Mutant PINK1 upregulates tyrosine hydroxylase and dopamine levels, leading to vulnerability of dopaminergic neurons

Free Radical Biology and Medicine

Volumn 68, Issue , 2014, Pages 220-233

  Zhou, Zhi Dong ^a,b   Refai, Fathima Shaffra ^a   Xie, Shao Ping ^a   Ng, Shin Hui ^a   Chan, Christine Hui Shan ^a   Ho, Patrick Ghim Hoe ^a   Zhang, Xiao Dong ^b   Lim, Tit Meng ^c   Tan, Eng King ^a,b,d  

^a NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d SINGAPORE GENERAL HOSPITAL   (Singapore)

Author keywords

Dopamine; Free radicals; Iron; Neurodegeneration; Parkinson disease; PINK1; Tyrosine hydroxylase

Indexed keywords

CASPASE 3; DOPAMINE; MUTANT PROTEIN; PINK1 PROTEIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; DOPAMINERGIC NERVE CELL; ENZYME ACTIVATION; ENZYME INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOCYTOCHEMISTRY; NERVE DEGENERATION; NONHUMAN; OXIDATIVE STRESS; PC12 CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; TRANSIENT TRANSFECTION; UPREGULATION;

DOPAMINE; FREE RADICALS; IRON; NEURODEGENERATION; PARKINSON DISEASE; PINK1; TYROSINE HYDROXYLASE;

CELL LINE; DOPAMINE; DOPAMINERGIC NEURONS; FREE RADICALS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; MUTATION; OXIDATIVE STRESS; PARKINSON DISEASE; PROTEIN KINASES; TYROSINE 3-MONOOXYGENASE;

EID: 84892188116     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.12.015     Document Type: Article

References (55)

