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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2019; 65(3): 61-72


Nonel approaches to correction of mitochondrial dysfunction and oxidative disorders in Parkinson’s disease

O. Gonchar1, I. Mankovska1, K. Rozova1, L. Bratus1, I. Karaban2

  1. O.O.Bogomoletz Institute of Physiology National Academy of Sciences of Ukraine, Kyiv, Ukraine
  2. D.F. Chebotarev Institute of Gerontology National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz65.03.061


Abstract

Mitochondrial dysfunction has been widely implicated in the neuronal degeneration in Parkinson’s disease (PD). The uses of mitochondria-targeted protective compounds that prevent or minimize a wide range of mitochondrial defects constitute potential therapeutic strategies in the prevention and treatment of neuronal degeneration in PD. This review discusses the latest findings in this field obtained in PD patients and animal and cellular models of PD with focusing on the effects of pharmacological agents on mitochondrial biogenesis, fission, fusion, mitophagy machinery, and transcription of endogenous cytoprotective antioxidant enzymes. We have also presented the data concerning the technologies for research and screening novel bioactive molecules to target mitochondrial dysfunction in Parkinson’s disease.

Keywords: Parkinson’s disease, mitochondrial dysfunction, mitochondria-targeted protective compounds.

References

  1. Frank C, Pari G, Rossiter JP. Approach to diagnosis of Parkinson disease. Can Fam Physician. 2006;52: 862-8.
  2.  
  3. Hudson G. The ageing brain, mitochondria and neurodegeneration. In: Reeve AK, Simcox EM, Duchen MR, Turnbull DM, eds. Mitochondrial Dysfunction in Neurodegenerative Disorders. 2nd ed. Springer Int Publishing 2016;59-80. CrossRef  
  4. Beal MF. Mitochondria take center stage in aging and neurodegeneration. Ann Neurol. 2005;58:495-505. CrossRef PubMed
  5.  
  6. Chaturvedi RK and Beal M. Mitochondrial approaches for neuroprotection. Ann NY Acad Sci. 2008;1147:395-412. CrossRef PubMed PubMedCentral
  7.  
  8. Langston JW, Ballard P, Tetrud JW and Irwin I. Chronic Parkinsonism in humans due to a product of meperidineanalog synthesis. Science. 1983;219:979-80. - CrossRef PubMed
  9.  
  10. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol. 2003; 53 (suppl 3):S26-36 doi:10.1002/ana.10483 CrossRef PubMed
  11.  
  12. Lin MT and Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006;443:787-95. CrossRef PubMed
  13.  
  14. Pan-Montojo F, Schwarz M, Winkler C, Arnhold M, O'Sullivan GA, Pal A, Said J, Marsico G, Verbavatz JM, Rodrigo-Angulo M, Gille G, Funk RH, Reichmann H. Environmental toxins trigger PD-like progression via increased alpha-synuclein release from enteric neurons in mice. Sci Rep. 2012;2:898. CrossRef PubMed PubMedCentral
  15.  
  16. Majd S, Power JH, Grantham HJ. Neuronal response in Alzheimer's and Parkinson's disease: the effect of toxic proteins on intracellular pathways. BMC Neurosci. 2015;16:69. CrossRef PubMed PubMedCentral
  17.  
  18. Cannon JR, Greenamyre JT. Neurotoxic in vivo models of Parkinson's disease recent advances. Prog Brain Res. 2010;184:17-33. CrossRef  
  19. Picard M, McManus MJ. Mitochondrial signaling and neurodegeneration. In: Reeve AK, Simcox EM, Duchen MR, Turnbull DM, eds. Mitochondrial Dysfunction in Neurodegenerative Disorders. 2nd ed. Springer Int Publishing 2016;107-37. CrossRef  
  20. Smith RAJ, Hartley RC, Cocheme HM, Murphy MP. Mitochondrial pharmacology. Trends Pharm Sci. 2012;33(6):341-52. CrossRef PubMed
  21.  
  22. Hudson G, Nalls M, Evans JR, Breen DP, Winder-Rhodes S, Morrison KE, Morris HR, Williams-Gray CH, Barker RA, Singleton AB, Hardy J, Wood NE, Burn DJ, Chinnery PF. Two-stage association study and meta-analysis of mitochondrial DNA variants in Parkinson's disease. Neurology. 2013;80:2042-48. CrossRef PubMed PubMedCentral
  23.  
