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Current Neuropharmacology

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ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

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General Review Article

Paraquat and Parkinson’s Disease: The Molecular Crosstalk of Upstream Signal Transduction Pathways Leading to Apoptosis

Author(s): Wesley Zhi Chung See, Rakesh Naidu and Kim San Tang*

Volume 22, Issue 1, 2024

Published on: 07 April, 2023

Page: [140 - 151] Pages: 12

DOI: 10.2174/1570159X21666230126161524

Price: $65

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Abstract

Parkinson’s disease (PD) is a heterogeneous disease involving a complex interaction between genes and the environment that affects various cellular pathways and neural networks. Several studies have suggested that environmental factors such as exposure to herbicides, pesticides, heavy metals, and other organic pollutants are significant risk factors for the development of PD. Among the herbicides, paraquat has been commonly used, although it has been banned in many countries due to its acute toxicity. Although the direct causational relationship between paraquat exposure and PD has not been established, paraquat has been demonstrated to cause the degeneration of dopaminergic neurons in the substantia nigra pars compacta. The underlying mechanisms of the dopaminergic lesion are primarily driven by the generation of reactive oxygen species, decrease in antioxidant enzyme levels, neuroinflammation, mitochondrial dysfunction, and ER stress, leading to a cascade of molecular crosstalks that result in the initiation of apoptosis. This review critically analyses the crucial upstream molecular pathways of the apoptotic cascade involved in paraquat neurotoxicity, including mitogenactivated protein kinase (MAPK), phosphatidylinositol-4,5-bisphosphate 3-kinase (PI3K)/AKT, mammalian target of rapamycin (mTOR), and Wnt/β-catenin signaling pathways.

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[1]
Tysnes, O.B.; Storstein, A. Epidemiology of Parkinson’s disease. J. Neural Transm. (Vienna), 2017, 124(8), 901-905.
[http://dx.doi.org/10.1007/s00702-017-1686-y] [PMID: 28150045]
[2]
Schapira, A.H.V.; Chaudhuri, K.R.; Jenner, P. Non-motor features of Parkinson disease. Nat. Rev. Neurosci., 2017, 18(7), 435-450.
[http://dx.doi.org/10.1038/nrn.2017.62] [PMID: 28592904]
[3]
Reeve, A.K.; Grady, J.P.; Cosgrave, E.M.; Bennison, E.; Chen, C.; Hepplewhite, P.D.; Morris, C.M. Mitochondrial dysfunction within the synapses of substantia nigra neurons in Parkinson’s disease. NPJ Parkinsons Dis., 2018, 4(1), 9.
[http://dx.doi.org/10.1038/s41531-018-0044-6] [PMID: 29872690]
[4]
Goedert, M.; Spillantini, M.G.; Del Tredici, K.; Braak, H. 100 years of Lewy pathology. Nat. Rev. Neurol., 2013, 9(1), 13-24.
[http://dx.doi.org/10.1038/nrneurol.2012.242] [PMID: 23183883]
[5]
Shahmoradian, S.H.; Lewis, A.J.; Genoud, C.; Hench, J.; Moors, T.E.; Navarro, P.P.; Castaño-Díez, D.; Schweighauser, G.; Graff-Meyer, A.; Goldie, K.N.; Sütterlin, R.; Huisman, E.; Ingrassia, A.; Gier, Y.; Rozemuller, A.J.M.; Wang, J.; Paepe, A.D.; Erny, J.; Staempfli, A.; Hoernschemeyer, J.; Großerüschkamp, F.; Niedieker, D.; El-Mashtoly, S.F.; Quadri, M.; Van IJcken, W.F.J.; Bonifati, V.; Gerwert, K.; Bohrmann, B.; Frank, S.; Britschgi, M.; Stahlberg, H.; Van de Berg, W.D.J.; Lauer, M.E. Lewy pathology in Parkinson’s disease consists of crowded organelles and lipid membranes. Nat. Neurosci., 2019, 22(7), 1099-1109.
[http://dx.doi.org/10.1038/s41593-019-0423-2] [PMID: 31235907]
[6]
Elkouzi, A.; Vedam-Mai, V.; Eisinger, R.S.; Okun, M.S. Emerging therapies in Parkinson disease — repurposed drugs and new approaches. Nat. Rev. Neurol., 2019, 15(4), 204-223.
[http://dx.doi.org/10.1038/s41582-019-0155-7] [PMID: 30867588]
[7]
Parmar, M.; Grealish, S.; Henchcliffe, C. The future of stem cell therapies for Parkinson disease. Nat. Rev. Neurosci., 2020, 21(2), 103-115.
[http://dx.doi.org/10.1038/s41583-019-0257-7] [PMID: 31907406]
[8]
Kalia, L.V.; Lang, A.E. Parkinson’s disease. Lancet, 2015, 386(9996), 896-912.
[http://dx.doi.org/10.1016/S0140-6736(14)61393-3] [PMID: 25904081]
[9]
Verstraeten, A.; Theuns, J.; Van Broeckhoven, C. Progress in unraveling the genetic etiology of Parkinson disease in a genomic era. Trends Genet., 2015, 31(3), 140-149.
[http://dx.doi.org/10.1016/j.tig.2015.01.004] [PMID: 25703649]
[10]
Ball, N.; Teo, W.P.; Chandra, S.; Chapman, J. Parkinson’s disease and the environment. Front. Neurol., 2019, 10(218), 218.
[http://dx.doi.org/10.3389/fneur.2019.00218] [PMID: 30941085]
[11]
Correia, G.L.; Mestre, T.; Outeiro, T.F.; Ferreira, J.J. Are genetic and idiopathic forms of Parkinson’s disease the same disease? J. Neurochem., 2020, 152(5), 515-522.
[http://dx.doi.org/10.1111/jnc.14902] [PMID: 31643079]
[12]
Priyadarshi, A.; Khuder, S.A.; Schaub, E.A.; Priyadarshi, S.S. Environmental risk factors and Parkinson’s disease: a metaanalysis. Environ. Res., 2001, 86(2), 122-127.