1. V.S. Van Laar, and S.B. Berman Mitochondrial dynamics in Parkinson's disease Exp. Neurol. 218 2009 247 256
2. J. Parkinson An essay on the shaking palsy: 1817 J. Neuropsychiatry Clin. Neurosci. 14 2002 223 236 (discussion 222)
3. A. Abeliovich Parkinson's disease: pro-survival effects of PINK1 Nature 448 2007 759 760 (Pubitemid 47266328)
4. T. Kitada, S. Asakawa, H. Matsumine, N. Hattori, S. Minoshima, N. Shimizu, and Y. Mizuno Positional cloning of the autosomal recessive juvenile parkinsonism (AR-JP) gene and its diversity in deletion mutations Parkinsonism Relat. Disord. 5 1999 163 168 (Pubitemid 29408670)
5. A. Zimprich, S. Biskup, P. Leitner, P. Lichtner, M. Farrer, S. Lincoln, J. Kachergus, M. Hulihan, R.J. Uitti, D.B. Calne, A.J. Stoessl, R.F. Pfeiffer, N. Patenge, I.C. Carbajal, P. Vieregge, F. Asmus, B. Müller-Myhsok, D.W. Dickson, T. Meitinger, T.M. Strom, Z.K. Wszolek, and T. Gasser Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology Neuron 44 2004 601 607 (Pubitemid 39531225)
6. E.M. Valente, P.M. Abou-Sleiman, V. Caputo, M.M.K. Muqit, K. Harvey, S. Gispert, Z. Ali, D. Del Turco, A.R. Bentivoglio, D.G. Healy, A. Albanese, R. Nussbaum, R. Gonzalez-Maldonado, T. Deller, S. Salvi, P. Cortelli, W.P. Gilks, D.S. Latchman, R.J. Harvey, B. Dallapiccola, G. Auburger, and N.W. Wood Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 2004 1158 1160 (Pubitemid 38661852)
7. V. Bonifati, P. Rizzu, F. Squitieri, E. Krieger, N. Vanacore, J.C. Swieten, A. Brice, C.M. Duijn, B. Oostra, G. Meco, and P. Heutink DJ-1(PARK7), a novel gene for autosomal recessive, early onset parkinsonism Neurol. Sci. 24 2003 159 160 (Pubitemid 37304291)
8. A. Di Fonzo, M.C. Dekker, P. Montagna, A. Baruzzi, E.H. Yonova, L. Correia Guedes, A. Szczerbinska, T. Zhao, L.O. Dubbel-Hulsman, C.H. Wouters, E. de Graaff, W.J. Oyen, E.J. Simons, G.J. Breedveld, B.A. Oostra, M.W. Horstink, and V. Bonifati FBXO7 mutations cause autosomal recessive, early-onset parkinsonian-pyramidal syndrome Neurology 72 2009 240 245
9. T. Zhao, E. De Graaff, G.J. Breedveld, A. Loda, L.A. Severijnen, C.H. Wouters, F.W. Verheijen, M.C. Dekker, P. Montagna, R. Willemsen, B.A. Oostra, and V. Bonifati Loss of nuclear activity of the FBXO7 protein in patients with parkinsonian-pyramidal syndrome (PARK15) PLoS One 6 2011 e16983
10. R.D. Mills, C.H. Sim, S.S. Mok, T.D. Mulhern, J.G. Culvenor, and H.-C. Cheng Biochemical aspects of the neuroprotective mechanism of PTEN-induced kinase-1 (PINK1) J. Neurochem. 105 2008 18 33 (Pubitemid 351441646)
11. I.E. Clark, M.W. Dodson, C. Jiang, J.H. Cao, J.R. Huh, J.H. Seol, S.J. Yoo, B.A. Hay, and M. Guo Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin Nature 441 2006 1162 1166 (Pubitemid 43990738)
12. N. Exner, B. Treske, D. Paquet, K. Holmstrom, C. Schiesling, S. Gispert, I. Carballo-Carbajal, D. Berg, H.-H. Hoepken, T. Gasser, R. Kruger, K.F. Winklhofer, F. Vogel, A.S. Reichert, G. Auburger, P.J. Kahle, B. Schmid, and C. Haass Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin J. Neurosci. 27 2007 12413 12418 (Pubitemid 350085485)
13. R.K. Dagda, S.J. Cherra, S.M. Kulich, A. Tandon, D. Park, and C.T. Chu Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission J. Biol. Chem. 284 2009 13843 13855
