Regulatory Non-coding RNAs Involved in Oxidative Stress and Neuroinflammation: An Intriguing Crosstalk in Parkinsons Disease
- Authors: Khish N.1, Ghiasizadeh P.2, Rasti A.3, Moghimi O.3, Zadeh A.3, Bahiraee A.4, Ebrahimi R.5
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Affiliations:
- Department of Biology, Payam Noor University International
- Student Research Committee, Arak University of Medical Science
- Student Research Committee, Faculty of Medicine, Hormozgan University of Medical Sciences
- Department of Medical Genetics, Faculty of Medicine, Hormozgan University of Medical Sciences
- Department of Neurogenetics, Max Planck Institute for Multidisciplinary Sciences
- Issue: Vol 31, No 34 (2024)
- Pages: 5576-5597
- Section: Anti-Infectives and Infectious Diseases
- URL: https://hum-ecol.ru/0929-8673/article/view/645064
- DOI: https://doi.org/10.2174/0929867331666230817102135
- ID: 645064
Cite item
Full Text
Abstract
:Parkinsons disease (PD) is a common neurodegenerative disorder characterized by the accumulation of α-synuclein and the degeneration of dopaminergic neurons in the substantia nigra. Although the molecular bases for PD development are not fully recognized, extensive evidence has suggested that the development of PD is strongly associated with neuroinflammation. It is noteworthy that while neuroinflammation might not be a primary factor in all patients with PD, it seems to be a driving force for disease progression, and therefore, exploring the role of pathways involved in neuroinflammation is of great importance. Besides, the importance of non-coding RNAs (ncRNAs), such as microRNAs (miRNAs), long non-coding RNAs (lncRNAs), and competing endogenous RNAs (ceRNAs), has been widely studied with a focus on the pathogenesis of PD. However, there is no comprehensive review regarding the role of neuroinflammation- related ncRNAs as prospective biomarkers and therapeutic targets involved in the pathogenesis of PD, even though the number of studies connecting ncRNAs to neuroinflammatory pathways and oxidative stress has markedly increased in the last few years. Hence, the present narrative review intended to describe the crosstalk between regulatory ncRNAs and neuroinflammatory targets with respect to PD to find and propose novel combining biomarkers or therapeutic targets in clinical settings.
About the authors
Naser Khish
Department of Biology, Payam Noor University International
Email: info@benthamscience.net
Pooran Ghiasizadeh
Student Research Committee, Arak University of Medical Science
Email: info@benthamscience.net
Abolhasan Rasti
Student Research Committee, Faculty of Medicine, Hormozgan University of Medical Sciences
Email: info@benthamscience.net
Omid Moghimi
Student Research Committee, Faculty of Medicine, Hormozgan University of Medical Sciences
Email: info@benthamscience.net
Arash Zadeh
Student Research Committee, Faculty of Medicine, Hormozgan University of Medical Sciences
Email: info@benthamscience.net
Alireza Bahiraee
Department of Medical Genetics, Faculty of Medicine, Hormozgan University of Medical Sciences
Author for correspondence.
Email: info@benthamscience.net
Reyhane Ebrahimi
Department of Neurogenetics, Max Planck Institute for Multidisciplinary Sciences
Author for correspondence.
Email: info@benthamscience.net
References
- Surmeier, D.J.; Obeso, J.A.; Halliday, G.M. Selective neuronal vulnerability in Parkinson disease. Nat. Rev. Neurosci., 2017, 18(2), 101-113. doi: 10.1038/nrn.2016.178 PMID: 28104909
- Jankovic, J.; Tan, E.K. Parkinsons disease: Etiopathogenesis and treatment. J. Neurol. Neurosurg. Psychiatry, 2020, 91(8), 795-808. doi: 10.1136/jnnp-2019-322338 PMID: 32576618
- Pajares, M.; I Rojo, A.; Manda, G.; Boscá, L.; Cuadrado, A. Inflammation in Parkinsons disease: Mechanisms and therapeutic implications. Cells, 2020, 9(7), 1687. doi: 10.3390/cells9071687 PMID: 32674367
- Blauwendraat, C.; Nalls, M.A.; Singleton, A.B. The genetic architecture of Parkinsons disease. Lancet Neurol., 2020, 19(2), 170-178. doi: 10.1016/S1474-4422(19)30287-X PMID: 31521533
- Klein, C.; Westenberger, A. Genetics of Parkinsons disease. Cold Spring Harb. Perspect. Med., 2012, 2(1), a008888. doi: 10.1101/cshperspect.a008888 PMID: 22315721