[http://dx.doi.org/10.1006/enrs.2001.4264] [PMID: 11437458]
[13]
Pouchieu, C.; Piel, C.; Carles, C.; Gruber, A.; Helmer, C.; Tual, S.; Marcotullio, E.; Lebailly, P.; Baldi, I. Pesticide use in agriculture and Parkinson’s disease in the AGRICAN cohort study. Int. J. Epidemiol., 2018, 47(1), 299-310.
[http://dx.doi.org/10.1093/ije/dyx225] [PMID: 29136149]
[14]
Cheng, Y.H.; Chou, W.C.; Yang, Y.F.; Huang, C.W.; How, C.M.; Chen, S.C.; Chen, W.Y.; Hsieh, N.H.; Lin, Y.J.; You, S.H.; Liao, C.M. PBPK/PD assessment for Parkinson’s disease risk posed by airborne pesticide paraquat exposure. Environ. Sci. Pollut. Res. Int., 2018, 25(6), 5359-5368.
[http://dx.doi.org/10.1007/s11356-017-0875-4] [PMID: 29209972]
[15]
Dawson, A.H.; Eddleston, M.; Senarathna, L.; Mohamed, F.; Gawarammana, I.; Bowe, S.J.; Manuweera, G.; Buckley, N.A. Acute human lethal toxicity of agricultural pesticides: a prospective cohort study. PLoS Med., 2010, 7(10), e1000357.
[http://dx.doi.org/10.1371/journal.pmed.1000357] [PMID: 21048990]
[16]
Grant, H.C.; Lantos, P.L.; Parkinson, C. Cerebral damage in paraquat poisoning. Histopathology, 1980, 4(2), 185-195.
[http://dx.doi.org/10.1111/j.1365-2559.1980.tb02911.x] [PMID: 7358347]
[17]
Weed, D.L. Does paraquat cause Parkinson’s disease? A review of reviews. Neurotoxicology, 2021, 86, 180-184.
[http://dx.doi.org/10.1016/j.neuro.2021.08.006] [PMID: 34400206]
[18]
Ali, S.F.; David, S.N.; Newport, G.D.; Cadet, J.L.; Slikker, W. Jr MPTP-induced oxidative stress and neurotoxicity are age-dependent: Evidence from measures of reactive oxygen species and striatal dopamine levels. Synapse, 1994, 18(1), 27-34.
[http://dx.doi.org/10.1002/syn.890180105] [PMID: 7825121]
[19]
Reczek, C.R.; Birsoy, K.; Kong, H.; Martínez-Reyes, I.; Wang, T.; Gao, P.; Sabatini, D.M.; Chandel, N.S. A CRISPR screen identifies a pathway required for paraquat-induced cell death. Nat. Chem. Biol., 2017, 13(12), 1274-1279.
[http://dx.doi.org/10.1038/nchembio.2499] [PMID: 29058724]
[20]
Shimizu, K.; Ohtaki, K.; Matsubara, K.; Aoyama, K.; Uezono, T.; Saito, O.; Suno, M.; Ogawa, K.; Hayase, N.; Kimura, K.; Shiono, H. Carrier-mediated processes in blood–brain barrier penetration and neural uptake of paraquat. Brain Res., 2001, 906(1-2), 135-142.
[http://dx.doi.org/10.1016/S0006-8993(01)02577-X] [PMID: 11430870]
[21]
Castello, P.R.; Drechsel, D.A.; Patel, M. Mitochondria are a major source of paraquat-induced reactive oxygen species production in the brain. J. Biol. Chem., 2007, 282(19), 14186-14193.
[http://dx.doi.org/10.1074/jbc.M700827200] [PMID: 17389593]
[22]
Cochemé, H.M.; Murphy, M.P.; Complex, I. Complex I is the major site of mitochondrial superoxide production by paraquat. J. Biol. Chem., 2008, 283(4), 1786-1798.
[http://dx.doi.org/10.1074/jbc.M708597200] [PMID: 18039652]
[23]
Shukla, A.K.; Pragya, P.; Chaouhan, H.S.; Patel, D.K.; Abdin, M.Z.; Kar, C.D. A mutation in Drosophila methuselah resists paraquat induced Parkinson-like phenotypes. Neurobiol. Aging, 2014, 35(10), 2419.e1-2419.e16.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.04.008] [PMID: 24819147]
[24]
Rappold, P.M.; Cui, M.; Chesser, A.S.; Tibbett, J.; Grima, J.C.; Duan, L.; Sen, N.; Javitch, J.A.; Tieu, K. Paraquat neurotoxicity is mediated by the dopamine transporter and organic cation transporter-3. Proc. Natl. Acad. Sci. USA, 2011, 108(51), 20766-20771.
[http://dx.doi.org/10.1073/pnas.1115141108] [PMID: 22143804]
[25]
Mitra, S.; Chakrabarti, N.; Bhattacharyya, A. Differential regional expression patterns of α-synuclein, TNF-α and IL-1β and variable status of dopaminergic neurotoxicity in mouse brain after Paraquat treatment. J. Neuroinflammation, 2011, 8(1), 163.
[http://dx.doi.org/10.1186/1742-2094-8-163] [PMID: 22112368]
[26]
Djukic, M.M.; Jovanovic, M.D.; Ninkovic, M.; Stevanovic, I.; Ilic, K.; Curcic, M.; Vekic, J. Protective role of glutathione reductase in paraquat induced neurotoxicity. Chem. Biol. Interact., 2012, 199(2), 74-86.
[http://dx.doi.org/10.1016/j.cbi.2012.05.008] [PMID: 22721943]
[27]
Wills, J.; Credle, J.; Oaks, A.W.; Duka, V.; Lee, J.H.; Jones, J.; Sidhu, A. Paraquat, but not maneb, induces synucleinopathy and tauopathy in striata of mice through inhibition of proteasomal and autophagic pathways. PLoS One, 2012, 7(1), e30745.
[http://dx.doi.org/10.1371/journal.pone.0030745] [PMID: 22292029]
[28]
Huang, C.L.; Chao, C.C.; Lee, Y.C.; Lu, M.K.; Cheng, J.J.; Yang, Y.C.; Wang, V.C.; Chang, W.C.; Huang, N.K. Paraquat induces cell death through impairing mitochondrial membrane permeability. Mol. Neurobiol., 2016, 53(4), 2169-2188.
