Mitochondrial kinases in Parkinson's disease: Converging insights from neurotoxin and genetic models

Mitochondrion

Volumn 9, Issue 5, 2009, Pages 289-298

  Dagda, Ruben K ^a   Zhu, Jianhui ^a   Chu, Charleen T ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; Kinases; Mitochondria; Neurodegeneration; Oxidative stress; Parkinson's disease

Indexed keywords

MITOCHONDRIAL KINASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUROTOXIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE INDUCED KINASE 1; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN PINK1; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

AUTOPHAGY; CELL TRANSPORT; DEGENERATIVE DISEASE; DYNAMICS; ENZYME LOCALIZATION; ENZYME REGULATION; GENETIC MODEL; HUMAN; MITOCHONDRIAL RESPIRATION; NERVE CELL LESION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PARKINSONISM; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PARKINSON DISEASE; PHOSPHOTRANSFERASES; SIGNAL TRANSDUCTION;

PARKINSONIA;

EID: 70149084131     PISSN: 15677249     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mito.2009.06.001     Document Type: Review

References (183)

1. Alemi M., Prigione A., Wong A., Schoenfeld R., DiMauro S., Hirano M., Taroni F., and Cortopassi G. Mitochondrial DNA deletions inhibit proteasomal activity and stimulate an autophagic transcript. Free Radical Biol. Med. 42 (2007) 32-43
2. Alonso M., Melani M., Converso D., Jaitovich A., Paz C., Carreras M.C., Medina J.H., and Poderoso J.J. Mitochondrial extracellular signal-regulated kinases 1/2 (ERK1/2) are modulated during brain development. J. Neurochem. 89 (2004) 248-256
3. Alvarez-Tejado M., Naranjo-Suarez S., Jimenez C., Carrera A.C., Landazuri M.O., and del Peso L. Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells: protective role in apoptosis. J. Biol. Chem. 276 (2001) 22368-22374
4. Baines C.P., Zhang J., Wang G.W., Zheng Y.T., Xiu J.X., Cardwell E.M., Bolli R., and Ping P. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ. Res. 90 (2002) 390-397
5. Baloh R.H., Schmidt R.E., Pestronk A., and Milbrandt J. Altered axonal mitochondrial transport in the pathogenesis of Charcot-Marie-Tooth disease from mitofusin 2 mutations. J. Neurosci. 27 (2007) 422-430
6. Barksdale K.A., and Bijur G.N. The basal flux of Akt in the mitochondria is mediated by heat shock protein 90. J. Neurochem. (2009)
7. Beilina A., Van Der Brug M., Ahmad R., Kesavapany S., Miller D.W., Petsko G.A., and Cookson M.R. 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
8. Betarbet R., Sherer T.B., Di Monte D.A., and Greenamyre J.T. Mechanistic approaches to Parkinson's disease pathogenesis. Brain Pathol. 12 (2002) 499-510
9. Bijur G.N., and Jope R.S. Rapid accumulation of Akt in mitochondria following phosphatidylinositol 3-kinase activation. J. Neurochem. 87 (2003) 1427-1435
10. Biskup S., Moore D.J., Celsi F., Higashi S., West A.B., Andrabi S.A., Kurkinen K., Yu S.W., Savitt J.M., Waldvogel H.J., Faull R.L., Emson P.C., Torp R., Ottersen O.P., Dawson T.M., and Dawson V.L. Localization of LRRK2 to membranous and vesicular structures in mammalian brain. Ann. Neurol. 60 (2006) 557-569
11. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., and Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 28 (2008) 6926-6937
12. Bonifati V., Rizzu P., Squitieri F., Krieger E., Vanacore N., van Swieten J.C., Brice A., van Duijn C.M., Oostra B., Meco G., and Heutink P. DJ-1(PARK7), a novel gene for autosomal recessive, early onset parkinsonism. Neurol. Sci. 24 (2003) 159-160
13. Bonifati V., Rohe C.F., Breedveld G.J., Fabrizio E., De Mari M., Tassorelli C., Tavella A., Marconi R., Nicholl D.J., Chien H.F., Fincati E., Abbruzzese G., Marini P., De Gaetano A., Horstink M.W., Maat-Kievit J.A., Sampaio C., Antonini A., Stocchi F., Montagna P., Toni V., Guidi M., Dalla Libera A., Tinazzi M., De Pandis F., Fabbrini G., Goldwurm S., de Klein A., Barbosa E., Lopiano L., Martignoni E., Lamberti P., Vanacore N., Meco G., and Oostra B.A. Early-onset parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology 65 (2005) 87-95
14. Bonny C., Borsello T., and Zine A. Targeting the JNK pathway as a therapeutic protective strategy for nervous system diseases. Rev. Neurosci. 16 (2005) 57-67
15. Borsello T., and Forloni G. JNK signalling: a possible target to prevent neurodegeneration. Curr. Pharm Des. 13 (2007) 1875-1886
16. Brichese L., Cazettes G., and Valette A. JNK is associated with Bcl-2 and PP1 in mitochondria: paclitaxel induces its activation and its association with the phosphorylated form of Bcl-2. Cell Cycle 3 (2004) 1312-1319
17. Brill II L.B., and Bennett Jr. J.P. Dependence on electron transport chain function and intracellular signaling of genomic responses in SH-SY5Y cells to the mitochondrial neurotoxin MPP(+). Exp. Neurol. 181 (2003) 25-38
