Brain 1999; 122(8): 1437-48.
[http://dx.doi.org/10.1093/brain/122.8.1437] [PMID: 10430830]
[100]
Sasajima H, Miyazono S, Noguchi T, Kashiwayanagi M. Intranasal administration of rotenone in mice attenuated olfactory functions through the lesion of dopaminergic neurons in the olfactory bulb. Neurotoxicology 2015; 51: 106-15.
[http://dx.doi.org/10.1016/j.neuro.2015.10.006] [PMID: 26493152]
[101]
Rakha MK, Tawfiq RA, Sadek MM, et al. Neurotherapeutic effects of bee venom in a rotenone-induced mouse model of Parkinson’s disease. Neurophysiology 2018; 50(6): 445-55.
[http://dx.doi.org/10.1007/s11062-019-09777-w]
[102]
Venkateshappa C, Harish G, Mythri RB, Mahadevan A, Srinivas Bharath MM, Shankar SK. Increased oxidative damage and decreased antioxidant function in aging human substantia nigra compared to striatum: Implications for Parkinson’s disease. Neurochem Res 2012; 37(2): 358-69.
[http://dx.doi.org/10.1007/s11064-011-0619-7] [PMID: 21971758]
[103]
Krishna G, Muralidhara . Aqueous extract of tomato seeds attenuates rotenone-induced oxidative stress and neurotoxicity in Drosophila melanogaster. J Sci Food Agric 2016; 96(5): 1745-55.
[http://dx.doi.org/10.1002/jsfa.7281] [PMID: 26033662]
[104]
Khadrawy YA, Salem AM, El-Shamy KA, Ahmed EK, Fadl NN, Hosny EN. Neuroprotective and therapeutic effect of caffeine on the rat model of Parkinson’s disease induced by rotenone. J Diet Suppl 2017; 14(5): 553-72.
[http://dx.doi.org/10.1080/19390211.2016.1275916] [PMID: 28301304]
[105]
Tsakiris S, Angelogianni P, Schulpis KH, Stavridis JC. Protective effect of l-phenylalanine on rat brain acetylcholinesterase inhibition induced by free radicals. Clin Biochem 2000; 33(2): 103-6.
[http://dx.doi.org/10.1016/S0009-9120(99)00090-9] [PMID: 10751587]
[106]
Richter F, Hamann M, Richter A. Chronic rotenone treatment induces behavioral effects but no pathological signs of parkinsonism in mice. J Neurosci Res 2007; 85(3): 681-91.
[http://dx.doi.org/10.1002/jnr.21159] [PMID: 17171705]
[107]
Harder B, Jiang T, Wu T, et al. Molecular mechanisms of Nrf2 regulation and how these influence chemical modulation for disease intervention. Biochem Soc Trans 2015; 43(4): 680-6.
[http://dx.doi.org/10.1042/BST20150020] [PMID: 26551712]
[108]
Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 2000; 3(12): 1301-6.
[http://dx.doi.org/10.1038/81834] [PMID: 11100151]
[109]
Ojha S, Javed H, Azimullah S, Abul Khair SB, Haque ME. Glycyrrhizic acid attenuates neuroinflammation and oxidative stress in rotenone model of Parkinson’s disease. Neurotox Res 2016; 29(2): 275-87.
[http://dx.doi.org/10.1007/s12640-015-9579-z] [PMID: 26607911]
[110]
Callizot N, Combes M, Henriques A, Poindron P. Necrosis, apoptosis, necroptosis, three modes of action of dopaminergic neuron neurotoxins. PLoS One 2019; 14(4): e0215277.
[http://dx.doi.org/10.1371/journal.pone.0215277] [PMID: 31022188]
[111]
Skulachev VP. Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 2006; 11(4): 473-85.
[http://dx.doi.org/10.1007/s10495-006-5881-9] [PMID: 16532373]
[112]
Liu S, Li Y, Choi HMC, et al. Lysosomal damage after spinal cord injury causes accumulation of RIPK1 and RIPK3 proteins and potentiation of necroptosis. Cell Death Dis 2018; 9(5): 476.