[http://dx.doi.org/10.1007/s12035-015-9198-y] [PMID: 25947082]
[29]
See, W.Z.C.; Naidu, R.; Tang, K.S. Cellular and molecular events leading to paraquat-induced apoptosis: mechanistic insights into Parkinson’s disease pathophysiology. Mol. Neurobiol., 2022, 59(6), 3353-3369.
[http://dx.doi.org/10.1007/s12035-022-02799-2] [PMID: 35306641]
[30]
Taylor, R.C.; Cullen, S.P.; Martin, S.J. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol., 2008, 9(3), 231-241.
[http://dx.doi.org/10.1038/nrm2312] [PMID: 18073771]
[31]
Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516.
[http://dx.doi.org/10.1080/01926230701320337] [PMID: 17562483]
[32]
Nguyen, T.T.M.; Gillet, G.; Popgeorgiev, N. Caspases in the developing central nervous system: apoptosis and beyond. Front. Cell Dev. Biol., 1910, 2021, 9.
[PMID: 34336853]
[33]
Redza-Dutordoir, M.; Averill-Bates, D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta Mol. Cell Res., 2016, 1863(12), 2977-2992.
[http://dx.doi.org/10.1016/j.bbamcr.2016.09.012] [PMID: 27646922]
[34]
Chowdhury, I.; Tharakan, B.; Bhat, G.K. Caspases — An update. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2008, 151(1), 10-27.
[http://dx.doi.org/10.1016/j.cbpb.2008.05.010] [PMID: 18602321]
[35]
Kale, J.; Osterlund, E.J.; Andrews, D.W. BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ., 2018, 25(1), 65-80.
[http://dx.doi.org/10.1038/cdd.2017.186] [PMID: 29149100]
[36]
Hsu, Y.T.; Wolter, K.G.; Youle, R.J. Cytosol-to-membrane redistribution of Bax and Bcl-XL during apoptosis. Proc. Natl. Acad. Sci. USA, 1997, 94(8), 3668-3672.
[http://dx.doi.org/10.1073/pnas.94.8.3668] [PMID: 9108035]
[37]
Kalkavan, H.; Green, D.R. MOMP, cell suicide as a BCL-2 family business. Cell Death Differ., 2018, 25(1), 46-55.
[http://dx.doi.org/10.1038/cdd.2017.179] [PMID: 29053143]
[38]
Huang, C.L.; Lee, Y.C.; Yang, Y.C.; Kuo, T.Y.; Huang, N.K. Minocycline prevents paraquat-induced cell death through attenuating endoplasmic reticulum stress and mitochondrial dysfunction. Toxicol. Lett., 2012, 209(3), 203-210.
[http://dx.doi.org/10.1016/j.toxlet.2011.12.021] [PMID: 22245251]
[39]
de Oliveira, M.R.; Ferreira, G.C.; Schuck, P.F. Protective effect of carnosic acid against paraquat-induced redox impairment and mitochondrial dysfunction in SH-SY5Y cells: Role for PI3K/Akt/Nrf2 pathway. Toxicol. In Vitro, 2016, 32, 41-54.
[http://dx.doi.org/10.1016/j.tiv.2015.12.005] [PMID: 26686574]
[40]
Del Pino, J.; Moyano, P.; Díaz, G.G.; Anadon, M.J.; Diaz, M.J.; García, J.M.; Lobo, M.; Pelayo, A.; Sola, E.; Frejo, M.T. Primary hippocampal neuronal cell death induction after acute and repeated paraquat exposures mediated by AChE variants alteration and cholinergic and glutamatergic transmission disruption. Toxicology, 2017, 390, 88-99.
[http://dx.doi.org/10.1016/j.tox.2017.09.008] [PMID: 28916328]
[41]
Srivastav, S.; Fatima, M.; Mondal, A.C. Bacopa monnieri alleviates paraquat induced toxicity in Drosophila by inhibiting jnk mediated apoptosis through improved mitochondrial function and redox stabilization. Neurochem. Int., 2018, 121, 98-107.
[http://dx.doi.org/10.1016/j.neuint.2018.10.001] [PMID: 30296463]
[42]
Fei, Q.; McCormack, A.L.; Di Monte, D.A.; Ethell, D.W. Paraquat neurotoxicity is mediated by a Bak-dependent mechanism. J. Biol. Chem., 2008, 283(6), 3357-3364.
[http://dx.doi.org/10.1074/jbc.M708451200] [PMID: 18056701]
[43]
Westphal, D.; Kluck, R.M.; Dewson, G. Building blocks of the apoptotic pore: how Bax and Bak are activated and oligomerize during apoptosis. Cell Death Differ., 2014, 21(2), 196-205.
[http://dx.doi.org/10.1038/cdd.2013.139] [PMID: 24162660]
[44]
Ray, R.; Chen, G.; Vande Velde, C.; Cizeau, J.; Park, J.H.; Reed, J.C.; Gietz, R.D.; Greenberg, A.H. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J. Biol. Chem., 2000, 275(2), 1439-1448.
[http://dx.doi.org/10.1074/jbc.275.2.1439] [PMID: 10625696]
[45]
Ploner, C.; Kofler, R.; Villunger, A. Noxa: at the tip of the balance between life and death. Oncogene, 2008, 27(Suppl. 1), S84-S92.
[http://dx.doi.org/10.1038/onc.2009.46] [PMID: 19641509]
[46]
Vela, L.; Gonzalo, O.; Naval, J.; Marzo, I. Direct interaction of Bax and Bak proteins with Bcl-2 homology domain 3 (BH3)-only proteins in living cells revealed by fluorescence complementation. J. Biol. Chem., 2013, 288(7), 4935-4946.
[http://dx.doi.org/10.1074/jbc.M112.422204] [PMID: 23283967]
[47]
Plotnikov, A.; Zehorai, E.; Procaccia, S.; Seger, R. The MAPK cascades: Signaling components, nuclear roles and mechanisms of nuclear translocation. Biochim. Biophys. Acta Mol. Cell Res., 2011, 1813(9), 1619-1633.
[http://dx.doi.org/10.1016/j.bbamcr.2010.12.012] [PMID: 21167873]
[48]
Bohush, A.; Niewiadomska, G.; Filipek, A. Role of mitogen activated protein kinase signaling in parkinson’s disease. Int. J. Mol. Sci., 2018, 19(10), 2973.