14. A. Wood-Kaczmar, S. Gandhi, Z. Yao, A.S.Y. Abramov, E.A. Miljan, G. Keen, L. Stanyer, I. Hargreaves, K. Klupsch, E. Deas, J. Downward, L. Mansfield, P. Jat, J. Taylor, S. Heales, M.R. Duchen, D. Latchman, S.J. Tabrizi, and N.W. Wood PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons PLoS One 3 2008 e2455
15. Y. Yang, S. Gehrke, Y. Imai, Z. Huang, Y. Ouyang, J.-W. Wang, L. Yang, M.F. Beal, H. Vogel, and B. Lu Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin Proc. Natl. Acad. Sci. USA 103 2006 10793 10798 (Pubitemid 44078055)
16. J. Park, S.B. Lee, S. Lee, Y. Kim, S. Song, S. Kim, E. Bae, J. Kim, M. Shong, J.-M. Kim, and J. Chung Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin Nature 441 2006 1157 1161 (Pubitemid 43990737)
17. S.M. Jin, and R.J. Youle PINK1- and Parkin-mediated mitophagy at a glance J. Cell Sci 125 2012 795 799
18. A.J. Whitworth, and L.J. Pallanck The PINK1/Parkin pathway: a mitochondrial quality control system? J. Bioenerg. Biomembr. 41 2009 499 503
19. S. Gandhi, M.M. Muqit, L. Stanyer, D.G. Healy, P.M. Abou-Sleiman, I. Hargreaves, S. Heales, M. Ganguly, L. Parsons, A.J. Lees, D.S. Latchman, J.L. Holton, N.W. Wood, and T. Revesz PINK1 protein in normal human brain and Parkinson's disease Brain 129 2006 1720 1731 (Pubitemid 43999406)
20. A. Beilina, M. Van Der Brug, R. Ahmad, S. Kesavapany, D.W. Miller, G.A. Petsko, and M.R. Cookson Mutations in PTEN-induced putative kinase 1 associated with recessive parkinsonism have differential effects on protein stability Proc. Natl. Acad. Sci. USA 102 2005 5703 5708 (Pubitemid 40559623)
21. A. Weihofen, B. Ostaszewski, Y. Minami, and D.J. Selkoe Pink1 Parkinson mutations, the Cdc37/Hsp90 chaperones and Parkin all influence the maturation or subcellular distribution of Pink1 Hum. Mol. Genet. 17 2008 602 616 (Pubitemid 351201772)
22. S. Takatori, G. Ito, and T. Iwatsubo Cytoplasmic localization and proteasomal degradation of N-terminally cleaved form of PINK1 Neurosci. Lett. 430 2008 13 17
23. W. Lin, and U.J. Kang Characterization of PINK1 processing, stability, and subcellular localization J. Neurochem. 106 2008 464 474 (Pubitemid 351840220)
24. M.E. Haque, K.J. Thomas, C. D'Souza, S. Callaghan, T. Kitada, R.S. Slack, P. Fraser, M.R. Cookson, A. Tandon, and D.S. Park Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP Proc. Natl. Acad. Sci. USA 105 2008 1716 1721 (Pubitemid 351346580)
25. E.K. Tan, F.S. Refai, M. Siddique, K. Yap, P. Ho, S. Fook-Chong, and Y. Zhao Clinically reported heterozygous mutations in the PINK1 kinase domain exert a gene dosage effect Hum. Mutat. 30 2009 1551 1557
26. D.D. Sarbassov, D.A. Guertin, S.M. Ali, and D.M. Sabatini Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex Science 307 2005 1098 1101 (Pubitemid 40262113)
27. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) Method Methods 25 2001 402 408 (Pubitemid 34164012)
28. E.M. Valente, P.M. Abou-Sleiman, V. Caputo, M.M. Muqit, K. Harvey, S. Gispert, Z. Ali, D. Del Turco, A.R. Bentivoglio, D.G. Healy, A. Albanese, R. Nussbaum, R. Gonzalez-Maldonado, T. Deller, S. Salvi, P. Cortelli, W.P. Gilks, D.S. Latchman, R.J. Harvey, B. Dallapiccola, G. Auburger, and N.W. Wood Hereditary early-onset Parkinson's disease caused by mutations in PINK1 Science 304 2004 1158 1160 (Pubitemid 38661852)