- Wirdefeldt, K.; Adami, H.O.; Cole, P.; Trichopoulos, D.; Mandel, J. Epidemiology and etiology of Parkinsons disease: A review of the evidence. Eur. J. Epidemiol., 2011, 26(S1), 1-58. doi: 10.1007/s10654-011-9581-6 PMID: 21626386
- McGeer, P.L.; Itagaki, S.; Boyes, B.E.; McGeer, E.G. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinsons and Alzheimers disease brains. Neurology, 1988, 38(8), 1285-1291. doi: 10.1212/WNL.38.8.1285 PMID: 3399080
- Frank-Cannon, T.C.; Tran, T.; Ruhn, K.A.; Martinez, T.N.; Hong, J.; Marvin, M.; Hartley, M.; Treviño, I.; OBrien, D.E.; Casey, B.; Goldberg, M.S.; Tansey, M.G. Parkin deficiency increases vulnerability to inflammation-related nigral degeneration. J. Neurosci., 2008, 28(43), 10825-10834. doi: 10.1523/JNEUROSCI.3001-08.2008 PMID: 18945890
- Qin, L.; Wu, X.; Block, M.L.; Liu, Y.; Breese, G.R.; Hong, J.S.; Knapp, D.J.; Crews, F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia, 2007, 55(5), 453-462. doi: 10.1002/glia.20467 PMID: 17203472
- Ramsey, C.P.; Tansey, M.G. A survey from 2012 of evidence for the role of neuroinflammation in neurotoxin animal models of Parkinsons disease and potential molecular targets. Exp. Neurol., 2014, 256, 126-132. doi: 10.1016/j.expneurol.2013.05.014 PMID: 23726958
- Stolzenberg, E.; Berry, D.; Yang, D.; Lee, E.Y.; Kroemer, A.; Kaufman, S.; Wong, G.C.L.; Oppenheim, J.J.; Sen, S.; Fishbein, T.; Bax, A.; Harris, B.; Barbut, D.; Zasloff, M.A. A role for neuronal alpha-synuclein in gastrointestinal immunity. J. Innate Immun., 2017, 9(5), 456-463. doi: 10.1159/000477990 PMID: 28651250
- Gao, H.M.; Kotzbauer, P.T.; Uryu, K.; Leight, S.; Trojanowski, J.Q.; Lee, V.M.Y. Neuroinflammation and oxidation/nitration of α-synuclein linked to dopaminergic neurodegeneration. J. Neurosci., 2008, 28(30), 7687-7698. doi: 10.1523/JNEUROSCI.0143-07.2008 PMID: 18650345
- He, Q.; Yu, W.; Wu, J.; Chen, C.; Lou, Z.; Zhang, Q.; Zhao, J.; Wang, J.; Xiao, B. Intranasal LPS-mediated Parkinsons model challenges the pathogenesis of nasal cavity and environmental toxins. PLoS. One., 2013, 8(11), e78418. doi: 10.1371/journal.pone.0078418 PMID: 24250796
- Witoelar, A.; Jansen, I.E.; Wang, Y.; Desikan, R.S.; Gibbs, J.R.; Blauwendraat, C.; Thompson, W.K.; Hernandez, D.G.; Djurovic, S.; Schork, A.J.; Bettella, F.; Ellinghaus, D.; Franke, A.; Lie, B.A.; McEvoy, L.K.; Karlsen, T.H.; Lesage, S.; Morris, H.R.; Brice, A.; Wood, N.W.; Heutink, P.; Hardy, J.; Singleton, A.B.; Dale, A.M.; Gasser, T.; Andreassen, O.A.; Sharma, M. Genome-wide pleiotropy between Parkinson disease and autoimmune diseases. JAMA Neurol., 2017, 74(7), 780-792. doi: 10.1001/jamaneurol.2017.0469 PMID: 28586827
- Stojkovska, I.; Wagner, B.M.; Morrison, B.E. Parkinsons disease and enhanced inflammatory response. Exp. Biol. Med., 2015, 240(11), 1387-1395. doi: 10.1177/1535370215576313 PMID: 25769314
- Chen, Z.; Trapp, B.D. Microglia and neuroprotection. J. Neurochem., 2016, 136(S1), 10-17. doi: 10.1111/jnc.13062 PMID: 25693054
- Liu, T.W.; Chen, C.M.; Chang, K.H. Biomarker of neuroinflammation in Parkinsons disease. Int. J. Mol. Sci., 2022, 23(8), 4148. doi: 10.3390/ijms23084148 PMID: 35456966
- Watson, C.N.; Belli, A.; Di Pietro, V. Small non-coding RNAs: New class of biomarkers and potential therapeutic targets in neurodegenerative disease. Front. Genet., 2019, 10, 364. doi: 10.3389/fgene.2019.00364 PMID: 31080456
- Ebrahimi, R.; Golestani, A. The emerging role of noncoding RNAs in neuroinflammation: Implications in pathogenesis and therapeutic approaches. J. Cell. Physiol., 2022, 237(2), 1206-1224. doi: 10.1002/jcp.30624 PMID: 34724212
- Moayedi, K.; Orandi, S.; Ebrahimi, R.; Tanhapour, M.; Moradi, M.; Abbastabar, M.; Golestani, A. A novel approach to type 3 diabetes mechanism: The interplay between noncoding RNAs and insulin signaling pathway in Alzheimers disease. J. Cell. Physiol., 2022, 237(7), 2838-2861. doi: 10.1002/jcp.30779 PMID: 35580144
- Bahiraee, A.; Ebrahimi, R. A noble pathological role for alpha-synuclein in triggering neurodegeneration of Parkinsons disease. Mov. Disord., 2018, 33(3), 404. doi: 10.1002/mds.27306 PMID: 29418023
- Stoker, T.B.; Greenland, J.C. Parkinsons Disease: Pathogenesis and Clinical Aspects; Codon Publications: Brisbane (AU), 2018.