[http://dx.doi.org/10.3390/ijms19102973] [PMID: 30274251]
[49]
Peti, W.; Page, R. Molecular basis of MAP kinase regulation. Protein Sci., 2013, 22(12), 1698-1710.
[http://dx.doi.org/10.1002/pro.2374] [PMID: 24115095]
[50]
Jha, S.K.; Jha, N.K.; Kar, R.; Ambasta, R.K.; Kumar, P. p38 MAPK and PI3K/AKT signalling cascades in Parkinson’s disease. Int. J. Mol. Cell. Med., 2015, 4(2), 67-86.
[PMID: 26261796]
[51]
Niso-Santano, M.; González-Polo, R.A.; Bravo-San Pedro, J.M.; Gómez-Sánchez, R.; Lastres-Becker, I.; Ortiz-Ortiz, M.A.; Soler, G.; Morán, J.M.; Cuadrado, A.; Fuentes, J.M. Activation of apoptosis signal-regulating kinase 1 is a key factor in paraquat-induced cell death: Modulation by the Nrf2/Trx axis. Free Radic. Biol. Med., 2010, 48(10), 1370-1381.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.02.024] [PMID: 20202476]
[52]
Lindholm, D.; Wootz, H.; Korhonen, L. ER stress and neurodegenerative diseases. Cell Death Differ., 2006, 13(3), 385-392.
[http://dx.doi.org/10.1038/sj.cdd.4401778] [PMID: 16397584]
[53]
Niso-Santano, M.; Bravo-San Pedro, J.M.; Gómez-Sánchez, R.; Climent, V.; Soler, G.; Fuentes, J.M.; González-Polo, R.A. ASK1 overexpression accelerates paraquat-induced autophagy via endoplasmic reticulum stress. Toxicol. Sci., 2011, 119(1), 156-168.
[http://dx.doi.org/10.1093/toxsci/kfq313] [PMID: 20929985]
[54]
Reinhard, C.; Shamoon, B.; Shyamala, V.; Williams, L.T. Tumor necrosis factor alpha -induced activation of c-jun N-terminal kinase is mediated by TRAF2. EMBO J., 1997, 16(5), 1080-1092.
[http://dx.doi.org/10.1093/emboj/16.5.1080] [PMID: 9118946]
[55]
Wang, M.C.; Bohmann, D.; Jasper, H. JNK signaling confers tolerance to oxidative stress and extends lifespan in Drosophila. Dev. Cell, 2003, 5(5), 811-816.
[http://dx.doi.org/10.1016/S1534-5807(03)00323-X] [PMID: 14602080]
[56]
Hamdi, M.; Kool, J.; Cornelissen-Steijger, P.; Carlotti, F.; Popeijus, H.E.; van der Burgt, C.; Janssen, J.M.; Yasui, A.; Hoeben, R.C.; Terleth, C.; Mullenders, L.H.; van Dam, H. DNA damage in transcribed genes induces apoptosis via the JNK pathway and the JNK-phosphatase MKP-1. Oncogene, 2005, 24(48), 7135-7144.
[http://dx.doi.org/10.1038/sj.onc.1208875] [PMID: 16044158]
[57]
Dhanasekaran, D.N.; Reddy, E.P. JNK signaling in apoptosis. Oncogene, 2008, 27(48), 6245-6251.
[http://dx.doi.org/10.1038/onc.2008.301] [PMID: 18931691]
[58]
Lin, A.; Dibling, B. The true face of JNK activation in apoptosis. Aging Cell, 2002, 1(2), 112-116.
[http://dx.doi.org/10.1046/j.1474-9728.2002.00014.x] [PMID: 12882340]
[59]
Liu, J.; Lin, A. Role of JNK activation in apoptosis: A double-edged sword. Cell Res., 2005, 15(1), 36-42.
[http://dx.doi.org/10.1038/sj.cr.7290262] [PMID: 15686625]
[60]
Tournier, C.; Dong, C.; Turner, T.K.; Jones, S.N.; Flavell, R.A.; Davis, R.J. MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev., 2001, 15(11), 1419-1426.
[http://dx.doi.org/10.1101/gad.888501] [PMID: 11390361]
[61]
Schreck, I.; Al-Rawi, M.; Mingot, J.M.; Scholl, C.; Diefenbacher, M.E.; O’Donnell, P.; Bohmann, D.; Weiss, C. c-Jun localizes to the nucleus independent of its phosphorylation by and interaction with JNK and vice versa promotes nuclear accumulation of JNK. Biochem. Biophys. Res. Commun., 2011, 407(4), 735-740.
[http://dx.doi.org/10.1016/j.bbrc.2011.03.092] [PMID: 21439937]
[62]
Ju, D.T.; Sivalingam, K.; Kuo, W.W.; Ho, T.J.; Chang, R.L.; Chung, L.C.; Day, C.H.; Viswanadha, V.P.; Liao, P.H.; Huang, C.Y. Effect of vasicinone against paraquat-induced MAPK/p53-mediated apoptosis via the IGF-1R/PI3K/AKT Pathway in a Parkinson’s disease-associated SH-SY5Y cell model. Nutrients, 2019, 11(7), 1655.
[http://dx.doi.org/10.3390/nu11071655] [PMID: 31331066]
[63]
Fuchs, S.Y.; Adler, V.; Pincus, M.R.; Ronai, Z. MEKK1/JNK signaling stabilizes and activates p53. Proc. Natl. Acad. Sci. USA, 1998, 95(18), 10541-10546.
[http://dx.doi.org/10.1073/pnas.95.18.10541] [PMID: 9724739]
[64]
Ferrer, I.; Blanco, R.; Carmona, M.; Puig, B.; Barrachina, M.; Gómez, C.; Ambrosio, S. Active, phosphorylation-dependent mitogen-activated protein kinase (MAPK/ERK), stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK), and p38 kinase expression in Parkinson’s disease and Dementia with Lewy bodies. J. Neural Transm. (Vienna), 2001, 108(12), 1383-1396.
[http://dx.doi.org/10.1007/s007020100015] [PMID: 11810403]
[65]
Cuenda, A.; Alonso, G.; Morrice, N.; Jones, M.; Meier, R.; Cohen, P.; Nebreda, A.R. Purification and cDNA cloning of SAPKK3, the major activator of RK/p38 in stress- and cytokine-stimulated monocytes and epithelial cells. EMBO J., 1996, 15(16), 4156-4164.