  24. Leonard JV, Schapira AH. Mitochondrial respiratory chain disorders II: neurodegenerative disorders and nuclear gene defects. Lancet 2000;355:389-94. CrossRef  
  25. Taira T, Saito Y, Niki T, Iguchi-Ariga SM, Takahashi K, Ariga H. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep. 2004;5:213-18. CrossRef PubMed PubMedCentral
  26.  
  27. Moore DJ, Zhang L, Troncoso J, Lee MK, Hattori N, Mizuno Y, Dawson TM, Dawson VL. Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum Mol Genet. 2005;14:71-84. CrossRef PubMed
  28.  
  29. Schapira AH. Mitochondria in the aetiology and pathogenesis of Parkinson's disease. Lancet Neurol. 2008;7:97-109. CrossRef  
  30. Bose A and Beal MF. Mitochondrial dysfunction in Parkinson's disease. J Neurochem. 2016; 139(Suppl.1):216-31. CrossRef PubMed
  31.  
  32. Ryan BJ, Hoek S, Fon EA, Wade-Martins R. Mitochondrial dysfunction and mitophagy in Parkinson's: From familial to sporadic disease. Trends Biochem Sci. 2015; 40:200-10. CrossRef PubMed
  33.  
  34. Truban D, Hou X, Caulfield TR, Fiesel FC, Springer W. PINK 1, Parkin, and Mitochondrial Quality Control: What can we learn about Parkinson's disease pathobiology? J Parkinson's disease. 2017;7:13-29. CrossRef PubMed PubMedCentral
  35.  
  36. Schapira HV, Olanow CW, Greenamyre JT, Bezard E. Slowing of neurodegeneration in Parkinson's disease and Huntington's disease: future therapeutic perspectives. The Lancet. 2014;384:545-55. CrossRef  
  37. Stewart VC, Heales SJ. Nitric oxide-induced mitochondrial dysfunction: Implications for neurodegeneration. Free Radic Biol Med. 2003; 34:287-303. CrossRef  
  38. Henchcliffe C and Beal MF. Mitochondrial biology and oxidative stress in Parkinson's disease pathogenesis. Nature Clin Pract Neurol. 2008;4:600-09. CrossRef PubMed
  39.  
  40. Narendra DP, Youle RJ. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal. 2011;14:1929-38. CrossRef PubMed PubMedCentral
  41.  
  42. Perier C, Bové J, Dehay B, Jackson-Lewis V, Rabinovitch PS, Przedborski S, and Vila M. Apoptosis-inducing factor deficiency sensitizes dopaminergic neurons to parkinsonian neurotoxins. Ann Neurol. 2010;68:184-92. CrossRef PubMed
  43.  
  44. Franco-Iborra S, Vila M, Perier C. The Parkinson's disease mitochondrial hypothesis: where are we at? Neuroscientist 2016;22:266-77. CrossRef PubMed
  45.  
  46. Milane L, Trivedi M, Singh A, Talekar M, Amiji M. Mitochondrial biology, targets, and drug delivery. J Control Release. 2015;207:40-58. CrossRef PubMed
  47.  
  48. Teicher BA, Holden SA, Cathcart KN. Efficacy of Pt(Rh-123)2 as a radiosensitizer with fractionated X rays. Int J Radiat Oncol Biol Phys. 1987;13:1217-24. CrossRef  
  49. Szeto HH, Schiller PW. Novel therapies targeting inner mitochondrial membrane - from discovery to clinical development. Pharm Res. 2011; 28:2669-79. CrossRef PubMed
  50.  
  51. Yousif LF, Stewart KM, Kelley SO. Targeting mitochondria with organelle-specific compounds: strategies and applications. Chem Biochem. 2009;10:1939-50. CrossRef PubMed
  52.  
  53. Snow BJ, Rolfe FL, Lockhart MM, Frampton CM, O'Sullivan JD, Fung V, Smith RA, Murphy MP, Taylor KM. A double-blind, placebo-controlled study to assess the mitochondria-targeted antioxidant MitoQ as a disease-modifying therapy in Parkinson's disease. Mov Disord. 2010; 25:1670-74. CrossRef PubMed
  54.  
  55. Smith RA and Murphy MP. Animal and human studies with the mitochondria-targeted antioxidant MitoQ. Ann NY Acad Sci. 2010;1201:96-103. CrossRef PubMed
  56.  