[http://dx.doi.org/10.1038/s41419-018-0469-1] [PMID: 29686269]
[113]
Shaikh SB, Nicholson LFB. Effects of chronic low dose rotenone treatment on human microglial cells. Mol Neurodegener 2009; 4(1): 55.
[http://dx.doi.org/10.1186/1750-1326-4-55] [PMID: 20042120]
[114]
Newhouse K, Hsuan SL, Chang SH, Cai B, Wang Y, Xia Z. Rotenone-induced apoptosis is mediated by p38 and JNK MAP kinases in human dopaminergic SH-SY5Y cells. Toxicol Sci 2004; 79(1): 137-46.
[http://dx.doi.org/10.1093/toxsci/kfh089] [PMID: 14976342]
[115]
Gao HM, Hong JS, Zhang W, Liu B. Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J Neurosci 2002; 22(3): 782-90.
[http://dx.doi.org/10.1523/JNEUROSCI.22-03-00782.2002] [PMID: 11826108]
[116]
Bashkatova V, Alam M, Vanin A, Schmidt WJ. Chronic administration of rotenone increases levels of nitric oxide and lipid peroxidation products in rat brain. Exp Neurol 2004; 186(2): 235-41.
[http://dx.doi.org/10.1016/j.expneurol.2003.12.005] [PMID: 15026259]
[117]
Zhu C, Vourc’h P, Fernagut PO, et al. Variable effects of chronic subcutaneous administration of rotenone on striatal histology. J Comp Neurol 2004; 478(4): 418-26.
[http://dx.doi.org/10.1002/cne.20305] [PMID: 15384065]
[118]
Panov A, Dikalov S, Shalbuyeva N, Taylor G, Sherer T, Greenamyre JT. Rotenone model of Parkinson disease: Multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J Biol Chem 2005; 280(51): 42026-35.
[http://dx.doi.org/10.1074/jbc.M508628200] [PMID: 16243845]
[119]
Saravanan KS, Sindhu KM, Mohanakumar KP. Acute intranigral infusion of rotenone in rats causes progressive biochemical lesions in the striatum similar to Parkinson’s disease. Brain Res 2005; 1049(2): 147-55.
[http://dx.doi.org/10.1016/j.brainres.2005.04.051] [PMID: 15936733]
[120]
Diaz-Corrales FJ, Asanuma M, Miyazaki I, Miyoshi K, Ogawa N. Rotenone induces aggregation of γ-tubulin protein and subsequent disorganization of the centrosome: Relevance to formation of inclusion bodies and neurodegeneration. Neuroscience 2005; 133(1): 117-35.
[http://dx.doi.org/10.1016/j.neuroscience.2005.01.044] [PMID: 15893636]
[121]
Phinney AL, Andringa G, Bol JGJM, et al. Enhanced sensitivity of dopaminergic neurons to rotenone-induced toxicity with aging. Parkinsonism Relat Disord 2006; 12(4): 228-38.
[http://dx.doi.org/10.1016/j.parkreldis.2005.12.002] [PMID: 16488175]
[122]
Ravenstijn PGM, Merlini M, Hameetman M, et al. The exploration of rotenone as a toxin for inducing Parkinson’s disease in rats, for application in BBB transport and PK–PD experiments. J Pharmacol Toxicol Methods 2008; 57(2): 114-30.
[http://dx.doi.org/10.1016/j.vascn.2007.10.003] [PMID: 18155613]
[123]
Swarnkar S, Tyagi E, Agrawal R, Singh MP, Nath C. A comparative study on oxidative stress induced by LPS and rotenone in homogenates of rat brain regions. Environ Toxicol Pharmacol 2009; 27(2): 219-24.