[http://dx.doi.org/10.1002/j.1460-2075.1996.tb00790.x] [PMID: 8861944]
[66]
Cuenda, A.; Cohen, P.; Buée-Scherrer, V.; Goedert, M. Activation of stress-activated protein kinase-3 (SAPK3) by cytokines and cellular stresses is mediated via SAPKK3 (MKK6); comparison of the specificities of SAPK3 and SAPK2 (RK/p38). EMBO J., 1997, 16(2), 295-305.
[http://dx.doi.org/10.1093/emboj/16.2.295] [PMID: 9029150]
[67]
Raingeaud, J.; Whitmarsh, A.J.; Barrett, T.; Dérijard, B.; Davis, R.J. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol. Cell. Biol., 1996, 16(3), 1247-1255.
[http://dx.doi.org/10.1128/MCB.16.3.1247] [PMID: 8622669]
[68]
Obergasteiger, J.; Frapporti, G.; Pramstaller, P.P.; Hicks, A.A.; Volta, M. A new hypothesis for Parkinson’s disease pathogenesis: GTPase-p38 MAPK signaling and autophagy as convergence points of etiology and genomics. Mol. Neurodegener., 2018, 13(1), 40.
[http://dx.doi.org/10.1186/s13024-018-0273-5] [PMID: 30071902]
[69]
Subramaniam, S.; Unsicker, K. Extracellular signal-regulated kinase as an inducer of non-apoptotic neuronal death. Neuroscience, 2006, 138(4), 1055-1065.
[http://dx.doi.org/10.1016/j.neuroscience.2005.12.013] [PMID: 16442236]
[70]
Seo, H.J.; Choi, S.J.; Lee, J.H. Paraquat induces apoptosis through cytochrome C release and ERK activation. Biomol. Ther. (Seoul), 2014, 22(6), 503-509.
[http://dx.doi.org/10.4062/biomolther.2014.115] [PMID: 25489417]
[71]
Niso-Santano, M.; Morán, J.M.; García-Rubio, L.; Gómez-Martín, A.; González-Polo, R.A.; Soler, G.; Fuentes, J.M. Low concentrations of paraquat induces early activation of extracellular signal-regulated kinase 1/2, protein kinase B, and c-Jun N-terminal kinase 1/2 pathways: role of c-Jun N-terminal kinase in paraquat-induced cell death. Toxicol. Sci., 2006, 92(2), 507-515.
[http://dx.doi.org/10.1093/toxsci/kfl013] [PMID: 16687388]
[72]
Zhu, J.H.; Kulich, S.M.; Oury, T.D.; Chu, C.T. Cytoplasmic aggregates of phosphorylated extracellular signal-regulated protein kinases in Lewy body diseases. Am. J. Pathol., 2002, 161(6), 2087-2098.
[http://dx.doi.org/10.1016/S0002-9440(10)64487-2] [PMID: 12466125]
[73]
Zhu, Y.; Carvey, P.M.; Ling, Z. Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain Res., 2006, 1090(1), 35-44.
[http://dx.doi.org/10.1016/j.brainres.2006.03.063] [PMID: 16647047]
[74]
Xu, F.; Na, L.; Li, Y.; Chen, L. RETRACTED ARTICLE: Roles of the PI3K/AKT/mTOR signalling pathways in neurodegenerative diseases and tumours. Cell Biosci., 2020, 10(1), 54.
[http://dx.doi.org/10.1186/s13578-020-00416-0] [PMID: 32266056]
[75]
Bilanges, B.; Posor, Y.; Vanhaesebroeck, B. PI3K isoforms in cell signalling and vesicle trafficking. Nat. Rev. Mol. Cell Biol., 2019, 20(9), 515-534.
[http://dx.doi.org/10.1038/s41580-019-0129-z] [PMID: 31110302]
[76]
Zheng, W.H.; Kar, S.; Quirion, R. Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol. Pharmacol., 2002, 62(2), 225-233.
[http://dx.doi.org/10.1124/mol.62.2.225] [PMID: 12130673]
[77]
Bianchi, V.; Locatelli, V.; Rizzi, L. Neurotrophic and neuroregenerative effects of GH/IGF1. Int. J. Mol. Sci., 2017, 18(11), 2441.
[http://dx.doi.org/10.3390/ijms18112441] [PMID: 29149058]
[78]
Pettmann, B.; Henderson, C.E. Neuronal cell death. Neuron, 1998, 20(4), 633-647.
[http://dx.doi.org/10.1016/S0896-6273(00)81004-1] [PMID: 9581757]
[79]
Malagelada, C.; Jin, Z.H.; Greene, L.A. RTP801 is induced in Parkinson’s disease and mediates neuron death by inhibiting Akt phosphorylation/activation. J. Neurosci., 2008, 28(53), 14363-14371.
[http://dx.doi.org/10.1523/JNEUROSCI.3928-08.2008] [PMID: 19118169]
[80]
Luo, S.; Kang, S.S.; Wang, Z.H.; Liu, X.; Day, J.X.; Wu, Z.; Peng, J.; Xiang, D.; Springer, W.; Ye, K. Akt phosphorylates NQO1 and triggers its degradation, abolishing its antioxidative activities in Parkinson’s disease. J. Neurosci., 2019, 39(37), 7291-7305.
[http://dx.doi.org/10.1523/JNEUROSCI.0625-19.2019] [PMID: 31358653]
[81]
Franke, T.F.; Hornik, C.P.; Segev, L.; Shostak, G.A.; Sugimoto, C. PI3K/Akt and apoptosis: size matters. Oncogene, 2003, 22(56), 8983-8998.
[http://dx.doi.org/10.1038/sj.onc.1207115] [PMID: 14663477]
[82]
Cardone, M.H.; Roy, N.; Stennicke, H.R.; Salvesen, G.S.; Franke, T.F.; Stanbridge, E.; Frisch, S.; Reed, J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science, 1998, 282(5392), 1318-1321.