18. Butow R.A., and Avadhani N.G. Mitochondrial signaling: the retrograde response. Mol. Cell. 14 (2004) 1-15
19. Callio J., Oury T.D., and Chu C.T. Manganese superoxide dismutase protects against 6-hydroxydopamine injury in mouse brains. J. Biol. Chem. 280 (2005) 18536-18542
20. Cha G.H., Kim S., Park J., Lee E., Kim M., Lee S.B., Kim J.M., Chung J., and Cho K.S. Parkin negatively regulates JNK pathway in the dopaminergic neurons of Drosophila. Proc. Natl. Acad. Sci. USA 102 (2005) 10345-10350
21. Chalovich E.M., Zhu J.H., Caltagarone J., Bowser R., and Chu C.T. Functional repression of cAMP response element in 6-hydroxydopamine-treated neuronal cells. J. Biol. Chem. 281 (2006) 17870-17881
22. Chang D.T., Rintoul G.L., Pandipati S., and Reynolds I.J. Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol. Dis. 22 (2006) 388-400
23. Chauhan D., Li G., Hideshima T., Podar K., Mitsiades C., Mitsiades N., Munshi N., Kharbanda S., and Anderson K.C. JNK-dependent release of mitochondrial protein, Smac, during apoptosis in multiple myeloma (MM) cells. J. Biol. Chem. 278 (2003) 17593-17596
24. Chen J., Rusnak M., Luedtke R.R., and Sidhu A. D1 dopamine receptor mediates dopamine-induced cytotoxicity via the ERK signal cascade. J. Biol. Chem. 279 (2004) 39317-39330
25. Chen S., Zhang X., Yang D., Du Y., Li L., Li X., Ming M., and Le W. D2/D3 receptor agonist ropinirole protects dopaminergic cell line against rotenone-induced apoptosis through inhibition of caspase- and JNK-dependent pathways. FEBS Lett. 582 (2008) 603-610
26. Cherra III S.J., and Chu C.T. Autophagy in neuroprotection and neurodegeneration: a question of balance. Future Neurol. 3 (2008) 309-323
27. Cheung E.C., McBride H.M., and Slack R.S. Mitochondrial dynamics in the regulation of neuronal cell death. Apoptosis 12 (2007) 979-992
28. Choi W.S., Yoon S.Y., Oh T.H., Choi E.J., O'Malley K.L., and Oh Y.J. Two distinct mechanisms are involved in 6-hydroxydopamine- and MPP+-induced dopaminergic neuronal cell death: role of caspases, ROS, and JNK. J. Neurosci. Res. 57 (1999) 86-94
29. Chu C.T., Levinthal D.J., Kulich S.M., Chalovich E.M., and DeFranco D.B. Oxidative neuronal injury. The dark side of ERK1/2. Eur. J. Biochem. 271 (2004) 2060-2066
30. Chu C.T., Zhu J.H., Cao G., Signore A., Wang S., and Chen J. Apoptosis inducing factor mediates caspase-independent 1-methyl-4-phenylpyridinium toxicity in dopaminergic cells. J. Neurochem. 94 (2005) 1685-1695
31. Chu C.T., Plowey E.D., Wang Y., Patel V., and Jordan-Sciutto K.L. Location, location, location: altered transcription factor trafficking in neurodegeneration. J. Neuropathol. Exp. Neurol. 66 (2007) 873-883
32. Chu C.T., Plowey E.D., Dagda R.K., Hickey R.W., Cherra III S.J., and Clark R.S. Autophagy in neurite injury and neurodegeneration: in vitro and in vivo models. Method Enzymol. 453 (2009) 217-249
33. Chuenkova M.V., and Pereira M.A. PDNF, a human parasite-derived mimic of neurotrophic factors, prevents caspase activation, free radical formation, and death of dopaminergic cells exposed to the parkinsonism-inducing neurotoxin MPP+. Brain Res. Mol. Brain Res. 119 (2003) 50-61
34. Clark I.E., Dodson M.W., Jiang C., Cao J.H., Huh J.R., Seol J.H., Yoo S.J., Hay B.A., and Guo M. Drosophila pink1 is required for mitochondrial function and interacts genetically with Parkin. Nature 441 (2006) 1162-1166
35. Colucci-D'Amato L., Perrone-Capano C., and di Porzio U. Chronic activation of ERK and neurodegenerative diseases. Bioessays 25 (2003) 1085-1095
36. Cribbs J.T., and Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 8 (2007) 939-944
37. Cuervo A.M., Stefanis L., Fredenburg R., Lansbury P.T., and Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 305 (2004) 1292-1295
38. Dagda R.K., Zhu J., Kulich S.M., and Chu C.T. Mitochondrially localized ERK2 regulates mitophagy and autophagic cell stress. Autophagy 4 (2008) 770-782
39. Dagda R.K., Cherra III S.J., Kulich S.M., Tandon A., Park D., and Chu C.T. Loss of pink1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 3 (2009) 5-7
40. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., and Greenberg M.E. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91 (1997) 231-241
41. Dawson T.M., and Dawson V.L. Molecular pathways of neurodegeneration in Parkinson's disease. Science 302 (2003) 819-822
42. Dawson V.L., and Dawson T.M. Deadly conversations: nuclear-mitochondrial cross-talk. J. Bioenerg. Biomembr. 36 (2004) 287-294
43. Dekker M.C., Bonifati V., and van Duijn C.M. Parkinson's disease: piecing together a genetic jigsaw. Brain 126 (2003) 1722-1733
44. del Peso L., Gonzalez-Garcia M., Page C., Herrera R., and Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278 (1997) 687-689