  57. Ghosh A, Solesio ME, Prime TA, Logan A, Murphy MP. Neuroprotection by a mitochondria-targeted drug in a Parkinson's disease model. Free Radic Biol Med. 2010;49:1674-84. CrossRef PubMed PubMedCentral
  58.  
  59. Twig G, Shirihai O S. The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal. 2011;14:1939-51. CrossRef PubMed PubMedCentral
  60.  
  61. Patki G, Lau Y-S. Melatonin protects against neurobehavioral and mitochondrial deficits in a chronic mouse model of Parkinson's disease. Pharmacol Biochem Behavior. 2011;99(4):704-11. CrossRef PubMed PubMedCentral
  62.  
  63. Dabbeni-Sala F, di Santo S, Franceschini D, Skaper SD, and Giusti P. Melatonin protects against 6-OHDAinduced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB J. 2001;15(1):164-70. CrossRef PubMed
  64.  
  65. Strathearn KE, Yousef GG, Grace MH, Roy SL, Tambe MA, Ferruzzi MG, Wu QL, Simon JE, Lila MA, Rochet JC. Neuroprotective effects of anthocyanin- and proanthocyanidin-rich extracts in cellular models of Parkinson's disease. Brain Res. 2014; 1555:60-77. CrossRef PubMed PubMedCentral
  66.  
  67. Geed M, Garabadu D, Ahmad A, and Krishnamurthy S. Silibinin pretreatment attenuates biochemical and behavioral changes induced by intrastriatal MPP+ injection in rats. Pharmacol Biochem Behavior. 2014;117:92-103. CrossRef PubMed
  68.  
  69. Guo S, Bezard E, and Zhao B. Protective effect of green tea polyphenols on the SH-SY5Y cells against 6-OHDA induced apoptosis through ROS-NO pathway. Free Radic Biol Med. 2005;39(5):682-95. CrossRef PubMed
  70.  
  71. Hwang CK, Chun HS. Isoliquiritigenin isolated from licorice Glycyrrhiza uralensis prevents 6-hydroxydopamine induced apoptosis in dopaminergic neuron. Biosci Biotechnol Biochem. 2012;76(3):536-43. CrossRef PubMed
  72.  
  73. Kim HG, Ju MS, Kim DH, Hong J, Cho SH, Cho KH, Park W, Lee EH, Kim SY, Oh MS Protective effects of Chunghyuldan against ROS-mediated neuronal cell death in models of Parkinson's disease. Basic Clin Pharmacol Toxicol. 2010; 107 (6):958-64. CrossRef PubMed
  74.  
  75. Tamilselvam K, Braidy N, Manivasagam T, Essa MM, Prasad NR, Karthikeyan S, Thenmozhi AJ, Selvaraju S, Guillemin GJ. Neuroprotective effects of hesperidin, a plant flavanone, on rotenone induced oxidative stress and apoptosis in a cellular model for Parkinson's disease. Oxid Med Cell Longev. 2013;2013:102741. CrossRef PubMed PubMedCentral
  76.  
  77. Karuppagounder SS, Madathil SK, Pandey M, Haobam R, Rajamma U, Mohanakumar KP. Quercetin up-regulates mitochondrial complex I activity to protect against programmed cell death in rotenone model of Parkinson's disease in rats. Neuroscience. 2013;236:136-48. CrossRef PubMed
  78.  
  79. Bournival J, Plouffe M, Renaud J, Provencher C, Martinoli M-G. Quercetin and sesamin protect dopaminergic cells from MPP+-induced neuroinflammation in a microglial (N9)-neuronal (PC12) coculture system. Oxid Med Cell Longev. 2012; 11. CrossRef PubMed PubMedCentral
  80.  
  81. Wang Y-H, Yu H-T, Pu X-P, Du G-H. Baicalein prevents 6-hydroxydopamine-induced mitochondrial dysfunction in SH-SY5Y cells via inhibition of mitochondrial oxidation and up-regulation of DJ-1 protein expression. Molecules. 2013 ;18(12):14726-38. CrossRef PubMed PubMedCentral
  82.  
  83. Li XX, He GR, Mu X, Xu B, Tian S, Yu X, Meng FR, Xuan ZH, Du GH. Protective effects of baicalein against rotenone-induced neurotoxicity in PC12 cells and isolated rat brain mitochondria. Eur J Pharmacol. 2012;674(2- 3):227-33. CrossRef PubMed
  84.  