[http://dx.doi.org/10.1126/science.282.5392.1318] [PMID: 9812896]
[83]
Romorini, L.; Garate, X.; Neiman, G.; Luzzani, C.; Furmento, V.A.; Guberman, A.S.; Sevlever, G.E.; Scassa, M.E.; Miriuka, S.G. AKT/GSK3β signaling pathway is critically involved in human pluripotent stem cell survival. Sci. Rep., 2016, 6(1), 35660.
[http://dx.doi.org/10.1038/srep35660] [PMID: 27762303]
[84]
Kale, J.; Kutuk, O.; Brito, G.C.; Andrews, T.S.; Leber, B.; Letai, A.; Andrews, D.W. Phosphorylation switches Bax from promoting to inhibiting apoptosis thereby increasing drug resistance. EMBO Rep., 2018, 19(9), e45235.
[http://dx.doi.org/10.15252/embr.201745235] [PMID: 29987135]
[85]
Yang, E.; Zha, J.; Jockel, J.; Boise, L.H.; Thompson, C.B.; Korsmeyer, S.J. Bad, a heterodimeric partner for Bcl-xL and Bcl-2, displaces bax and promotes cell death. Cell, 1995, 80(2), 285-291.
[http://dx.doi.org/10.1016/0092-8674(95)90411-5] [PMID: 7834748]
[86]
Tan, Y.; Demeter, M.R.; Ruan, H.; Comb, M.J. BAD Ser-155 phosphorylation regulates BAD/Bcl-XL interaction and cell survival. J. Biol. Chem., 2000, 275(33), 25865-25869.
[http://dx.doi.org/10.1074/jbc.M004199200] [PMID: 10837486]
[87]
Hirai, I.; Wang, H.G. Survival-factor-induced phosphorylation of Bad results in its dissociation from Bcl-xL but not Bcl-2. Biochem. J., 2001, 359(2), 345-352.
[http://dx.doi.org/10.1042/bj3590345] [PMID: 11583580]
[88]
Yamaguchi, H.; Wang, H.G. The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene, 2001, 20(53), 7779-7786.
[http://dx.doi.org/10.1038/sj.onc.1204984] [PMID: 11753656]
[89]
Kennedy, S.G.; Kandel, E.S.; Cross, T.K.; Hay, N. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol. Cell. Biol., 1999, 19(8), 5800-5810.
[http://dx.doi.org/10.1128/MCB.19.8.5800] [PMID: 10409766]
[90]
Gottlieb, T.M.; Leal, J.F.M.; Seger, R.; Taya, Y.; Oren, M. Cross-talk between Akt, p53 and Mdm2: possible implications for the regulation of apoptosis. Oncogene, 2002, 21(8), 1299-1303.
[http://dx.doi.org/10.1038/sj.onc.1205181] [PMID: 11850850]
[91]
Lam, E.W.F.; Francis, R.E.; Petkovic, M. FOXO transcription factors: key regulators of cell fate. Biochem. Soc. Trans., 2006, 34(5), 722-726.
[http://dx.doi.org/10.1042/BST0340722] [PMID: 17052182]
[92]
Hu, W.; Yang, Z.; Yang, W.; Han, M.; Xu, B.; Yu, Z.; Shen, M.; Yang, Y. Roles of forkhead box O (FoxO) transcription factors in neurodegenerative diseases: A panoramic view. Prog. Neurobiol., 2019, 181, 101645.
[http://dx.doi.org/10.1016/j.pneurobio.2019.101645] [PMID: 31229499]
[93]
Zhang, X.; Tang, N.; Hadden, T.J.; Rishi, A.K. Akt, FoxO and regulation of apoptosis. Biochimica et Biophysica Acta (BBA) -. Mol. Cell Res., 2011, 1813(11), 1978-1986.
[94]
Essers, M.A.G.; Weijzen, S.; de Vries-Smits, A.M.M.; Saarloos, I.; de Ruiter, N.D.; Bos, J.L.; Burgering, B.M.T. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J., 2004, 23(24), 4802-4812.
[http://dx.doi.org/10.1038/sj.emboj.7600476] [PMID: 15538382]
[95]
Kim, A.H.; Khursigara, G.; Sun, X.; Franke, T.F.; Chao, M.V. Akt phosphorylates and negatively regulates apoptosis signal-regulating kinase 1. Mol. Cell. Biol., 2001, 21(3), 893-901.
[http://dx.doi.org/10.1128/MCB.21.3.893-901.2001] [PMID: 11154276]
[96]
Wullschleger, S.; Loewith, R.; Hall, M.N. TOR signaling in growth and metabolism. Cell, 2006, 124(3), 471-484.
[http://dx.doi.org/10.1016/j.cell.2006.01.016] [PMID: 16469695]
[97]
Saxton, R.A.; Sabatini, D.M. mTOR signaling in growth, metabolism, and disease. Cell, 2017, 168(6), 960-976.
[http://dx.doi.org/10.1016/j.cell.2017.02.004] [PMID: 28283069]
[98]
Frias, M.A.; Thoreen, C.C.; Jaffe, J.D.; Schroder, W.; Sculley, T.; Carr, S.A.; Sabatini, D.M. mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr. Biol., 2006, 16(18), 1865-1870.
[http://dx.doi.org/10.1016/j.cub.2006.08.001] [PMID: 16919458]
[99]
Nakajima, S.; Hiramatsu, N.; Hayakawa, K.; Saito, Y.; Kato, H.; Huang, T.; Yao, J.; Paton, A.W.; Paton, J.C.; Kitamura, M. Selective abrogation of BiP/GRP78 blunts activation of NF-κB through the ATF6 branch of the UPR: involvement of C/EBPβ and mTOR-dependent dephosphorylation of Akt. Mol. Cell. Biol., 2011, 31(8), 1710-1718.
[http://dx.doi.org/10.1128/MCB.00939-10] [PMID: 21300786]
[100]
Kato, H.; Nakajima, S.; Saito, Y.; Takahashi, S.; Katoh, R.; Kitamura, M. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1–JNK pathway. Cell Death Differ., 2012, 19(2), 310-320.
[http://dx.doi.org/10.1038/cdd.2011.98] [PMID: 21779001]
[101]
Chen, C.H.; Shaikenov, T.; Peterson, T.R.; Aimbetov, R.; Bissenbaev, A.K.; Lee, S.W.; Wu, J.; Lin, H.K.; Sarbassov, D.D. ER stress inhibits mTORC2 and Akt signaling through GSK-3β-mediated phosphorylation of rictor. Sci. Signal., 2011, 4(161), ra10-ra10.