45. Deng H., Jankovic J., Guo Y., Xie W., and Le W. Small interfering RNA targeting the PINK1 induces apoptosis in dopaminergic cells SH-SY5Y. Biochem. Biophys. Res. Commun. 337 (2005) 1133-1138
46. Devi L., Raghavendran V., Prabhu B.M., Avadhani N.G., and Anandatheerthavarada H.K. Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem. 283 (2008) 9089-9100
47. Dougherty C.J., Kubasiak L.A., Frazier D.P., Li H., Xiong W.C., Bishopric N.H., and Webster K.A. Mitochondrial signals initiate the activation of c-Jun N-terminal kinase (JNK) by hypoxia-reoxygenation. Faseb J. 18 (2004) 1060-1070
48. Eminel S., Klettner A., Roemer L., Herdegen T., and Waetzig V. JNK2 translocates to the mitochondria and mediates cytochrome c release in PC12 cells in response to 6-hydroxydopamine. J. Biol. Chem. 279 (2004) 55385-55392
49. Exner N., Treske B., Paquet D., Holmstrom K., Schiesling C., Gispert S., Carballo-Carbajal I., Berg D., Hoepken H.H., Gasser T., Kruger R., Winklhofer K.F., Vogel F., Reichert A.S., Auburger G., Kahle P.J., Schmid B., and Haass C. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by Parkin. J. Neurosci. 27 (2007) 12413-12418
50. Feliciello A., Gottesman M.E., and Avvedimento E.V. cAMP-PKA signaling to the mitochondria: protein scaffolds, mRNA and phosphatases. Cell. Signal. 17 (2005) 279-287
51. Gandhi S., Muqit M.M., Stanyer L., Healy D.G., Abou-Sleiman P.M., Hargreaves I., Heales S., Ganguly M., Parsons L., Lees A.J., Latchman D.S., Holton J.L., Wood N.W., and Revesz T. PINK1 protein in normal human brain and Parkinson's disease. Brain 129 (2006) 1720-1731
52. Gautier C.A., Kitada T., and Shen J. Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl. Acad. Sci. USA 105 (2008) 11364-11369
53. Gazaryan I.G., and Brown A.M. Intersection between mitochondrial permeability pores and mitochondrial fusion/fission. Neurochem. Res. 32 (2007) 917-929
54. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., and Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science 290 (2000) 985-989
55. Gloeckner C.J., Schumacher A., Boldt K., and Ueffing M. The Parkinson disease-associated protein kinase LRRK2 exhibits MAPKKK activity and phosphorylates MKK3/6 and MKK4/7, in vitro. J. Neurochem. (2009)
56. Glotin A.L., Calipel A., Brossas J.Y., Faussat A.M., Treton J., and Mascarelli F. Sustained versus transient ERK1/2 signaling underlies the anti- and proapoptotic effects of oxidative stress in human RPE cells. Invest Ophthalmol. Vis. Sci. 47 (2006) 4614-4623
57. Gomes L.C., and Scorrano L. High levels of Fis1, a pro-fission mitochondrial protein, trigger autophagy. Biochim. Biophys. Acta 1777 (2008) 860-866
58. Gomez-Lazaro M., Bonekamp N.A., Galindo M.F., Jordan J., and Schrader M. 6-Hydroxydopamine (6-OHDA) induces Drp1-dependent mitochondrial fragmentation in SH-SY5Y cells. Free Radical Biol. Med. 44 (2008) 1960-1969
59. Gomez-Santos C., Ferrer I., Reiriz J., Vinals F., Barrachina M., and Ambrosio S. MPP+ increases alpha-synuclein expression and ERK/MAP-kinase phosphorylation in human neuroblastoma SH-SY5Y cells. Brain Res. 935 (2002) 32-39
60. Greggio E., Jain S., Kingsbury A., Bandopadhyay R., Lewis P., Kaganovich A., van der Brug M.P., Beilina A., Blackinton J., Thomas K.J., Ahmad R., Miller D.W., Kesavapany S., Singleton A., Lees A., Harvey R.J., Harvey K., and Cookson M.R. Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol. Dis. 23 (2006) 329-341
61. Gu G., Reyes P.E., Golden G.T., Woltjer R.L., Hulette C., Montine T.J., and Zhang J. Mitochondrial DNA deletions/rearrangements in Parkinson disease and related neurodegenerative disorders. J. Neuropathol. Exp. Neurol. 61 (2002) 634-639
62. Hanawa N., Shinohara M., Saberi B., Gaarde W.A., Han D., and Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J. Biol. Chem. 283 (2008) 13565-13577
63. Haque M.E., Thomas K.J., D'Souza C., Callaghan S., Kitada T., Slack R.S., Fraser P., Cookson M.R., Tandon A., and Park D.S. Cytoplasmic Pink1 activity protects neurons from dopaminergic neurotoxin MPTP. Proc. Natl. Acad. Sci. USA 105 (2008) 1716-1721
64. Hara H., Ohta M., Ohta K., Kuno S., and Adachi T. Increase of antioxidative potential by tert-butylhydroquinone protects against cell death associated with 6-hydroxydopamine-induced oxidative stress in neuroblastoma SH-SY5Y cells. Brain Res. Mol. Brain Res. 119 (2003) 125-131
65. Hashimoto M., Rockenstein E., Mante M., Mallory M., and Masliah E. Beta-synuclein inhibits alpha-synuclein aggregation: a possible role as an anti-parkinsonian factor. Neuron 32 (2001) 213-223
66. Hashimoto M., Bar-On P., Ho G., Takenouchi T., Rockenstein E., Crews L., and Masliah E. Beta-synuclein regulates Akt activity in neuronal cells. A possible mechanism for neuroprotection in Parkinson's disease. J. Biol. Chem. 279 (2004) 23622-23629
67. Horbinski C., and Chu C.T. Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radical Biol. Med. 38 (2005) 2-11