- Kuo, M.C.; Liu, S.C.H.; Hsu, Y.F.; Wu, R.M. The role of noncoding RNAs in Parkinsons disease: Biomarkers and associations with pathogenic pathways. J. Biomed. Sci., 2021, 28(1), 78. doi: 10.1186/s12929-021-00775-x PMID: 34794432
- Tehrani, S.S.; Ebrahimi, R.; Al-E-Ahmad, A.; Panahi, G.; Meshkani, R.; Younesi, S.; Saadat, P.; Parsian, H. Competing endogenous RNAs (CeRNAs): Novel network in neurological disorders. Curr. Med. Chem., 2021, 28(29), 5983-6010. doi: 10.2174/1875533XMTEy1NTAiz PMID: 33334276
- Drepper, C.; Sendtner, M. A new postal code for dendritic mRNA transport in neurons. EMBO Rep., 2011, 12(7), 614-616. doi: 10.1038/embor.2011.119 PMID: 21681203
- Li, S.; Bi, G.; Han, S.; Huang, R. MicroRNAs play a role in Parkinsons Disease by regulating microglia function: From pathogenetic involvement to therapeutic potential. Front. Mol. Neurosci., 2022, 14, 744942. doi: 10.3389/fnmol.2021.744942 PMID: 35126050
- Konovalova, J.; Gerasymchuk, D.; Parkkinen, I.; Chmielarz, P.; Domanskyi, A. Interplay between MicroRNAs and oxidative stress in neurodegenerative diseases. Int. J. Mol. Sci., 2019, 20(23), 6055. doi: 10.3390/ijms20236055 PMID: 31801298
- Aghabozorgi, A.S.; Ahangari, N.; Eftekhaari, T.E.; Torbati, P.N.; Bahiraee, A.; Ebrahimi, R.; Pasdar, A. Circulating exosomal miRNAs in cardiovascular disease pathogenesis: New emerging hopes. J. Cell. Physiol., 2019, 234(12), 21796-21809. doi: 10.1002/jcp.28942 PMID: 31273798
- Abbastabar, M.; Sarfi, M.; Golestani, A.; Khalili, E. lncRNA involvement in hepatocellular carcinoma metastasis and prognosis. EXCLI J., 2018, 17, 900-913. PMID: 30564069
- Ebrahimi, R.; Toolabi, K.; Jannat Ali Pour, N.; Mohassel Azadi, S.; Bahiraee, A.; Zamani-Garmsiri, F.; Emamgholipour, S. Adipose tissue gene expression of long non-coding RNAs; MALAT1, TUG1 in obesity: is it associated with metabolic profile and lipid homeostasis-related genes expression? Diabetol. Metab. Syndr., 2020, 12(1), 36. doi: 10.1186/s13098-020-00544-0 PMID: 32368256
- Salta, E.; De Strooper, B. Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol., 2012, 11(2), 189-200. doi: 10.1016/S1474-4422(11)70286-1 PMID: 22265214
- Lyu, Y.; Bai, L.; Qin, C. Long noncoding RNAs in neurodevelopment and Parkinsons disease. Animal Model. Exp. Med., 2019, 2(4), 239-251. doi: 10.1002/ame2.12093 PMID: 31942556
- Jiang, H.; Zhang, Y.; Yue, J.; Shi, Y.; Xiao, B.; Xiao, W.; Luo, Z. Non-coding RNAs: The neuroinflammatory regulators in neurodegenerative diseases. Front. Neurol., 2022, 13, 929290. doi: 10.3389/fneur.2022.929290 PMID: 36034298
- Manna, I; Quattrone, A; De Benedittis, S; Iaccino, E; Quattrone, A. Roles of non-coding RNAs as novel diagnostic biomarkers in Parkinson's disease. J. Parkinsons Dis., 2021, 11(4), 1475-1489. doi: 10.3233/JPD-212726
- Nuzziello, N.; Liguori, M. The MicroRNA centrism in the orchestration of neuroinflammation in neurodegenerative diseases. Cells, 2019, 8(10), 1193. doi: 10.3390/cells8101193 PMID: 31581723
- Dias, V.; Junn, E.; Mouradian, M.M. The role of oxidative stress in Parkinsons disease. J. Parkinsons Dis., 2013, 3(4), 461-491. doi: 10.3233/JPD-130230 PMID: 24252804
- Golestani, A.; Rastegar, R.; Shariftabrizi, A.; Khaghani, S.; Payabvash, S.M.; Salmasi, A.H.; Dehpour, A.R.; Pasalar, P. Paradoxical dose- and time-dependent regulation of superoxide dismutase and antioxidant capacity by vitamin E in rat. Clin. Chim. Acta, 2006, 365(1-2), 153-159. doi: 10.1016/j.cca.2005.08.008 PMID: 16183047
- Zhang, S.; Wang, R.; Wang, G. Impact of dopamine oxidation on dopaminergic neurodegeneration. ACS Chem. Neurosci., 2019, 10(2), 945-953. doi: 10.1021/acschemneuro.8b00454 PMID: 30592597
- Lohr, K.M.; Miller, G.W. VMAT2 and Parkinsons disease: Harnessing the dopamine vesicle. Expert Rev. Neurother., 2014, 14(10), 1115-1117. doi: 10.1586/14737175.2014.960399 PMID: 25220836
- Hwang, D.Y.; Hong, S.; Jeong, J.W.; Choi, S.; Kim, H.; Kim, J.; Kim, K.S. Vesicular monoamine transporter 2 and dopamine transporter are molecular targets of Pitx3 in the ventral midbrain dopamine neurons. J. Neurochem., 2009, 111(5), 1202-1212. doi: 10.1111/j.1471-4159.2009.06404.x PMID: 19780901
- Li, Y.; Li, C.; Chen, Z.; He, J.; Tao, Z.; Yin, Z.Q. A MicroRNA, mir133b, suppresses melanopsin expression mediated by failure dopaminergic amacrine cells in RCS rats. Cell. Signal., 2012, 24(3), 685-698. doi: 10.1016/j.cellsig.2011.10.017 PMID: 22101014
- Caudle, W.M.; Richardson, J.R.; Wang, M.Z.; Taylor, T.N.; Guillot, T.S.; McCormack, A.L.; Colebrooke, R.E.; Di Monte, D.A.; Emson, P.C.; Miller, G.W. Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J. Neurosci., 2007, 27(30), 8138-8148. doi: 10.1523/JNEUROSCI.0319-07.2007 PMID: 17652604
- Kim, J.; Inoue, K.; Ishii, J.; Vanti, W.B.; Voronov, S.V.; Murchison, E.; Hannon, G.; Abeliovich, A. A MicroRNA feedback circuit in midbrain dopamine neurons. Science, 2007, 317(5842), 1220-1224. doi: 10.1126/science.1140481 PMID: 17761882
- Jia, X.; Wang, F.; Han, Y.; Geng, X.; Li, M.; Shi, Y.; Lu, L.; Chen, Y. miR-137 and miR-491 negatively regulate dopamine transporter expression and function in neural cells. Neurosci. Bull., 2016, 32(6), 512-522. doi: 10.1007/s12264-016-0061-6 PMID: 27628529
- Choi, J.; Sullards, M.C.; Olzmann, J.A.; Rees, H.D.; Weintraub, S.T.; Bostwick, D.E.; Gearing, M.; Levey, A.I.; Chin, L.S.; Li, L. Oxidative damage of DJ-1 is linked to sporadic Parkinson and Alzheimer diseases. J. Biol. Chem., 2006, 281(16), 10816-10824. doi: 10.1074/jbc.M509079200 PMID: 16517609
- Hayashi, T.; Ishimori, C.; Takahashi-Niki, K.; Taira, T.; Kim, Y.; Maita, H.; Maita, C.; Ariga, H.; Iguchi-Ariga, S.M.M. DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem. Biophys. Res. Commun., 2009, 390(3), 667-672. doi: 10.1016/j.bbrc.2009.10.025 PMID: 19822128
- Ariga, H.; Takahashi-Niki, K.; Kato, I.; Maita, H.; Niki, T.; Iguchi-Ariga, S.M. Neuroprotective function of DJ-1 in Parkinsons disease. Oxid. Med. Cell Longev., 2013, 2013, 683920.
