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


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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.

作者简介

Wesley Chung See

Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia

Email: info@benthamscience.net

Rakesh Naidu

Jeffrey Cheah School of Medicine and Health Sciences, Monash University Malaysia

Email: info@benthamscience.net

Kim Tang

School of Pharmacy, Monash University Malaysia

编辑信件的主要联系方式.
Email: info@benthamscience.net

参考

  1. Tysnes, O.B.; Storstein, A. Epidemiology of Parkinson’s disease. J. Neural Transm. (Vienna), 2017, 124(8), 901-905. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1038/s41583-019-0257-7 PMID: 31907406
  8. Kalia, L.V.; Lang, A.E. Parkinson’s disease. Lancet, 2015, 386(9996), 896-912. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1038/nrm2312 PMID: 18073771
  31. Elmore, S. Apoptosis: a review of programmed cell death. Toxicol. Pathol., 2007, 35(4), 495-516. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.3390/ijms19102973 PMID: 30274251
  49. Peti, W.; Page, R. Molecular basis of MAP kinase regulation. Protein Sci., 2013, 22(12), 1698-1710. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1038/sj.onc.1208875 PMID: 16044158
  57. Dhanasekaran, D.N.; Reddy, E.P. JNK signaling in apoptosis. Oncogene, 2008, 27(48), 6245-6251. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.3390/ijms18112441 PMID: 29149058
  78. Pettmann, B.; Henderson, C.E. Neuronal cell death. Neuron, 1998, 20(4), 633-647. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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 doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1038/ncb1405 PMID: 16604061
  125. Bernkopf, D.B.; Behrens, J. Cell intrinsic Wnt/β-catenin signaling activation. Aging, 2018, 10(5), 855-856. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.fct.2018.08.064 PMID: 30171970

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