  85. Jagatha B, Mythri RB, Vali S, Bharath M. M. S. Curcumin treatment alleviates the effects of glutathione depletion in vitro and in vivo: therapeutic implications for Parkinson's disease explained via in silico studies. Free Radic Biol Med. 2008;44(5):907-17. CrossRef PubMed
  86.  
  87. Liu Z, Yu Y, Li X, Ross CA, Smith WW. Curcumin protects against A53T alpha-synuclein-induced toxicity in a PC12 inducible cell model for Parkinsonism. Pharmacol Res. 2011;63(5):439-44. CrossRef PubMed
  88.  
  89. Subramaniam SR and Ellis EM. Neuroprotective effects of umbelliferone and esculetin in a mouse model of Parkinson's disease. J Neurosci Res. 2013;91(3):453-61. CrossRef PubMed
  90.  
  91. Liu WB, Zhou J, Qu Y, Li X, Lu CT, Xie KL, Sun XL, Fei Z. Neuroprotective effect of osthole on MPP+-induced cytotoxicity in PC12 cells via inhibition of mitochondrial dysfunction and ROS production. Neurochem Int. 2010;57(3):206-15. CrossRef PubMed
  92.  
  93. Yi F, He X, Wang D. Lycopene protects against MPP+-induced cytotoxicity by maintaining mitochondrial function in SH-SY5Y cells. Neurochem Res. 2013;38(8):1747-57. CrossRef PubMed
  94.  
  95. Kaur H, Chauhan S, Sandhir R. Protective effect of lycopene on oxidative stress and cognitive decline in rotenone induced model of Parkinson's disease. Neurochemic Res. 2011 ;36(8):1435-43. CrossRef PubMed
  96.  
  97. Seidl SE and Potashkin JA. The promise of neuroprotective agents in Parkinson's disease.Front Neurol; 2011; 2: 68. CrossRef PubMed PubMedCentral
  98.  
  99. Helliwell SB.. Development of treatments and therapies to target mitochondrial dysfunction. In: Reeve AK, Simcox EM, Duchen MR, Turnbull DM, eds. Mitochondrial Dysfunction in Neurodegenerative Disorders. Springer 2nd ed. Int Publishing 2016;349-371. CrossRef  
  100. Moosmann B and Behl C. Antioxidants as treatment for neurodegenerative disorders. Expert Opin Invest Drugs. 2002;11:1407-35. CrossRef PubMed
  101.  
  102. van Muiswinkel FL and Kuiperij HB. The Nrf2-ARE signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders. Curr Drug Targets CNS Neurol Disord. 2005;4:267-81. CrossRef PubMed
  103.  
  104. Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol. 2003; 43:233-60. CrossRef PubMed
  105.  
  106. Surh YJ, Kundu JK, Na HK. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 2008;74:1526-39. CrossRef PubMed
  107.  
  108. Wu KC, McDonald PR, Liu J, Klaassen CD. Screening of natural compounds as activators of the Keap 1-Nrf2 pathway. Planta Med. 2013;80:97-104. CrossRef PubMed PubMedCentral
  109.  
  110. Calkins MJ, Johnson DA, Townsend JA, Vargas MR, Dowell JA, Williamson TP, Kraft AD, Lee JM, Li J, Johnson JA. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal. 2009;11:497-508. CrossRef PubMed PubMedCentral
  111.  
  112. Lee C, Park GH, Lee SR, Jang JH. Attenuation of betaamyloid-induced oxidative cell death by sulforaphane via activation of NF-E2-related factor 2. Oxid Med Cell Longev. 2013; 2013 :313510. CrossRef PubMed PubMedCentral
  113.  
  114. Eggler AL, Gay KA, Mesecar AD. Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2. Mol Nutr Food Res. 2008;52 (Suppl. 1):S84-S94. CrossRef PubMed
  115.  
  116. Yang L, Zhao K, Calingasan NY, Luo G, Szeto HH, Beal MF. Mitochondria targeted peptides protect against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity. Antioxid Redox Signal. 2009;11:2095-2104. CrossRef PubMed PubMedCentral
  117.  
  118. Miclea A, Leussink VI, Hartung HP, Gold R, and Hoepner R. Safety and efficacy of dimethyl fumarate in multiple sclerosis: a multi-center observational study. J Neurol. 2016. CrossRef PubMed
  119.  