- Xiong, R.; Wang, Z.; Zhao, Z.; Li, H.; Chen, W.; Zhang, B.; Wang, L.; Wu, L.; Li, W.; Ding, J.; Chen, S. MicroRNA-494 reduces DJ-1 expression and exacerbates neurodegeneration. Neurobiol. Aging, 2014, 35(3), 705-714. doi: 10.1016/j.neurobiolaging.2013.09.027 PMID: 24269020
- Oh, S.E.; Park, H.J.; He, L.; Skibiel, C.; Junn, E.; Mouradian, M.M. The Parkinsons disease gene product DJ-1 modulates miR-221 to promote neuronal survival against oxidative stress. Redox Biol., 2018, 19, 62-73. doi: 10.1016/j.redox.2018.07.021 PMID: 30107296
- Chen, Y.; Gao, C.; Sun, Q.; Pan, H.; Huang, P.; Ding, J.; Chen, S. MicroRNA-4639 is a regulator of DJ-1 expression and a potential early diagnostic marker for Parkinsons disease. Front. Aging Neurosci., 2017, 9, 232. doi: 10.3389/fnagi.2017.00232 PMID: 28785216
- Miñones-Moyano, E.; Porta, S.; Escaramís, G.; Rabionet, R.; Iraola, S.; Kagerbauer, B.; Espinosa-Parrilla, Y.; Ferrer, I.; Estivill, X.; Martí, E. MicroRNA profiling of Parkinsons disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum. Mol. Genet., 2011, 20(15), 3067-3078. doi: 10.1093/hmg/ddr210 PMID: 21558425
- Barodia, S.K.; Creed, R.B.; Goldberg, M.S. Parkin and PINK1 functions in oxidative stress and neurodegeneration. Brain Res. Bull., 2017, 133, 51-59. doi: 10.1016/j.brainresbull.2016.12.004 PMID: 28017782
- Wang, H.L.; Chou, A.H.; Wu, A.S.; Chen, S.Y.; Weng, Y.H.; Kao, Y.C.; Yeh, T.H.; Chu, P.J.; Lu, C.S. PARK6 PINK1 mutants are defective in maintaining mitochondrial membrane potential and inhibiting ROS formation of substantia nigra dopaminergic neurons. Biochim. Biophys. Acta Mol. Basis Dis., 2011, 1812(6), 674-684. doi: 10.1016/j.bbadis.2011.03.007 PMID: 21421046
- Wood-Kaczmar, A.; Gandhi, S.; Yao, Z.; Abramov, A.S.Y.; Miljan, E.A.; Keen, G.; Stanyer, L.; Hargreaves, I.; Klupsch, K.; Deas, E.; Downward, J.; Mansfield, L.; Jat, P.; Taylor, J.; Heales, S.; Duchen, M.R.; Latchman, D.; Tabrizi, S.J.; Wood, N.W. PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS. One., 2008, 3(6), e2455. doi: 10.1371/journal.pone.0002455 PMID: 18560593
- Kim, J.; Fiesel, F.C.; Belmonte, K.C.; Hudec, R.; Wang, W.X.; Kim, C.; Nelson, P.T.; Springer, W.; Kim, J. miR-27a and miR-27b regulate autophagic clearance of damaged mitochondria by targeting PTEN-induced putative kinase 1 (PINK1). Mol. Neurodegener., 2016, 11(1), 55. doi: 10.1186/s13024-016-0121-4 PMID: 27456084
- Hajiani, M.; Golestani, A.; Shariftabrizi, A.; Rastegar, R.; Payabvash, S.; Hassanzadeh Salmasi, A.; Reza Dehpour, A.; Pasalar, P. Dose-dependent modulation of systemic lipid peroxidation and activity of anti-oxidant enzymes by vitamin E in the rat. Redox Rep., 2008, 13(2), 60-66. doi: 10.1179/135100008X259114 PMID: 18339248
- Kabaria, S.; Choi, D.C.; Chaudhuri, A.D.; Jain, M.R.; Li, H.; Junn, E. MicroRNA-7 activates Nrf2 pathway by targeting Keap1 expression. Free Radic. Biol. Med., 2015, 89, 548-556. doi: 10.1016/j.freeradbiomed.2015.09.010 PMID: 26453926
- Narasimhan, M.; Patel, D.; Vedpathak, D.; Rathinam, M.; Henderson, G.; Mahimainathan, L. Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells. PLoS. One., 2012, 7(12), e51111. doi: 10.1371/journal.pone.0051111 PMID: 23236440
- Cressatti, M.; Song, W.; Turk, A.Z.; Garabed, L.R.; Benchaya, J.A.; Galindez, C.; Liberman, A.; Schipper, H.M. Glial HMOX1 expression promotes central and peripheral α-synuclein dysregulation and pathogenicity in parkinsonian mice. Glia., 2019, 67(9), 1730-1744. PMID: 31180611
- Wang, J.; Le, T.; Wei, R.; Jiao, Y. Knockdown of JMJD1C, a target gene of hsa-miR-590-3p, inhibits mitochondrial dysfunction and oxidative stress in MPP+-treated MES23.5 and SH-SY5Y cells. Cell. Mol. Biol., 2016, 62(3), 39-45. PMID: 27064872
- Farrer, M.J. Genetics of Parkinson disease: Paradigm shifts and future prospects. Nat. Rev. Genet., 2006, 7(4), 306-318. doi: 10.1038/nrg1831 PMID: 16543934
- Thome, A.D.; Harms, A.S.; Volpicelli-Daley, L.A.; Standaert, D.G. microRNA-155 regulates alpha-synuclein-induced inflammatory responses in models of Parkinson disease. J. Neurosci., 2016, 36(8), 2383-2390. doi: 10.1523/JNEUROSCI.3900-15.2016 PMID: 26911687