[http://dx.doi.org/10.1016/j.etap.2008.10.003] [PMID: 21783943]
[124]
Swarnkar S, Singh S, Sharma S, Mathur R, Patro IK, Nath C. Rotenone induced neurotoxicity in rat brain areas: A histopathological study. Neurosci Lett 2011; 501(3): 123-7.
[http://dx.doi.org/10.1016/j.neulet.2011.03.036] [PMID: 21435374]
[125]
Ullrich C, Humpel C. Rotenone induces cell death of cholinergic neurons in an organotypic co-culture brain slice model. Neurochem Res 2009; 34(12): 2147-53.
[http://dx.doi.org/10.1007/s11064-009-0014-9] [PMID: 19495971]
[126]
Leuner K, Schütt T, Kurz C, et al. Mitochondrion-derived reactive oxygen species lead to enhanced amyloid beta formation. Antioxid Redox Signal 2012; 16(12): 1421-33.
[http://dx.doi.org/10.1089/ars.2011.4173] [PMID: 22229260]
[127]
Sonia Angeline M, Chaterjee P, Anand K, Ambasta RK, Kumar P. Rotenone-induced parkinsonism elicits behavioral impairments and differential expression of parkin, heat shock proteins and caspases in the rat. Neuroscience 2012; 220: 291-301.
[http://dx.doi.org/10.1016/j.neuroscience.2012.06.021] [PMID: 22710069]
[128]
Abdel-Salam OME, Khadrawy YA, Youness ER, et al. Effect of a single intrastriatal rotenone injection on oxidative stress and neurodegeneration in the rat brain. Comp Clin Pathol 2014; 23(5): 1457-67.
[http://dx.doi.org/10.1007/s00580-013-1807-4]
[129]
Murakami S, Miyazaki I, Miyoshi K, Asanuma M. Long-term systemic exposure to rotenone induces central and peripheral pathology of Parkinson’s disease in mice. Neurochem Res 2015; 40(6): 1165-78.
[http://dx.doi.org/10.1007/s11064-015-1577-2] [PMID: 25894684]
[130]
Abdel-Salam OME, Youness ER, Khadrawy YA, et al. The effect of cannabis on oxidative stress and neurodegeneration induced by intrastriatal rotenone injection in rats. Comp Clin Pathol 2015; 24(2): 359-78.
[http://dx.doi.org/10.1007/s00580-014-1907-9]
[131]
Xiong ZK, Lang J, Xu G, et al. Excessive levels of nitric oxide in rat model of Parkinson’s disease induced by rotenone. Exp Ther Med 2015; 9(2): 553-8.
[http://dx.doi.org/10.3892/etm.2014.2099] [PMID: 25574233]
[132]
Wrangel C, Schwabe K, John N, Krauss JK, Alam M. The rotenone-induced rat model of Parkinson’s disease: Behavioral and electrophysiological findings. Behav Brain Res 2015; 279: 52-61.
[http://dx.doi.org/10.1016/j.bbr.2014.11.002] [PMID: 25446762]
[133]
Zhang ZN, Zhang JS, Xiang J, et al. Subcutaneous rotenone rat model of Parkinson’s disease: Dose exploration study. Brain Res 2017; 1655: 104-13.
[http://dx.doi.org/10.1016/j.brainres.2016.11.020] [PMID: 27876560]
[134]
Dodiya HB, Forsyth CB, Voigt RM, et al. Chronic stress-induced gut dysfunction exacerbates Parkinson’s disease phenotype and pathology in a rotenone-induced mouse model of Parkinson’s disease. Neurobiol Dis 2020; 135: 104352.
[http://dx.doi.org/10.1016/j.nbd.2018.12.012] [PMID: 30579705]
[135]
Guo Z, Ruan Z, Zhang D, Liu X, Hou L, Wang Q. Rotenone impairs learning and memory in mice through microglia-mediated blood brain barrier disruption and neuronal apoptosis. Chemosphere 2022; 291(Pt 2): 132982.
[http://dx.doi.org/10.1016/j.chemosphere.2021.132982] [PMID: 34822863]

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