  120. Ahuja M, Ammal Kaidery N, Yang L, Calingasan N, Smirnova N, Gaisin A, Gaisina IN, Gazaryan I, Hushpulian DM, Kaddour-Djebbar I, Bollag WB, Morgan JC, Ratan RR, Starkov AA, Beal MF, Thomas B. Distinct Nrf2 signaling mechanisms of fumaric acid esters and their role in neuroprotection against 1-methyl-4- phenyl-1,2,3,6- tetrahydropyridine-induced experimental Parkinson's-like disease. J Neurosci. 2016;36:6332-51. CrossRef PubMed PubMedCentral
  121.  
  122. Wenz T. Regulation of mitochondrial biogenesis and PGC-1alpha under cellular stress. Mitochondrion. 2013;13(2):134-42. CrossRef PubMed
  123.  
  124. Chen H and Chan DC. Mitochondrial dynamics in mammals. Curr Top Dev Biol. 2004; 59:119-44. CrossRef  
  125. Mishra P, Carelli V, Manfredi G, Chan DC. Proteolytic cleavage of Opa 1 stimulates mitochondrial inner membrane fusion and couples fusion to oxidative phosphorylation. Cell Metab. 2014;19(4):630-41. CrossRef PubMed PubMedCentral
  126.  
  127. Mourier A. Mitochondrial dynamics and neurodegeneration. In: Reeve AK, Simcox EM, Duchen MR, Turnbull DM, eds. Mitochondrial Dysfunction in Neurodegenerative Disorders. Springer 2nd ed. Int Publishing 2016;175-191. CrossRef  
  128. Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Publ Gr. 2011;12(1):9-14. CrossRef PubMed PubMedCentral
  129.  
  130. Wang D, Wang J, Bonamy GM, Meeusen S, Brusch RG, Turk C, Yang P, Schultz PG. A small molecule promotes mitochondrial fusion in mammalian. Angew Chem. 2012;51:9302-5. CrossRef PubMed
  131.  
  132. Yue W, Chen Z, Liu H, Yan C, Chen M, Feng D, Yan C, Wu H, Du L, Wang Y, Liu J, Huang X, Xia L, Liu L, Wang X, Jin H, Wang J, Song Z, Hao X, Chen Q. A small natural molecule promotes mitochondrial fusion through inhibition of the deubiquitinase USP30. Cell Res. 2014; 24(4) :482-96. CrossRef PubMed PubMedCentral
  133.  
  134. Rappold PM, Cui M, Grima JC, Fan RZ, de Mesy-Bentley KL, Chen L, Zhuang X, Bowers WJ, Tieu K. Drp1 inhibition attenuates neurotoxicity and dopamine release deficits in vivo. Nat Commun. 2014; 5:5244. CrossRef PubMed PubMedCentral
  135.  
  136. Taymans JM, Greggio E. LRRK2 Kinase Inhibition as a Therapeutic Strategy for Parkinson's Disease. Where Do We Stand ? Curr Neuropharmacol. 2016;14(3):214-25. CrossRef PubMed PubMedCentral
  137.  
  138. Ventura-Clapier R, Garnier A, Veksler V.Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res. 2008;79:208-17. CrossRef PubMed
  139.  
  140. Mudò G, Mäkelä J, Di Liberto V, Tselykh TV, Olivieri M, Piepponen P, Eriksson O, Mälkiä A, Bonomo A, Kairisalo M, Aguirre JA, Korhonen L, Belluardo N, Lindholm D. Transgenic expression and activation of PGC-1α protect dopaminergic neurons in the MPTP mouse model of Parkinson's disease. Cell Mol Life Sci. 2012; 69:1153-65. CrossRef PubMed
  141.  
  142. Borra MT, Smith BC, Denu JM. Mechanism of human SIRT 1 activation by resveratrol. J Biol Chem. 2005;280(17):17187-95. CrossRef PubMed
  143.  
  144. Hasegawa K, Yasuda T, Shiraishi C, Fujiwara K, Przedborski S, Mochizuki H, Yoshikawa K. Promotion of mitochondrial biogenesis by necdin protects neurons against mitochondrial insults. Nat Commun. 2016;7:10943. CrossRef PubMed PubMedCentral
  145.  
  146. Otten EG, Manni D, Korolchuk VI. Mitochondrial degradation, autophagy and neurodegenerative disease. In: Reeve AK, Simcox EM, Duchen MR, Turnbull DM, eds. Mitochondrial Dysfunction in Neurodegenerative Disorders. 2nd ed. Springer Int Publishing 2016;255-278. CrossRef  
  147. Corti O, Lesage S, Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol Rev. 2011;91(4):1161-218. CrossRef PubMed
  148.  