[http://dx.doi.org/10.1126/scisignal.2001731] [PMID: 21343617]
[102]
Dijkstra, A.A.; Ingrassia, A.; de Menezes, R.X.; van Kesteren, R.E.; Rozemuller, A.J.M.; Heutink, P.; van de Berg, W.D.J. Evidence for immune response, axonal dysfunction and reduced endocytosis in the substantia nigra in early stage Parkinson’s Disease. PLoS One, 2015, 10(6), e0128651.
[http://dx.doi.org/10.1371/journal.pone.0128651] [PMID: 26087293]
[103]
Crews, L.; Spencer, B.; Desplats, P.; Patrick, C.; Paulino, A.; Rockenstein, E.; Hansen, L.; Adame, A.; Galasko, D.; Masliah, E. Selective molecular alterations in the autophagy pathway in patients with Lewy body disease and in models of α-synucleinopathy. PLoS One, 2010, 5(2), e9313.
[http://dx.doi.org/10.1371/journal.pone.0009313] [PMID: 20174468]
[104]
Liu, Z.; Zhuang, W.; Cai, M.; Lv, E.; Wang, Y.; Wu, Z.; Wang, H.; Fu, W. Kaemperfol protects dopaminergic neurons by promoting mtor-mediated autophagy in Parkinson’s disease models. Neurochem. Res., 2022. Dec 5. doi: 10.1007/s11064-022-03819-2. Epub ahead of print. PMID: 36469163
[http://dx.doi.org/10.1007/s11064-022-03819-2] [PMID: 36469163]
[105]
Morita, M.; Prudent, J.; Basu, K.; Goyon, V.; Katsumura, S.; Hulea, L.; Pearl, D.; Siddiqui, N.; Strack, S.; McGuirk, S.; St-Pierre, J.; Larsson, O.; Topisirovic, I.; Vali, H.; McBride, H.M.; Bergeron, J.J.; Sonenberg, N. mTOR controls mitochondrial dynamics and cell survival via MTFP1. Mol. Cell, 2017, 67(6), 922-935.e5.
[http://dx.doi.org/10.1016/j.molcel.2017.08.013] [PMID: 28918902]
[106]
Shirgadwar, S.M.; Kumar, R.; Preeti, K.; Khatri, D.K.; Singh, S.B. Neuroprotective effect of phloretin in rotenone-induced mice Model of Parkinson’s disease: modulating mTOR-NRF2-p62 mediated autophagy-oxidative stress crosstalk. J. Alzheimers Dis., 2022, 1-16.
[http://dx.doi.org/10.3233/JAD-220793] [PMID: 36463449]
[107]
González-Polo, R.A.; Niso-Santano, M.; Ortíz-Ortíz, M.A.; Gómez-Martín, A.; Morán, J.M.; García-Rubio, L.; Francisco-Morcillo, J.; Zaragoza, C.; Soler, G.; Fuentes, J.M. Inhibition of paraquat-induced autophagy accelerates the apoptotic cell death in neuroblastoma SH-SY5Y cells. Toxicol. Sci., 2007, 97(2), 448-458.
[http://dx.doi.org/10.1093/toxsci/kfm040] [PMID: 17341480]
[108]
Kong, D.; Ding, Y.; Liu, J.; Liu, R.; Zhang, J.; Zhou, Q.; Long, Z.; Peng, J.; Li, L.; Bai, H.; Hai, C. Chlorogenic acid prevents paraquat-induced apoptosis via Sirt1-mediated regulation of redox and mitochondrial function. Free Radic. Res., 2019, 53(6), 680-693.
[http://dx.doi.org/10.1080/10715762.2019.1621308] [PMID: 31106605]
[109]
Zhang, J.; Culp, M.L.; Craver, J.G.; Darley-Usmar, V. Mitochondrial function and autophagy: integrating proteotoxic, redox, and metabolic stress in Parkinson’s disease. J. Neurochem., 2018, 144(6), 691-709.
[http://dx.doi.org/10.1111/jnc.14308] [PMID: 29341130]
[110]
Inestrosa, N.C.; Varela-Nallar, L. Wnt signalling in neuronal differentiation and development. Cell Tissue Res., 2015, 359(1), 215-223.
[http://dx.doi.org/10.1007/s00441-014-1996-4] [PMID: 25234280]
[111]
Huang, P.; Yan, R.; Zhang, X.; Wang, L.; Ke, X.; Qu, Y. Activating Wnt/β-catenin signaling pathway for disease therapy: Challenges and opportunities. Pharmacol. Ther., 2019, 196, 79-90.
[http://dx.doi.org/10.1016/j.pharmthera.2018.11.008] [PMID: 30468742]
[112]
Stamos, J.L.; Weis, W.I. The β-catenin destruction complex. Cold Spring Harb. Perspect. Biol., 2013, 5(1), a007898.
[http://dx.doi.org/10.1101/cshperspect.a007898] [PMID: 23169527]
[113]
Libro, R.; Bramanti, P.; Mazzon, E. The role of the Wnt canonical signaling in neurodegenerative diseases. Life Sci., 2016, 158, 78-88.
[http://dx.doi.org/10.1016/j.lfs.2016.06.024] [PMID: 27370940]
[114]
Joksimovic, M.; Awatramani, R. Wnt/-catenin signaling in midbrain dopaminergic neuron specification and neurogenesis. J. Mol. Cell Biol., 2014, 6(1), 27-33.
[http://dx.doi.org/10.1093/jmcb/mjt043] [PMID: 24287202]
[115]
Wurst, W.; Prakash, N. Wnt1-regulated genetic networks in midbrain dopaminergic neuron development. J. Mol. Cell Biol., 2014, 6(1), 34-41.
[http://dx.doi.org/10.1093/jmcb/mjt046] [PMID: 24326514]
[116]
Arenas, E. Wnt signaling in midbrain dopaminergic neuron development and regenerative medicine for Parkinson’s disease. J. Mol. Cell Biol., 2014, 6(1), 42-53.