- Recasens, A.; Perier, C.; Sue, C.M. Role of microRNAs in the regulation of α-synuclein expression: A systematic review. Front. Mol. Neurosci., 2016, 9, 128. doi: 10.3389/fnmol.2016.00128 PMID: 27917109
- Su, Q.; Chen, N.; Tang, J.; Wang, J.; Chou, W.C.; Zheng, F.; Shao, W.; Yu, G.; Cai, P.; Guo, Z.; He, M.; Li, H.; Wu, S. Paraquat-induced oxidative stress regulates N6-methyladenosine (m6A) modification of long noncoding RNAs in Neuro-2a cells. Ecotoxicol. Environ. Saf., 2022, 237, 113503. doi: 10.1016/j.ecoenv.2022.113503 PMID: 35453019
- Simchovitz, A.; Hanan, M.; Yayon, N.; Lee, S.; Bennett, E.R.; Greenberg, D.S.; Kadener, S.; Soreq, H. A lncRNA survey finds increases in neuroprotective LINC-PINT in Parkinsons disease Substantia nigra. Aging. Cell., 2020, 19(3), e13115. doi: 10.1111/acel.13115 PMID: 32080970
- Simchovitz, A.; Hanan, M.; Niederhoffer, N.; Madrer, N.; Yayon, N.; Bennett, E.R.; Greenberg, D.S.; Kadener, S.; Soreq, H. NEAT1 is overexpressed in Parkinsons disease substantia nigra and confers drug-inducible neuroprotection from oxidative stress. FASEB J., 2019, 33(10), 11223-11234. doi: 10.1096/fj.201900830R PMID: 31311324
- Zhou, S.; Zhang, D.; Guo, J.; Chen, Z.; Chen, Y.; Zhang, J. Deficiency of NEAT1 prevented MPP+-induced inflammatory response, oxidative stress and apoptosis in dopaminergic SK-N-SH neuroblastoma cells via miR-1277-5p/ARHGAP26 axis. Brain Res., 2021, 1750, 147156. doi: 10.1016/j.brainres.2020.147156 PMID: 33069733
- Meng, C.; Gao, J.; Ma, Q.; Sun, Q.; Qiao, T. LINC00943 knockdown attenuates MPP+-induced neuronal damage via miR-15b-5p/RAB3IP axis in SK-N-SH cells. Neurol. Res., 2021, 43(3), 181-190. doi: 10.1080/01616412.2020.1834290 PMID: 33208053
- Lang, Y.; Zhang, H.; Yu, H.; Li, Y.; Liu, X.; Li, M. Long non-coding RNA myocardial infarction-associated transcript promotes 1-Methyl-4-phenylpyridinium ion-induced neuronal inflammation and oxidative stress in Parkinsons disease through regulating microRNA-221-3p/transforming growth factor/nuclear factor E2-related factor 2 axis. Bioengineered, 2022, 13(1), 930-940. doi: 10.1080/21655979.2021.2015527 PMID: 34967706
- Zhou, S.; Zhang, D.; Guo, J.; Chen, Z.; Chen, Y.; Zhang, J. Long non-coding RNA NORAD functions as a MICRORNA-204-5P sponge to repress the progression of Parkinsons disease in vitro by increasing the solute carrier family 5 member 3 expression. IUBMB. Life., 2020, 72(9), 2045-2055. doi: 10.1002/iub.2344 PMID: 32687247
- Ding, X.M.; Zhao, L.J.; Qiao, H.Y.; Wu, S.L.; Wang, X.H. Long non-coding RNA-p21 regulates MPP+-induced neuronal injury by targeting miR-625 and derepressing TRPM2 in SH-SY5Y cells. Chem. Biol. Interact., 2019, 307, 73-81. doi: 10.1016/j.cbi.2019.04.017 PMID: 31004593
- Li, Y.; Fang, J.; Zhou, Z.; Zhou, Q.; Sun, S.; Jin, Z.; Xi, Z.; Wei, J. Downregulation of lncRNA BACE1-AS improves dopamine-dependent oxidative stress in rats with Parkinsons disease by upregulating microRNA-34b-5p and downregulating BACE1. Cell Cycle, 2020, 19(10), 1158-1171. doi: 10.1080/15384101.2020.1749447 PMID: 32308102
- Yan, L.; Li, L.; Lei, J. Long noncoding RNA small nucleolar RNA host gene 12/microRNA-138-5p/nuclear factor I/B regulates neuronal apoptosis, inflammatory response, and oxidative stress in Parkinsons disease. Bioengineered., 2021, 12(2), 12867-12879. doi: 10.1080/21655979.2021.2005928 PMID: 34783303
- Guo, Y.; Liu, Y.; Wang, H.; Liu, P. Long noncoding RNA SRY-box transcription factor 2 overlapping transcript participates in Parkinsons disease by regulating the microRNA-942-5p/nuclear apoptosis-inducing factor 1 axis. Bioengineered., 2021, 12(1), 8570-8582. doi: 10.1080/21655979.2021.1987126 PMID: 34607512
- Jin, M.; Yang, F.; Yang, I.; Yin, Y.; Luo, J.J.; Wang, H.; Yang, X.F. Uric acid, hyperuricemia and vascular diseases. Front. Biosci., 2012, 17(1), 656-669. doi: 10.2741/3950 PMID: 22201767
- Xu, C.; Bailly-Maitre, B.; Reed, J.C. Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Invest., 2005, 115(10), 2656-2664. doi: 10.1172/JCI26373 PMID: 16200199