68. Hunot S., Vila M., Teismann P., Davis R.J., Hirsch E.C., Przedborski S., Rakic P., and Flavell R.A. JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 101 (2004) 665-670
69. Jiang H., Ren Y., Zhao J., and Feng J. Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum. Mol. Genet. 13 (2004) 1745-1754
70. Kachergus J., Mata I.F., Hulihan M., Taylor J.P., Lincoln S., Aasly J., Gibson J.M., Ross O.A., Lynch T., Wiley J., Payami H., Nutt J., Maraganore D.M., Czyzewski K., Styczynska M., Wszolek Z.K., Farrer M.J., and Toft M. Identification of a novel LRRK2 mutation linked to autosomal dominant parkinsonism: evidence of a common founder across European populations. Am. J. Hum. Genet. 76 (2005) 672-680
71. Karbowski M., and Youle R.J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 10 (2003) 870-880
72. Kharbanda S., Saxena S., Yoshida K., Pandey P., Kaneki M., Wang Q., Cheng K., Chen Y.N., Campbell A., Sudha T., Yuan Z.M., Narula J., Weichselbaum R., Nalin C., and Kufe D. Translocation of SAPK/JNK to mitochondria and interaction with Bcl-x(L) in response to DNA damage. J. Biol. Chem. 275 (2000) 322-327
73. Kim S.Y., Kim M.Y., Mo J.S., Park J.W., and Park H.S. SAG protects human neuroblastoma SH-SY5Y cells against 1-methyl-4-phenylpyridinium ion (MPP+)-induced cytotoxicity via the downregulation of ROS generation and JNK signaling. Neurosci. Lett. 413 (2007) 132-136
74. Kiselyov K., Jennigs Jr. J.J., Rbaibi Y., and Chu C.T. Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 3 (2007) 259-262
75. Kitada T., Asakawa S., Matsumine H., Hattori N., Minoshima S., Shimizu N., and Mizuno Y. Positional cloning of the autosomal recessive juvenile parkinsonism (AR-JP) gene and its diversity in deletion mutations. Parkinsonism Relat. Disord. 5 (1999) 163-168
76. Kitada T., Pisani A., Porter D.R., Yamaguchi H., Tscherter A., Martella G., Bonsi P., Zhang C., Pothos E.N., and Shen J. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc. Natl. Acad. Sci. USA 104 (2007) 11441-11446
77. Klintworth H., Newhouse K., Li T., Choi W.S., Faigle R., and Xia Z. Activation of c-Jun N-terminal protein kinase is a common mechanism underlying paraquat- and rotenone-induced dopaminergic cell apoptosis. Toxicol. Sci. 97 (2007) 149-162
78. Klivenyi P., St Clair D., Wermer M., Yen H.C., Oberley T., Yang L., and Flint Beal M. Manganese superoxide dismutase overexpression attenuates MPTP toxicity. Neurobiol. Dis. 5 (1998) 253-258
79. Kuan C.Y., and Burke R.E. Targeting the JNK signaling pathway for stroke and Parkinson's diseases therapy. Curr. Drug Targets 4 (2005) 63-67
80. Kulich S.M., and Chu C.T. Sustained extracellular signal-regulated kinase activation by 6-hydroxydopamine: implications for Parkinson's disease. J. Neurochem. 77 (2001) 1058-1066
81. Kulich S.M., Horbinski C., Patel M., and Chu C.T. 6-Hydroxydopamine induces mitochondrial ERK activation. Free Radical Biol. Med. 43 (2007) 372-383
82. Kumazawa R., Tomiyama H., Li Y., Imamichi Y., Funayama M., Yoshino H., Yokochi F., Fukusako T., Takehisa Y., Kashihara K., Kondo T., Elibol B., Bostantjopoulou S., Toda T., Takahashi H., Yoshii F., Mizuno Y., and Hattori N. Mutation analysis of the PINK1 gene in 391 patients with Parkinson disease. Arch. Neurol. 65 (2008) 802-808
83. Leeds P., Leng Y., Chalecka-Franaszek E., and Chuang D.M. Neurotrophins protect against cytosine arabinoside-induced apoptosis of immature rat cerebellar neurons. Neurochem. Int. 46 (2005) 61-72
84. Li Z., Okamoto K., Hayashi Y., and Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119 (2004) 873-887
85. Li Z., Hu Y., Zhu Q., and Zhu J. Neurotrophin-3 reduces apoptosis induced by 6-OHDA in PC12 cells through Akt signaling pathway. Int. J. Dev. Neurosci. 26 (2008) 635-640
86. Liang C.L., Wang T.T., Luby-Phelps K., and German D.C. Mitochondria mass is low in mouse substantia nigra dopamine neurons: implications for Parkinson's disease. Exp. Neurol. 203 (2007) 370-380
87. Lin E., Cavanaugh J.E., Leak R.K., Perez R.G., and Zigmond M.J. Rapid activation of ERK by 6-hydroxydopamine promotes survival of dopaminergic cells. J. Neurosci. Res. 86 (2008) 108-117
88. Lin W., and Kang U.J. Characterization of PINK1 processing, stability, and subcellular localization. J. Neurochem. 106 (2008) 464-474
89. Liou A.K., Leak R.K., Li L., and Zigmond M.J. Wild-type LRRK2 but not its mutant attenuates stress-induced cell death via ERK pathway. Neurobiol. Dis. 32 (2008) 116-124
90. Liu M., Aneja R., Sun X., Xie S., Wang H., Wu X., Dong J.T., Li M., Joshi H.C., and Zhou J. Parkin regulates Eg5 expression by Hsp70 ubiquitination-dependent inactivation of the c-Jun NH2-terminal kinase. J. Biol. Chem. (2008)
91. Mandemakers W., Morais V.A., and De Strooper B. A cell biological perspective on mitochondrial dysfunction in Parkinson disease and other neurodegenerative diseases. J. Cell. Sci. 120 (2007) 1707-1716