  149. Trempe JF and Fon EA. Structure and function of Parkin, PINK 1, and DJ-1, the three musketeers of neuroprotection. Front Neurol. 2013;4:38. CrossRef PubMed PubMedCentral
  150.  
  151. Palacino JJ, Sagi D, Goldberg MS, Krauss S, Motz C, Wacker M, Klose J, Shen J. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J Biol Chem. 2004;279(18):18614-22. CrossRef PubMed
  152.  
  153. Gandhi S, Wood-Kaczmar A, Yao Z, Plun-Favreau H, Deas E, Klupsch K, Downward J, Latchman DS, Tabrizi SJ, Wood NW, Duchen MR, Abramov AY. PINK 1 - associated Parkinson's disease is caused by neuronal vulnerability to calcium-induced cell death. Mol cell. 2009;33(5):627-38. CrossRef PubMed PubMedCentral
  154.  
  155. Canet-Avilés RM, Wilson MA, Miller DW, Ahmad R, McLendon C, Bandyopadhyay S, Baptista MJ, Ringe D, Petsko GA, Cookson MR The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci USA. 2004;101(24):9103-8. CrossRef PubMed PubMedCentral
  156.  
  157. Thomas KJ, McCoy MK, Blackinton J, Beilina A, van der Brug M, Sandebring A, Miller D, Maric D, CedazoMinguez A, Cookson MR. DJ-1 acts in parallel to the PINK 1/parkin pathway to control mitochondrial function and autophagy. Hum Mol Genet. 2011;20(1):40-50.
  158. Bian M, Liu J, Hong X, Yu M, Huang Y, Sheng Z, Fei J, Huang F. Overexpression of parkin ameliorates dopaminergic neurodegeneration induced by 1-methyl- 4-phenyl-1,2,3,6-tetrahydropyridine in mice. PLoS Biol. 2012;7(6):e39953. CrossRef PubMed PubMedCentral
  159.  
  160. Santos RX, Correia SC, Carvalho C, Cardoso S, Santos MS, Moreira PI. Mitophagy in neurodegeneration:an opportunity for therapy? Curr Drug Targets. 2011; 12(6):790-9. CrossRef PubMed
  161.  
  162. Cheng Y, Ren X, Hait WN, Yang JM. Therapeutic targeting of autophagy in disease: biology and pharmacology. Pharmacol Rev. 2013;65(4):1162-97. CrossRef PubMed PubMedCentral
  163.  
  164. Hasson SA, Fogel AI, Wang C, MacArthur R, Guha R, Heman-Ackah S, Martin S, Youle RJ, Inglese J. Chemogenomic profiling of endogenous PARK2 expression using a genome-edited coincidence reporter. ACS Chem Biol. 2015;10:1188-97. CrossRef PubMed
  165.  
  166. Chambers JW, Pachori A, Howard S, Ganno M, Hansen D Jr, Kamenecka T, Song X, Duckett D, Chen W, Ling YY, Cherry L, Cameron MD, Lin L, Ruiz CH, Lograsso P. Small molecule c-jun-N-terminal kinase inhibitors protect dopaminergic neurons in a model of Parkinson's disease. ACS Chem Neurosci. 2011;2(4):198-206. CrossRef PubMed PubMedCentral
  167.  
  168. Hertz NT, Berthet A, Sos ML, Thorn KS, Burlingame AL, Nakamura K, and Shokat KM. A neo-substrate that amplifies catalytic activity of Parkinson's-disease-related kinase PINK1. Cell. 2013;154:737-47. CrossRef PubMed PubMedCentral
  169.  
  170. Bingol B, Tea JS, Phu L, Reichelt M, Bakalarski CE, Song Q, Foreman O, Kirkpatrick DS & Sheng M. The mitochondrial deubiquitinase USP30 opposes parkinmediated mitophagy. Nature. 2014;510:370-75. CrossRef PubMed
  171.  