- Zhang, S.X.; Sanders, E.; Fliesler, S.J.; Wang, J.J. Endoplasmic reticulum stress and the unfolded protein responses in retinal degeneration. Exp. Eye Res., 2014, 125, 30-40. doi: 10.1016/j.exer.2014.04.015 PMID: 24792589
- Zhang, K.; Kaufman, R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature, 2008, 454(7203), 455-462. doi: 10.1038/nature07203 PMID: 18650916
- Xiang, C.; Wang, Y.; Zhang, H.; Han, F. The role of endoplasmic reticulum stress in neurodegenerative disease. Apoptosis, 2017, 22(1), 1-26. doi: 10.1007/s10495-016-1296-4 PMID: 27815720
- Jiang, M.; Yun, Q.; Shi, F.; Niu, G.; Gao, Y.; Xie, S.; Yu, S. Downregulation of miR-384-5p attenuates rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through inhibiting endoplasmic reticulum stress. Am. J. Physiol. Cell Physiol., 2016, 310(9), C755-C763. doi: 10.1152/ajpcell.00226.2015 PMID: 26864693
- Ge, B.; Li, S.; Li, F. Astragaloside-IV regulates endoplasmic reticulum stress-mediated neuronal apoptosis in a murine model of Parkinsons disease via the lincRNA-p21/CHOP pathway. Exp. Mol. Pathol., 2020, 115, 104478. doi: 10.1016/j.yexmp.2020.104478 PMID: 32511947
- Erta, M.; Quintana, A.; Hidalgo, J. Interleukin-6, a major cytokine in the central nervous system. Int. J. Biol. Sci., 2012, 8(9), 1254-1266. doi: 10.7150/ijbs.4679 PMID: 23136554
- Bahiraee, A.; Ebrahimi, R.; Halabian, R.; Aghabozorgi, A.S.; Amani, J. The role of inflammation and its related microRNAs in breast cancer: A narrative review. J. Cell. Physiol., 2019, 234(11), 19480-19493. doi: 10.1002/jcp.28742 PMID: 31025369
- Mameli, G.; Arru, G.; Caggiu, E.; Niegowska, M.; Leoni, S.; Madeddu, G.; Babudieri, S.; Sechi, G.P.; Sechi, L.A. Natalizumab therapy modulates miR-155, miR-26a and proinflammatory cytokine expression in MS patients. PLoS One, 2016, 11(6), e0157153. doi: 10.1371/journal.pone.0157153 PMID: 27310932
- Li, B.; Wang, X.; Choi, I.Y.; Wang, Y.C.; Liu, S.; Pham, A.T.; Moon, H.; Smith, D.J.; Rao, D.S.; Boldin, M.P.; Yang, L. miR-146a modulates autoreactive Th17 cell differentiation and regulates organ-specific autoimmunity. J. Clin. Invest., 2017, 127(10), 3702-3716. doi: 10.1172/JCI94012 PMID: 28872459
- Wu, D.; Cerutti, C.; Lopez-Ramirez, M.A.; Pryce, G.; King-Robson, J.; Simpson, J.E.; van der Pol, S.M.A.; Hirst, M.C.; de Vries, H.E.; Sharrack, B.; Baker, D.; Male, D.K.; Michael, G.J.; Romero, I.A. Brain endothelial miR-146a negatively modulates T-cell adhesion through repressing multiple targets to inhibit NF-κB activation. J. Cereb. Blood Flow Metab., 2015, 35(3), 412-423. doi: 10.1038/jcbfm.2014.207 PMID: 25515214
- Lian, H.; Wang, B.; Lu, Q.; Chen, B.; Yang, H. LINC00943 knockdown exerts neuroprotective effects in Parkinsons disease through regulates CXCL12 expression by sponging miR-7-5p. Genes Genomics, 2021, 43(7), 797-805. doi: 10.1007/s13258-021-01084-1 PMID: 33886117
- Deng, M.; Du, G.; Zhao, J.; Du, X. miR-146a negatively regulates the induction of proinflammatory cytokines in response to Japanese encephalitis virus infection in microglial cells. Arch. Virol., 2017, 162(6), 1495-1505. doi: 10.1007/s00705-017-3226-3 PMID: 28190197
- Hofmann, K.W.; Schuh, A.F.S.; Saute, J.; Townsend, R.; Fricke, D.; Leke, R.; Souza, D.O.; Portela, L.V.; Chaves, M.L.F.; Rieder, C.R.M. Interleukin-6 serum levels in patients with Parkinsons disease. Neurochem. Res., 2009, 34(8), 1401-1404. doi: 10.1007/s11064-009-9921-z PMID: 19214748
- Sébire, G.; Emilie, D.; Wallon, C.; Héry, C.; Devergne, O.; Delfraissy, J.F.; Galanaud, P.; Tardieu, M. In vitro production of IL-6, IL-1 beta, and tumor necrosis factor-alpha by human embryonic microglial and neural cells. J. Immunol., 1993, 150(4), 1517-1523. doi: 10.4049/jimmunol.150.4.1517 PMID: 8432992
- Song, Y.; Liu, Y.; Chen, X. MiR-212 attenuates MPP+-induced neuronal damage by targeting KLF4 in SH-SY5Y cells. Yonsei Med. J., 2018, 59(3), 416-424. doi: 10.3349/ymj.2018.59.3.416 PMID: 29611404
- He, Q; Wang, Q; Yuan, C; Wang, Y. Downregulation of miR-7116-5p in microglia by MPP(+) sensitizes TNF-α production to induce dopaminergic neuron damage. Glia., 2017, 65(8), 1251-1263.