92. Marongiu R., Ferraris A., Ialongo T., Michiorri S., Soleti F., Ferrari F., Elia A.E., Ghezzi D., Albanese A., Altavista M.C., Antonini A., Barone P., Brusa L., Cortelli P., Martinelli P., Pellecchia M.T., Pezzoli G., Scaglione C., Stanzione P., Tinazzi M., Zecchinelli A., Zeviani M., Cassetta E., Garavaglia B., Dallapiccola B., Bentivoglio A.R., and Valente E.M. PINK1 heterozygous rare variants: prevalence, significance and phenotypic spectrum. Hum. Mutat. 29 (2008) 565
93. Martella G., Platania P., Vita D., Sciamanna G., Cuomo D., Tassone A., Tscherter A., Kitada T., Bonsi P., Shen J., and Pisani A. Enhanced sensitivity to group II mGlu receptor activation at corticostriatal synapses in mice lacking the familial parkinsonism-linked genes PINK1 or Parkin. Exp. Neurol. 215 (2009) 388-396
94. Martinez-Vicente M., Talloczy Z., Kaushik S., Massey A.C., Mazzulli J., Mosharov E.V., Hodara R., Fredenburg R., Wu D.C., Follenzi A., Dauer W., Przedborski S., Ischiropoulos H., Lansbury P.T., Sulzer D., and Cuervo A.M. Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J. Clin. Invest. 118 (2008) 777-788
95. McBride H.M., Neuspiel M., and Wasiak S. Mitochondria: more than just a powerhouse. Curr. Biol. 16 (2006) R551-560
96. Mills R.D., Sim C.H., Mok S.S., Mulhern T.D., Culvenor J.G., and Cheng H.C. Biochemical aspects of the neuroprotective mechanism of PTEN-induced kinase-1 (PINK1). J. Neurochem. 105 (2008) 18-33
97. Mizushima N., Ohsumi Y., and Yoshimori T. Autophagosome formation in mammalian cells. Cell Struct. Funct. 27 (2002) 421-429
98. Monick M.M., Powers L.S., Barrett C.W., Hinde S., Ashare A., Groskreutz D.J., Nyunoya T., Coleman M., Spitz D.R., and Hunninghake G.W. Constitutive ERK MAPK activity regulates macrophage ATP production and mitochondrial integrity. J. Immunol. 180 (2008) 7485-7496
99. Mookherjee P., Quintanilla R., Roh M.S., Zmijewska A.A., Jope R.S., and Johnson G.V. Mitochondrial-targeted active Akt protects SH-SY5Y neuroblastoma cells from staurosporine-induced apoptotic cell death. J. Cell. Biochem. 102 (2007) 196-210
100. Moreira P.I., Siedlak S.L., Wang X., Santos M.S., Oliveira C.R., Tabaton M., Nunomura A., Szweda L.I., Aliev G., Smith M.A., Zhu X., and Perry G. Autophagocytosis of mitochondria is prominent in Alzheimer disease. J. Neuropathol. Exp. Neurol. 66 (2007) 525-532
101. Moriwaki Y., Kim Y.J., Ido Y., Misawa H., Kawashima K., Endo S., and Takahashi R. L347P PINK1 mutant that fails to bind to Hsp90/Cdc37 chaperones is rapidly degraded in a proteasome-dependent manner. Neurosci. Res. 61 (2008) 43-48
102. Munch G., Luth H.J., Wong A., Arendt T., Hirsch E., Ravid R., and Riederer P. Crosslinking of alpha-synuclein by advanced glycation endproducts - an early pathophysiological step in Lewy body formation?. J. Chem. Neuroanat. 20 (2000) 253-257
103. Nair V.D. Activation of p53 signaling initiates apoptotic death in a cellular model of Parkinson's disease. Apoptosis 11 (2006) 955-966
104. Namikawa K., Honma M., Abe K., Takeda M., Mansur K., Obata T., Miwa A., Okado H., and Kiyama H. Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J. Neurosci. 20 (2000) 2875-2886
105. Namura S., Iihara K., Takami S., Nagata I., Kikuchi H., Matsushita K., Moskowitz M.A., Bonventre J.V., and Alessandrini A. Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia. Proc. Natl. Acad. Sci. USA 98 (2001) 11569-11574
106. Narendra D., Tanaka A., Suen D.F., and Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 183 (2008) 795-803
107. Newhouse K., Hsuan S.L., Chang S.H., Cai B., Wang Y., and Xia Z. Rotenone-induced apoptosis is mediated by p38 and JNK MAP kinases in human dopaminergic SH-SY5Y cells. Toxicol. Sci. 79 (2004) 137-146
108. Nixon R.A., Wegiel J., Kumar A., Yu W.H., Peterhoff C., Cataldo A., and Cuervo A.M. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64 (2005) 113-122
109. Nowak G., Clifton G.L., Godwin M.L., and Bakajsova D. Activation of ERK1/2 pathway mediates oxidant-induced decreases in mitochondrial function in renal cells. Am. J. Physiol. Renal Physiol. 291 (2006) F840-855
110. Orr A.L., Li S., Wang C.E., Li H., Wang J., Rong J., Xu X., Mastroberardino P.G., Greenamyre J.T., and Li X.J. N-terminal mutant huntingtin associates with mitochondria and impairs mitochondrial trafficking. J. Neurosci. 28 (2008) 2783-2792
111. Pagliarini D.J., and Dixon J.E. Mitochondrial modulation: reversible phosphorylation takes center stage?. Trends Biochem. Sci. 31 (2006) 26-34
112. Pan J., Zhao Y.X., Wang Z.Q., Jin L., Sun Z.K., and Chen S.D. Expression of FasL and its interaction with Fas are mediated by c-Jun N-terminal kinase (JNK) pathway in 6-OHDA-induced rat model of Parkinson disease. Neurosci. Lett. 428 (2007) 82-87