  172. Mankovska IM., Rosova KV, Gonchar OO, Nosar VI, Bratus LV, Drevitska TI, Karasevich NV, Karaban IM. Effect of Capicor on the Parkinson's disease pathogenic links. Fiziol Zh. 2018;64(1):16-24 [Ukraine]. CrossRef  
  173. Gardian G, Yang L, Cleren C, Calingasan NY, Klivenyi P, Beal MF. Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity. Neuromolecular Med. 2004;5:235-241. CrossRef  
  174. Inden M, Kitamura Y, Takeuchi H, Yanagida T, Takata K, Kobayashi Y, Taniguchi T, Yoshimoto K, Kaneko M, Okuma Y, Taira T, Ariga H, and Shimohama S. Neurodegeneration of mouse nigrostriatal dopaminergic system induced by repeated oral administration of rotenone is prevented by 4-phenylbutyrate, a chemical chaperone. J Neurochem. 2007;101:1491-1504. CrossRef PubMed
  175.  
  176. Wilkins HM, Carl SM, Swerdlow RH. Cytoplasmic hybrid (cybrid) cell lines as a practical model for mitochondriopathies. Redox Biol. 2014;2(1):619-31. CrossRef PubMed PubMedCentral
  177.  
  178. Cooper O, Seo H, Andrabi S, Guardia-laguarta C. Pharmacological rescue of mitochondrial deficis in iPSC-derived neural cells from patients with familial Parkinson's disease. Sci Transl Med. 2012;4(141):141-90. CrossRef PubMed PubMedCentral
  179.  
  180. Sanders LH, Laganière J, Cooper O, Mak SK, Vu BJ, Huang YA, Paschon DE, Vangipuram M, Sundararajan R, Urnov FD, Langston JW, Gregory PD, Zhang HS, Greenamyre JT, Isacson O, Schüle B. LRRK2 mutations cause mitochondrial DNA damage in iPSC-derived neural cells from Parkinson's disease patients: reversal by gene correction. Neurobiol Dis. 2014;62:381-6. CrossRef PubMed PubMedCentral
  181.  
  182. Tang FL, Liu W, Hu JX, Erion JR, Ye J, Mei L, Xiong WC. VPS35 deficiency or mutation causes dopaminergic neuronal loss by impairing mitochondrial fusion and function. Cell Rep. 2015;12:1631-43. CrossRef PubMed PubMedCentral
  183.  
  184. Dong J, Li S, Mo JL, Cai HB, Le WD. Nurr1-based therapies for Parkinson's disease. CNS Neurosci Ther. 2016;22:351-59. CrossRef PubMed PubMedCentral
  185.  
  186. Lotharius J, Dugan LL, O'Malley KL. Distinct mechanisms underlie neurotoxin-mediated cell death in cultured dopaminergic neurons. J Neurosci Res. 1999;19(4):1284-93. CrossRef  
  187. Jin H, Chen WQ, Tang XW, Chiang LY, Yang CY, Schloss JV, Wu JY. Polyhydroxylated C60, fullerenols, as glutamate receptor antagonists and neuroprotective agents. J Neurosci Res. 2000;62:600-7. CrossRef  
  188. Foley S, Crowley C, Smaihi M, Bonfils C, Erlanger BF, Seta P, Larroque C. Cellular localisation of a water-soluble fullerene derivative. Biochem Biophys Res Commun. 2002;294 (1) :116-19. CrossRef  
  189. Cai X, Jia H, Liu Z, Hou B, Luo C, Feng Z, Li W, Liu J. Polyhydroxylated fullerene derivative C60(OH)24 prevents mitochondrial dysfunction and oxidative damage in an MPP+-induced cellular model of Parkinson's disease. J Neurosci Res. 2008;86(16): 3622-34. CrossRef PubMed
  190.  
  191. Prylutskyy YI, Vereshchaka IV, Maznychenko AV, Bulgakova NV, Gonchar OO, Kyzyma OA, Ritter U, Scharff P, Tomiak T, Nozdrenko DM, Mishchenko IV, Kostyukov AI. C60 fullerene as promising therapeutic agent for correcting and preventing skeletal muscle fatigue. J Nanobiotechnol. 2017; 15:8. CrossRef PubMed PubMedCentral
  192.  
  193. Gonchar O., Maznychenko A., Bulgakova N., Vereschaka I., Tomiak T., Ritter U., Prylutskyy Y., Mankovska I., Kostyukov A. C60 Fullerene prevents restraint stressinduced oxidative disorders in rat tissues: possible involvement of the Nrf2/ARE-antioxidant pathway. Oxid Med Cell Long. 2018; 2018 (Article ID 2518676): 17 CrossRef PubMed PubMedCentral
  194.  

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