- Ren, Y.; Li, H.; Xie, W.; Wei, N.; Liu, M. MicroRNA-195 triggers neuroinflammation in Parkinsons disease in a Rho-associated kinase 1-dependent manner. Mol. Med. Rep., 2019, 19(6), 5153-5161. doi: 10.3892/mmr.2019.10176 PMID: 31059087
- Cheng, J; Duan, Y; Zhang, F; Shi, J; Li, H; Wang, F The role of lncRNA TUG1 in the parkinson disease and its effect on microglial inflammatory response. Neuromolecular Med., 2021, 23(2), 327-334. doi: 10.1007/s12017-020-08626-y
- Ma, X.; Wang, Y.; Yin, H.; Hua, L.; Zhang, X.; Xiao, J.; Yuan, Q.; Wang, S.; Liu, Y.; Zhang, S.; Wang, Y. Down-regulated long non-coding RNA RMST ameliorates dopaminergic neuron damage in Parkinsons disease rats via regulation of TLR/NF-κB signaling pathway. Brain Res. Bull., 2021, 174, 22-30. doi: 10.1016/j.brainresbull.2021.04.026 PMID: 33933526
- Xu, W.; Zhang, L.; Geng, Y.; Liu, Y.; Zhang, N. Long noncoding RNA GAS5 promotes microglial inflammatory response in Parkinsons disease by regulating NLRP3 pathway through sponging miR-223-3p. Int. Immunopharmacol., 2020, 85, 106614. doi: 10.1016/j.intimp.2020.106614 PMID: 32470877
- Wang, H.; Wang, X.; Zhang, Y.; Zhao, J. LncRNA SNHG1 promotes neuronal injury in Parkinsons disease cell model by miR-181a-5p/CXCL12 axis. J. Mol. Histol., 2021, 52(2), 153-163. doi: 10.1007/s10735-020-09931-3 PMID: 33389428
- Han, Y.; Kang, C.; Kang, M.; Quan, W.; Gao, H.; Zhong, Z. RETRACTED: Long non-coding RNA Mirt2 prevents TNF-α-triggered inflammation via the repression of microRNA-101. Int. Immunopharmacol., 2019, 76, 105878. doi: 10.1016/j.intimp.2019.105878 PMID: 31513985
- Zhao, Y; Xie, Y; Yao, WY; Wang, YY; Song, N Long non-coding RNA Mirt2 prevents TNF-α-triggered inflammation via the repression of microRNA-101. Int. Immunopharmacol., 2022, 76, 105878.
- Wu, Q.; Ye, X.; Xiong, Y.; Zhu, H.; Miao, J.; Zhang, W.; Wan, J. The protective role of microRNA-200c in Alzheimers disease pathologies is induced by beta amyloid-triggered endoplasmic reticulum stress. Front. Mol. Neurosci., 2016, 9, 140. doi: 10.3389/fnmol.2016.00140 PMID: 28008308
- Li, H.; Yu, L.; Li, M.; Chen, X.; Tian, Q.; Jiang, Y.; Li, N. MicroRNA-150 serves as a diagnostic biomarker and is involved in the inflammatory pathogenesis of Parkinsons disease. Mol. Genet. Genomic Med., 2020, 8(4), e1189. doi: 10.1002/mgg3.1189 PMID: 32077254
- Emamgholipour, S.; Ebrahimi, R.; Bahiraee, A.; Niazpour, F.; Meshkani, R. Acetylation and insulin resistance: A focus on metabolic and mitogenic cascades of insulin signaling. Crit. Rev. Clin. Lab. Sci., 2020, 57(3), 196-214. doi: 10.1080/10408363.2019.1699498 PMID: 31894999
- Ebrahimi, R.; Bahiraee, A.; Niazpour, F.; Emamgholipour, S.; Meshkani, R. The role of microRNAs in the regulation of insulin signaling pathway with respect to metabolic and mitogenic cascades: A review. J. Cell. Biochem., 2019, 120(12), 19290-19309. doi: 10.1002/jcb.29299 PMID: 31364207
- Sánchez-Alegría, K.; Flores-León, M.; Avila-Muñoz, E.; Rodríguez-Corona, N.; Arias, C. PI3K signaling in neurons: A central node for the control of multiple functions. Int. J. Mol. Sci., 2018, 19(12), 3725. doi: 10.3390/ijms19123725 PMID: 30477115
- Long, H.Z.; Cheng, Y.; Zhou, Z.W.; Luo, H.Y.; Wen, D.D.; Gao, L.C. PI3K/AKT signal pathway: A target of natural products in the prevention and treatment of Alzheimers disease and Parkinsons disease. Front. Pharmacol., 2021, 12, 648636. doi: 10.3389/fphar.2021.648636 PMID: 33935751
- Zhou, T.; Lin, D.; Chen, Y.; Peng, S.; Jing, X.; Lei, M.; Tao, E.; Liang, Y. α-synuclein accumulation in SH-SY5Y cell impairs autophagy in microglia by exosomes overloading miR-19a-3p. Epigenomics, 2019, 11(15), 1661-1677. doi: 10.2217/epi-2019-0222 PMID: 31646884
- OConnell, R.M.; Chaudhuri, A.A.; Rao, D.S.; Baltimore, D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc. Natl. Acad. Sci., 2009, 106(17), 7113-7118. doi: 10.1073/pnas.0902636106 PMID: 19359473
- Caggiu, E.; Paulus, K.; Mameli, G.; Arru, G.; Sechi, G.P.; Sechi, L.A. Differential expression of miRNA 155 and miRNA 146a in Parkinsons disease patients. eNeurologicalSci, 2018, 13, 1-4. doi: 10.1016/j.ensci.2018.09.002 PMID: 30255159