113. Park J., Lee S.B., Lee S., Kim Y., Song S., Kim S., Bae E., Kim J., Shong M., Kim J.M., and Chung J. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by Parkin. Nature 441 (2006) 1157-1161
114. Park S.W., Kim S.H., Park K.H., Kim S.D., Kim J.Y., Baek S.Y., Chung B.S., and Kang C.D. Preventive effect of antioxidants in MPTP-induced mouse model of Parkinson's disease. Neurosci. Lett. 363 (2004) 243-246
115. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., and Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122 (2005) 927-939
116. Petit A., Kawarai T., Paitel E., Sanjo N., Maj M., Scheid M., Chen F., Gu Y., Hasegawa H., Salehi-Rad S., Wang L., Rogaeva E., Fraser P., Robinson B., St George-Hyslop P., and Tandon A. Wild-type PINK1 prevents basal and induced neuronal apoptosis, a protective effect abrogated by Parkinson disease-related mutations. J. Biol. Chem. 280 (2005) 34025-34032
117. Plowey E.D., Cherra III S.J., Liu Y.J., and Chu C.T. Role of autophagy in G2019S-LRRK2-associated neurite shortening in differentiated SH-SY5Y cells. J. Neurochem. 105 (2008) 1048-1056
118. Plun-Favreau H., Klupsch K., Moisoi N., Gandhi S., Kjaer S., Frith D., Harvey K., Deas E., Harvey R.J., McDonald N., Wood N.W., Martins L.M., and Downward J. The mitochondrial protease HtrA2 is regulated by Parkinson's disease-associated kinase PINK1. Nat. Cell Biol. 9 (2007) 1243-1252
119. Poderoso C., Converso D.P., Maloberti P., Duarte A., Neuman I., Galli S., Maciel F.C., Paz C., Carreras M.C., Poderoso J.J., and Podesta E.J. A mitochondrial kinase complex is essential to mediate an ERK1/2-dependent phosphorylation of a key regulatory protein in steroid biosynthesis. PLoS ONE 3 (2008) e1443
120. Polymeropoulos M.H., Lavedan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., and Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
121. Poole A.C., Thomas R.E., Andrews L.A., McBride H.M., Whitworth A.J., and Pallanck L.J. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. USA 105 (2008) 1638-1643
122. Pridgeon J.W., Olzmann J.A., Chin L.S., and Li L. PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol. 5 (2007) e172
123. Przedborski S., and Jackson-Lewis V. Mechanisms of MPTP toxicity. Mov. Disord. 13 Suppl. 1 (1998) 35-38
124. Ramirez A., Heimbach A., Grundemann J., Stiller B., Hampshire D., Cid L.P., Goebel I., Mubaidin A.F., Wriekat A.L., Roeper J., Al-Din A., Hillmer A.M., Karsak M., Liss B., Woods C.G., Behrens M.I., and Kubisch C. Hereditary parkinsonism with dementia is caused by mutations in ATP13A2, encoding a lysosomal type 5 P-type ATPase. Nat. Genet. 38 (2006) 1184-1191
125. Reetz K., Lencer R., Steinlechner S., Gaser C., Hagenah J., Buchel C., Petersen D., Kock N., Djarmati A., Siebner H.R., Klein C., and Binkofski F. Limbic and frontal cortical degeneration is associated with psychiatric symptoms in PINK1 mutation carriers. Biol. Psychiat. 64 (2008) 241-247
126. Ren Y., Jiang H., Yang F., Nakaso K., and Feng J. Parkin protects dopaminergic neurons against microtubule-depolymerizing toxins by attenuating microtubule-associated protein kinase activation. J. Biol. Chem. 284 (2009) 4009-4017
127. Ries V., Henchcliffe C., Kareva T., Rzhetskaya M., Bland R., During M.J., Kholodilov N., and Burke R.E. Oncoprotein Akt/PKB induces trophic effects in murine models of Parkinson's disease. Proc. Natl. Acad. Sci. USA 103 (2006) 18757-18762
128. Ross O.A., and Farrer M.J. Pathophysiology, pleiotrophy and paradigm shifts: genetic lessons from Parkinson's disease. Biochem. Soc. Trans. 33 (2005) 586-590
129. Rubinsztein D.C., DiFiglia M., Heintz N., Nixon R.A., Qin Z.-H., Ravikumar B., Stefanis L., and Tolkovsky A. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy 1 (2005) 11-22
130. Rumora L., Lovric J., Sairam M.R., and Maysinger D. Impairments of heat shock protein expression and MAPK translocation in the central nervous system of follitropin receptor knockout mice. Exp. Gerontol. 42 (2007) 619-628
131. Ryu E.J., Harding H.P., Angelastro J.M., Vitolo O.V., Ron D., and Greene L.A. Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22 (2002) 10690-10698
132. Saporito M.S., Brown E.M., Miller M.S., and Carswell S. CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons In vivo. J. Pharmacol. Exp. Ther. 288 (1999) 421-427
133. Schapira A.H., Cooper J.M., Dexter D., Clark J.B., Jenner P., and Marsden C.D. Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54 (1990) 823-827
134. Seo J.H., Rah J.C., Choi S.H., Shin J.K., Min K., Kim H.S., Park C.H., Kim S., Kim E.M., Lee S.H., Lee S., Suh S.W., and Suh Y.H. Alpha-synuclein regulates neuronal survival via Bcl-2 family expression and PI3/Akt kinase pathway. Faseb J. 16 (2002) 1826-1828