29. V. Bonifati, C.F. Rohe, G.J. Breedveld, E. Fabrizio, M. De Mari, C. Tassorelli, A. Tavella, R. Marconi, D.J. Nicholl, H.F. Chien, E. Fincati, G. Abbruzzese, P. Marini, A. De Gaetano, M.W. Horstink, J.A. Maat-Kievit, C. Sampaio, A. Antonini, F. Stocchi, P. Montagna, V. Toni, M. Guidi, A. Dalla Libera, M. Tinazzi, F. De Pandis, G. Fabbrini, S. Goldwurm, A. de Klein, E. Barbosa, L. Lopiano, E. Martignoni, P. Lamberti, N. Vanacore, G. Meco, and B.A. Oostra Early-onset parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes Neurology 65 2005 87 95 (Pubitemid 40967781)
30. Y. Hatano, Y. Li, K. Sato, S. Asakawa, Y. Yamamura, H. Tomiyama, H. Yoshino, M. Asahina, S. Kobayashi, S. Hassin-Baer, C.S. Lu, A.R. Ng, R.L. Rosales, N. Shimizu, T. Toda, Y. Mizuno, and N. Hattori Novel PINK1 mutations in early-onset parkinsonism Ann. Neurol. 56 2004 424 427 (Pubitemid 39166562)
31. R. Kumazawa, H. Tomiyama, Y. Li, Y. Imamichi, M. Funayama, H. Yoshino, F. Yokochi, T. Fukusako, Y. Takehisa, K. Kashihara, T. Kondo, B. Elibol, S. Bostantjopoulou, T. Toda, H. Takahashi, F. Yoshii, Y. Mizuno, and N. Hattori Mutation analysis of the PINK1 gene in 391 patients with Parkinson disease Arch. Neurol. 65 2008 802 808 (Pubitemid 351831459)
32. V. Scornaienchi, D. Civitelli, E.V. De Marco, G. Annesi, P. Tarantino, F.E. Rocca, V. Greco, G. Provenzano, F. Annesi, G. Nicoletti, C. Colica, A. Uncini, M. Salsone, F. Novellino, M. Morelli, G. Arabia, A. Gambardella, and A. Quattrone Mutation analysis of the PINK1 gene in Southern Italian patients with early- and late-onset parkinsonism Parkinsonism Relat. Disord. 18 2012 651 653
33. E.M. Valente, S. Salvi, T. Ialongo, R. Marongiu, A.E. Elia, V. Caputo, L. Romito, A. Albanese, B. Dallapiccola, and A.R. Bentivoglio PINK1 mutations are associated with sporadic early-onset parkinsonism Ann. Neurol. 56 2004 336 341 (Pubitemid 39166552)
34. C. Klein, K. Lohmann-Hedrich, E. Rogaeva, M.G. Schlossmacher, and A.E. Lang Deciphering the role of heterozygous mutations in genes associated with parkinsonism Lancet Neurol. 6 2007 652 662 (Pubitemid 46921058)
35. R. Marongiu, A. Ferraris, T. Ialongo, S. Michiorri, F. Soleti, F. Ferrari, A.E. Elia, D. Ghezzi, A. Albanese, M.C. Altavista, A. Antonini, P. Barone, L. Brusa, P. Cortelli, P. Martinelli, M.T. Pellecchia, G. Pezzoli, C. Scaglione, P. Stanzione, M. Tinazzi, A. Zecchinelli, M. Zeviani, E. Cassetta, B. Garavaglia, B. Dallapiccola, A.R. Bentivoglio, and E.M. Valente PINK1 heterozygous rare variants: prevalence, significance and phenotypic spectrum Hum. Mutat. 29 2008 565
36. E.K. Tan, and L.M. Skipper Pathogenic mutations in Parkinson disease Hum. Mutat. 28 2007 641 653 (Pubitemid 47047290)
37. Z.D. Zhou, Y.H. Lan, E.K. Tan, and T.M. Lim Iron species-mediated dopamine oxidation, proteasome inhibition, and dopaminergic cell demise: implications for iron-related dopaminergic neuron degeneration Free Radic. Biol. Med. 49 2010 1856 1871
38. Z. Zhou, S. Kerk, and T. Meng Lim Endogenous dopamine (DA) renders dopaminergic cells vulnerable to challenge of proteasome inhibitor MG132 Free Radic. Res. 42 2008 456 466 (Pubitemid 351935159)
39. A.R. Giandomenico, G.E. Cerniglia, J.E. Biaglow, C.W. Stevens, and C.J. Koch The importance of sodium pyruvate in assessing damage produced by hydrogen peroxide Free Radic. Biol. Med. 23 1997 426 434 (Pubitemid 27276779)