- Cai, L.; Tu, L.; Li, T.; Yang, X.; Ren, Y.; Gu, R.; Zhang, Q.; Yao, H.; Qu, X.; Wang, Q.; Tian, J. Downregulation of lncRNA UCA1 ameliorates the damage of dopaminergic neurons, reduces oxidative stress and inflammation in Parkinsons disease through the inhibition of the PI3K/Akt signaling pathway. Int. Immunopharmacol., 2019, 75, 105734. doi: 10.1016/j.intimp.2019.105734 PMID: 31301558
- Ma, J.; Sun, W.; Chen, S.; Wang, Z.; Zheng, J.; Shi, X.; Li, M.; Li, D.; Gu, Q. The long noncoding RNA GAS5 potentiates neuronal injury in Parkinsons disease by binding to microRNA-150 to regulate Fosl1 expression. Exp. Neurol., 2022, 347, 113904. doi: 10.1016/j.expneurol.2021.113904 PMID: 34755654
- Zhai, K.; Liu, B.; Gao, L. Long-noncoding RNA TUG1 promotes Parkinsons disease via modulating MiR-152-3p/PTEN pathway. Hum. Gene Ther., 2020, 31(23-24), 1274-1287. doi: 10.1089/hum.2020.106 PMID: 32808542
- Zhao, J.; Geng, L.; Chen, Y.; Wu, C. SNHG1 promotes MPP+-induced cytotoxicity by regulating PTEN/AKT/mTOR signaling pathway in SH-SY5Y cells via sponging miR-153-3p. Biol. Res., 2020, 53(1), 1. doi: 10.1186/s40659-019-0267-y PMID: 31907031
- Fan, J; Wu, D; Guo, Y; Yang, Z. OS1-IT1 silencing alleviates MPP(+)-induced neuronal cell injury through regulating the miR-124-3p/PTEN/AKT/mTOR pathway. J. Clin. Neurosci., 2022, 99, 137-146.
- Shih, R.H.; Wang, C.Y.; Yang, C.M. NF-kappaB signaling pathways in neurological inflammation: A mini review. Front. Mol. Neurosci., 2015, 8, 77. doi: 10.3389/fnmol.2015.00077 PMID: 26733801
- Yu, L.; Li, L.; Medeiros, L.J.; Young, K.H. NF-κB signaling pathway and its potential as a target for therapy in lymphoid neoplasms. Blood Rev., 2017, 31(2), 77-92. doi: 10.1016/j.blre.2016.10.001 PMID: 27773462
- Bellucci, A.; Bubacco, L.; Longhena, F.; Parrella, E.; Faustini, G.; Porrini, V.; Bono, F.; Missale, C.; Pizzi, M. Nuclear Factor-κB dysregulation and α-synuclein pathology: Critical interplay in the pathogenesis of Parkinsons disease. Front. Aging Neurosci., 2020, 12, 68. doi: 10.3389/fnagi.2020.00068 PMID: 32265684
- Huang, D.B.; Vu, D.; Ghosh, G. NF-kappaB RelB forms an intertwined homodimer. Structure., 2005, 13(9), 1365-1373. doi: 10.1016/j.str.2005.06.018 PMID: 16154093
- Ghosh, A.; Roy, A.; Liu, X.; Kordower, J.H.; Mufson, E.J.; Hartley, D.M.; Ghosh, S.; Mosley, R.L.; Gendelman, H.E.; Pahan, K. Selective inhibition of NF-κB activation prevents dopaminergic neuronal loss in a mouse model of Parkinsons disease. Proc. Natl. Acad. Sci., 2007, 104(47), 18754-18759. doi: 10.1073/pnas.0704908104 PMID: 18000063
- Chaudhuri, AD; Kabaria, S; Choi, DC; Mouradian, MM; Junn, E MicroRNA-7 promotes glycolysis to protect against 1-methyl-4-phenylpyridinium-induced cell death. J. Biol. Chem., 2015, 290(19), 12425-12434.
- Choi, DC; Chae, YJ; Kabaria, S; Chaudhuri, AD; Jain, MR; Li, H MicroRNA-7 protects against 1-methyl-4-phenylpyridinium-induced cell death by targeting RelA. J Neurosci., 2014, 34(38), 12725-12737.
- Li, X.; Su, Y.; Li, N.; Zhang, F.R.; Zhang, N. Berberine attenuates MPP+-induced neuronal injury by regulating LINC00943/miR-142-5p/KPNA4/NF-κB pathway in SK-N-SH Cells. Neurochem. Res., 2021, 46(12), 3286-3300. doi: 10.1007/s11064-021-03431-w PMID: 34427876
- Cao, H.; Han, X.; Jia, Y.; Zhang, B. Inhibition of long non-coding RNA HOXA11-AS against neuroinflammation in Parkinsons disease model via targeting miR-124-3p mediated FSTL1/NF-κB axis. Aging., 2021, 13(8), 11455-11469. doi: 10.18632/aging.202837 PMID: 33839699
- Zhang, H.; Wang, Z.; Hu, K.; Liu, H. Downregulation of long noncoding RNA SNHG7 protects against inflammation and apoptosis in Parkinsons disease model by targeting the miR-425-5p/TRAF5/NF-κB axis. J. Biochem. Mol. Toxicol., 2021, 35(10), e22867. doi: 10.1002/jbt.22867 PMID: 34369042
- Ghafouri-Fard, S.; Gholipour, M.; Abak, A.; Mazdeh, M.; Taheri, M.; Sayad, A. Expression analysis of NF-κB-related lncRNAs in Parkinsons disease. Front. Immunol., 2021, 12, 755246. doi: 10.3389/fimmu.2021.755246 PMID: 34721431
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