135. Sherer T.B., Betarbet R., Stout A.K., Lund S., Baptista M., Panov A.V., Cookson M.R., and Greenamyre J.T. An in vitro model of Parkinson's disease: linking mitochondrial impairment to altered alpha-synuclein metabolism and oxidative damage. J. Neurosci. 22 (2002) 7006-7015
136. Silvestri L., Caputo V., Bellacchio E., Atorino L., Dallapiccola B., Valente E.M., and Casari G. Mitochondrial import and enzymatic activity of PINK1 mutants associated to recessive parkinsonism. Hum. Mol. Genet. 14 (2005) 3477-3492
137. Simon D.K., Lin M.T., Zheng L., Liu G.J., Ahn C.H., Kim L.M., Mauck W.M., Twu F., Beal M.F., and Johns D.R. Somatic mitochondrial DNA mutations in cortex and substantia nigra in aging and Parkinson's disease. Neurobiol. Aging 25 (2004) 71-81
138. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M.R., Muenter M., Baptista M., Miller D., Blancato J., Hardy J., and Gwinn-Hardy K. Alpha-synuclein locus triplication causes Parkinson's disease. Science 302 (2003) 841
139. Steinlechner S., Stahlberg J., Volkel B., Djarmati A., Hagenah J., Hiller A., Hedrich K., Konig I., Klein C., and Lencer R. Co-occurrence of affective and schizophrenia spectrum disorders with PINK1 mutations. J. Neurol. Neurosurg. Psychiat. 78 (2007) 532-535
140. Subramaniam S., and Unsicker K. Extracellular signal-regulated kinase as an inducer of non-apoptotic neuronal death. Neuroscience 138 (2006) 1055-1065
141. Swerdlow R.H., Parks J.K., Miller S.W., Tuttle J.B., Trimmer P.A., Sheehan J.P., Bennett Jr. J.P., Davis R.E., and Parker Jr. W.D. Origin and functional consequences of the complex I defect in Parkinson's disease. Ann. Neurol. 40 (1996) 663-671
142. 2+-mediated apoptosis. Mol. Cell 16 (2004) 59-68
143. Teismann P., Tieu K., Choi D.K., Wu D.C., Naini A., Hunot S., Vila M., Jackson-Lewis V., and Przedborski S. Cyclooxygenase-2 is instrumental in Parkinson's disease neurodegeneration. Proc. Natl. Acad. Sci. USA 100 (2003) 5473-5478
144. Tian L.L., Zhou Z., Zhang Q., Sun Y.N., Li C.R., Cheng C.H., Zhong Z.Y., and Wang S.Q. Protective effect of (+/-) isoborneol against 6-OHDA-induced apoptosis in SH-SY5Y cells. Cell Physiol. Biochem. 20 (2007) 1019-1032
145. Tomaska L. Mitochondrial protein phosphorylation: lessons from yeasts. Gene 255 (2000) 59-64
146. Trimmer P.A., Smith T.S., Jung A.B., and Bennett Jr. J.P. Dopamine neurons from transgenic mice with a knockout of the p53 gene resist MPTP neurotoxicity. Neurodegeneration 5 (1996) 233-239
147. Trimmer P.A., Swerdlow R.H., Parks J.K., Keeney P., Bennett Jr. J.P., Miller S.W., Davis R.E., and Parker Jr. W.D. Abnormal mitochondrial morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp. Neurol. 162 (2000) 37-50
148. Twig G., Elorza A., Molina A.J., Mohamed H., Wikstrom J.D., Walzer G., Stiles L., Haigh S.E., Katz S., Las G., Alroy J., Wu M., Py B.F., Yuan J., Deeney J.T., Corkey B.E., and Shirihai O.S. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. Embo J. 27 (2008) 433-446
149. Uversky V.N., Li J., Souillac P., Millett I.S., Doniach S., Jakes R., Goedert M., and Fink A.L. Biophysical properties of the synucleins and their propensities to fibrillate: inhibition of alpha-synuclein assembly by beta- and gamma-synucleins. J. Biol. Chem. 277 (2002) 11970-11978
150. Valente E.M., Abou-Sleiman P.M., Caputo V., Muqit M.M., Harvey K., Gispert S., Ali Z., Del Turco D., Bentivoglio A.R., Healy D.G., Albanese A., Nussbaum R., Gonzalez-Maldonado R., Deller T., Salvi S., Cortelli P., Gilks W.P., Latchman D.S., Harvey R.J., Dallapiccola B., Auburger G., and Wood N.W. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 304 (2004) 1158-1160
151. Valente E.M., Salvi S., Ialongo T., Marongiu R., Elia A.E., Caputo V., Romito L., Albanese A., Dallapiccola B., and Bentivoglio A.R. PINK1 mutations are associated with sporadic early-onset parkinsonism. Ann. Neurol. 56 (2004) 336-341
152. Verstreken P., Ly C.V., Venken K.J., Koh T.W., Zhou Y., and Bellen H.J. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47 (2005) 365-378
153. Wang D., Qian L., Xiong H., Liu J., Neckameyer W.S., Oldham S., Xia K., Wang J., Bodmer R., and Zhang Z. Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proc. Natl. Acad. Sci. USA 103 (2006) 13520-13525
154. Wang H.L., Chou A.H., Yeh T.H., Li A.H., Chen Y.L., Kuo Y.L., Tsai S.R., and Yu S.T. PINK1 mutants associated with recessive Parkinson's disease are defective in inhibiting mitochondrial release of cytochrome c. Neurobiol. Dis. 28 (2007) 216-226
155. 2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 136 (2009) 163-174
156. Wasiak S., Zunino R., and McBride H.M. Bax/Bak promote sumoylation of DRP1 and its stable association with mitochondria during apoptotic cell death. J. Cell Biol. 177 (2007) 439-450
157. Weihofen, A., Thomas, K.J., Ostaszewski, B., Cookson, M., Selkoe, D.J., 2009. Pink1 forms a multi-protein complex with Miro and Milton, linking Pink1 function to mitochondrial trafficking. Biochemistry.