40. S. Desagher, J. Glowinski, and J. Premont Pyruvate protects neurons against hydrogen peroxide-induced toxicity J. Neurosci. 17 1997 9060 9067 (Pubitemid 27498433)
41. Z.D. Zhou, and T.M. Lim Dopamine (DA) induced irreversible proteasome inhibition via DA derived quinones Free Radic. Res. 43 2009 417 430
42. Z.D. Zhou, S.Y. Kerk, G.G. Xiong, and T.M. Lim Dopamine auto-oxidation aggravates non-apoptotic cell death induced by over-expression of human A53T mutant alpha-synuclein in dopaminergic PC12 cells J. Neurochem. 108 2009 601 610
43. H. Jiang, Y. Ren, J. Zhao, and J. Feng Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis Hum. Mol. Genet. 13 2004 1745 1754 (Pubitemid 39173443)
44. M.B. Bagh, A.K. Maiti, S. Jana, K. Banerjee, A. Roy, and S. Chakrabarti Quinone and oxyradical scavenging properties of N-acetylcysteine prevent dopamine mediated inhibition of Na+, K+-ATPase and mitochondrial electron transport chain activity in rat brain: implications in the neuroprotective therapy of Parkinson's disease Free Radic. Res. 42 2008 574 581 (Pubitemid 351935150)
45. T. Kitada, A. Pisani, D.R. Porter, H. Yamaguchi, A. Tscherter, G. Martella, P. Bonsi, C. Zhang, E.N. Pothos, and J. Shen Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice Proc. Natl. Acad. Sci. USA 104 2007 11441 11446 (Pubitemid 47175159)
46. H. Zhou, B.H. Falkenburger, J.B. Schulz, K. Tieu, Z. Xu, and X.G. Xia Silencing of the Pink1 gene expression by conditional RNAi does not induce dopaminergic neuron death in mice Int. J. Biol. Sci. 3 2007 242 250 (Pubitemid 46425506)
47. H. Zhou, C. Huang, J. Tong, and X.G. Xia Early exposure to paraquat sensitizes dopaminergic neurons to subsequent silencing of PINK1 gene expression in mice Int. J. Biol. Sci. 7 2011 1180 1187
48. R. Lenartowski, and A. Goc Epigenetic, transcriptional and posttranscriptional regulation of the tyrosine hydroxylase gene Int. J. Dev. Neurosci. 29 2011 873 883
49. S.D. Reddy, S.K. Rayala, K. Ohshiro, S.B. Pakala, N. Kobori, P. Dash, S. Yun, J. Qin, B.W. O'Malley, and R. Kumar Multiple coregulatory control of tyrosine hydroxylase gene transcription Proc. Natl. Acad. Sci. USA 108 2011 4200 4205
50. L. Zecca, M.B. Youdim, P. Riederer, J.R. Connor, and R.R. Crichton Iron, brain ageing and neurodegenerative disorders Nat. Rev. Neurosci. 5 2004 863 873 (Pubitemid 39482155)
51. M. Takanashi, H. Mochizuki, K. Yokomizo, N. Hattori, H. Mori, Y. Yamamura, and Y. Mizuno Iron accumulation in the substantia nigra of autosomal recessive juvenile parkinsonism (ARJP) Parkinsonism Relat. Disord. 7 2001 311 314 (Pubitemid 32409973)
52. K.J. Schweitzer, T. Brussel, P. Leitner, R. Kruger, P. Bauer, D. Woitalla, J. Tomiuk, T. Gasser, and D. Berg Transcranial ultrasound in different monogenetic subtypes of Parkinson's disease J. Neurol. 254 2007 613 616 (Pubitemid 46781971)
53. M. Gerlach, D. Ben-Shachar, P. Riederer, and M.B. Youdim Altered brain metabolism of iron as a cause of neurodegenerative diseases? J. Neurochem. 63 1994 793 807 (Pubitemid 24266591)
54. G. Cohen Oxidative stress, mitochondrial respiration, and Parkinson's disease Ann. N. Y. Acad. Sci. 899 2000 112 120 (Pubitemid 30352780)
55. P. Jenner, and C.W. Olanow Understanding cell death in Parkinson's disease Ann. Neurol. 44 1998 S72 S84