[http://dx.doi.org/10.1093/jmcb/mju001] [PMID: 24431302]
[117]
Cantuti-Castelvetri, I.; Keller-McGandy, C.; Bouzou, B.; Asteris, G.; Clark, T.W.; Frosch, M.P.; Standaert, D.G. Effects of gender on nigral gene expression and parkinson disease. Neurobiol. Dis., 2007, 26(3), 606-614.
[http://dx.doi.org/10.1016/j.nbd.2007.02.009] [PMID: 17412603]
[118]
Zhang, L.; Deng, J.; Pan, Q.; Zhan, Y.; Fan, J.B.; Zhang, K.; Zhang, Z. Targeted methylation sequencing reveals dysregulated Wnt signaling in Parkinson disease. J. Genet. Genomics, 2016, 43(10), 587-592.
[http://dx.doi.org/10.1016/j.jgg.2016.05.002] [PMID: 27692691]
[119]
Yang, J.M.; Huang, H.M.; Cheng, J.J.; Huang, C.L.; Lee, Y.C.; Chiou, C.T.; Huang, H.T.; Huang, N.K.; Yang, Y.C. LGK974, a PORCUPINE inhibitor, mitigates cytotoxicity in an in vitro model of Parkinson’s disease by interfering with the WNT/β-CATENIN pathway. Toxicology, 2018, 410, 65-72.
[http://dx.doi.org/10.1016/j.tox.2018.09.003] [PMID: 30205152]
[120]
Cross, D.A.; Alessi, D.R.; Vandenheede, J.R.; McDowell, H.E.; Hundal, H.S.; Cohen, P. The inhibition of glycogen synthase kinase-3 by insulin or insulin-like growth factor 1 in the rat skeletal muscle cell line L6 is blocked by wortmannin, but not by rapamycin: evidence that wortmannin blocks activation of the mitogen-activated protein kinase pathway in L6 cells between Ras and Raf. Biochem. J., 1994, 303(Pt 1), 21-26.
[http://dx.doi.org/10.1042/bj3030021] [PMID: 7945242]
[121]
Stambolic, V.; Woodgett, J.R. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem. J., 1994, 303(Pt 1), 701-704.
[http://dx.doi.org/10.1042/bj3030701] [PMID: 7980435]
[122]
Cross, D.A.E.; Alessi, D.R.; Cohen, P.; Andjelkovich, M.; Hemmings, B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 1995, 378(6559), 785-789.
[http://dx.doi.org/10.1038/378785a0] [PMID: 8524413]
[123]
Verheyen, E.M.; Gottardi, C.J. Regulation of Wnt/beta-catenin signaling by protein kinases. Dev. Dyn., 2010, 239(1), 34-44.
[PMID: 19623618]
[124]
Funato, Y.; Michiue, T.; Asashima, M.; Miki, H. The thioredoxin-related redox-regulating protein nucleoredoxin inhibits Wnt-β-catenin signalling through Dishevelled. Nat. Cell Biol., 2006, 8(5), 501-508.
[http://dx.doi.org/10.1038/ncb1405] [PMID: 16604061]
[125]
Bernkopf, D.B.; Behrens, J. Cell intrinsic Wnt/β-catenin signaling activation. Aging, 2018, 10(5), 855-856.
[http://dx.doi.org/10.18632/aging.101455] [PMID: 29787999]
[126]
Sekine, S.; Kanamaru, Y.; Koike, M.; Nishihara, A.; Okada, M.; Kinoshita, H.; Kamiyama, M.; Maruyama, J.; Uchiyama, Y.; Ishihara, N.; Takeda, K.; Ichijo, H. Rhomboid protease PARL mediates the mitochondrial membrane potential loss-induced cleavage of PGAM5. J. Biol. Chem., 2012, 287(41), 34635-34645.
[http://dx.doi.org/10.1074/jbc.M112.357509] [PMID: 22915595]
[127]
Bernkopf, D.B.; Jalal, K.; Brückner, M.; Knaup, K.X.; Gentzel, M.; Schambony, A.; Behrens, J. Pgam5 released from damaged mitochondria induces mitochondrial biogenesis via Wnt signaling. J. Cell Biol., 2018, 217(4), 1383-1394.
[http://dx.doi.org/10.1083/jcb.201708191] [PMID: 29438981]
[128]
Rosenbloom, A.B. Tarczyński, M.; Lam, N.; Kane, R.S.; Bugaj, L.J.; Schaffer, D.V. β-Catenin signaling dynamics regulate cell fate in differentiating neural stem cells. Proc. Natl. Acad. Sci., 2020, 117(46), 28828-28837.
[http://dx.doi.org/10.1073/pnas.2008509117] [PMID: 33139571]
[129]
Sherr, C.J.; Roberts, J.M. Living with or without cyclins and cyclin-dependent kinases. Genes Dev., 2004, 18(22), 2699-2711.
[http://dx.doi.org/10.1101/gad.1256504] [PMID: 15545627]
[130]
Fu, M.; Wang, C.; Li, Z.; Sakamaki, T.; Pestell, R.G. Minireview: Cyclin D1: normal and abnormal functions. Endocrinology, 2004, 145(12), 5439-5447.
[http://dx.doi.org/10.1210/en.2004-0959] [PMID: 15331580]
[131]
Kafri, P.; Hasenson, S.E.; Kanter, I.; Sheinberger, J.; Kinor, N.; Yunger, S.; Shav-Tal, Y. Quantifying β-catenin subcellular dynamics and cyclin D1 mRNA transcription during Wnt signaling in single living cells. eLife, 2016, 5, e16748.
[http://dx.doi.org/10.7554/eLife.16748] [PMID: 27879202]
[132]
Guo, Z.; Hao, X.; Tan, F.F.; Pei, X.; Shang, L.M.; Jiang, X.; Yang, F. The elements of human cyclin D1 promoter and regulation involved. Clin. Epigenetics, 2011, 2(2), 63-76.
[http://dx.doi.org/10.1007/s13148-010-0018-y] [PMID: 22704330]
[133]
Zhao, L.; Yan, M.; Wang, X.; Xiong, G.; Wu, C.; Wang, Z.; Zhou, Z.; Chang, X. Modification of Wnt signaling pathway on paraquat-induced inhibition of neural progenitor cell proliferation. Food Chem. Toxicol., 2018, 121, 311-325.
[http://dx.doi.org/10.1016/j.fct.2018.08.064] [PMID: 30171970]

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