158. Weng Z., Signore A.P., Gao Y., Wang S., Zhang F., Hastings T., Yin X.M., and Chen J. Leptin protects against 6-hydroxydopamine-induced dopaminergic cell death via mitogen-activated protein kinase signaling. J. Biol. Chem. 282 (2007) 34479-34491
159. West A.B., Moore D.J., Biskup S., Bugayenko A., Smith W.W., Ross C.A., Dawson V.L., and Dawson T.M. Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc. Natl. Acad. Sci. USA 102 (2005) 16842-16847
160. White L.R., Toft M., Kvam S.N., Farrer M.J., and Aasly J.O. MAPK-pathway activity, LRRK2 G2019S, and Parkinson's disease. J. Neurosci. Res. 85 (2007) 1288-1294
161. Wood-Kaczmar A., Gandhi S., Yao Z., Abramov A.S., Miljan E.A., Keen G., Stanyer L., Hargreaves I., Klupsch K., Deas E., Downward J., Mansfield L., Jat P., Taylor J., Heales S., Duchen M.R., Latchman D., Tabrizi S.J., and Wood N.W. PINK1 is necessary for long term survival and mitochondrial function in human dopaminergic neurons. PLoS ONE 3 (2008) e2455
162. Xia X.G., Harding T., Weller M., Bieneman A., Uney J.B., and Schulz J.B. Gene transfer of the JNK interacting protein-1 protects dopaminergic neurons in the MPTP model of Parkinson's disease. Proc. Natl. Acad. Sci. USA 98 (2001) 10433-10438
163. Xiromerisiou G., Hadjigeorgiou G.M., Papadimitriou A., Katsarogiannis E., Gourbali V., and Singleton A.B. Association between AKT1 gene and Parkinson's disease: a protective haplotype. Neurosci. Lett. 436 (2008) 232-234
164. Yang Y., Gehrke S., Haque M.E., Imai Y., Kosek J., Yang L., Beal M.F., Nishimura I., Wakamatsu K., Ito S., Takahashi R., and Lu B. Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl. Acad. Sci. USA 102 (2005) 13670-13675
165. Yang Y., Gehrke S., Imai Y., Huang Z., Ouyang Y., Wang J.W., Yang L., Beal M.F., Vogel H., and Lu B. 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
166. Yang Y., Ouyang Y., Yang L., Beal M.F., McQuibban A., Vogel H., and Lu B. Pink1 regulates mitochondrial dynamics through interaction with the fission/fusion machinery. Proc. Natl. Acad. Sci. USA 105 (2008) 7070-7075
167. Yang Y.X., Wood N.W., and Latchman D.S. Molecular basis of Parkinson's disease. Neuroreport 20 (2009) 150-156
168. Yoon S., and Seger R. The extracellular signal-regulated kinase: multiple substrates regulate diverse cellular functions. Growth Factors 24 (2006) 21-44
169. Youle R.J., and Karbowski M. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6 (2005) 657-663
170. Yuan H., Gerencser A.A., Liot G., Lipton S.A., Ellisman M., Perkins G.A., and Bossy-Wetzel E. Mitochondrial fission is an upstream and required event for bax foci formation in response to nitric oxide in cortical neurons. Cell Death Differ. 14 (2007) 462-471
171. Zablocka B., Dluzniewska J., Zajac H., and Domanska-Janik K. Opposite reaction of ERK and JNK in ischemia vulnerable and resistant regions of hippocampus: involvement of mitochondria. Brain Res. Mol. Brain Res. 110 (2003) 245-252
172. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., and Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 154 (1999) 1423-1429
173. Zhang Y., Qi H., Taylor R., Xu W., Liu L.F., and Jin S. The role of autophagy in mitochondria maintenance. characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 3 (2007) 337-346
174. Zhong J., Deng J., Phan J., Dlouhy S., Wu H., Yao W., Ye P., D'Ercole A.J., and Lee W.H. Insulin-like growth factor-I protects granule neurons from apoptosis and improves ataxia in weaver mice. J. Neurosci. Res. 80 (2005) 481-490
175. Zhou C., Huang Y., Shao Y., May J., Prou D., Perier C., Dauer W., Schon E.A., and Przedborski S. The kinase domain of mitochondrial PINK1 faces the cytoplasm. Proc. Natl. Acad. Sci. USA 105 (2008) 12022-12027
176. Zhou H., Falkenburger B.H., Schulz J.B., Tieu K., Xu Z., and Xia X.G. 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
177. Zhou Q., Lam P.Y., Han D., and Cadenas E. C-Jun N-terminal kinase regulates mitochondrial bioenergetics by modulating pyruvate dehydrogenase activity in primary cortical neurons. J. Neurochem. 104 (2008) 325-335
178. Zhu J.H., Kulich S.M., Oury T.D., and Chu C.T. Cytoplasmic aggregates of phosphorylated extracellular signal-regulated protein kinases in Lewy body diseases. Am. J. Pathol. 161 (2002) 2087-2098
179. Zhu J.H., Guo F., Shelburne J., Watkins S., and Chu C.T. Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases. Brain Pathol. 13 (2003) 473-481
180. Zhu J.H., Horbinski C., Guo F., Watkins S., Uchiyama Y., and Chu C.T. Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am. J. Pathol. 170 (2007) 75-86
181. Zhuang S., and Schnellmann R.G. A death-promoting role for extracellular signal-regulated kinase. J. Pharmacol. Exp. Ther. 319 (2006) 991-997
182. Zhuang S., Kinsey G.R., Yan Y., Han J., and Schnellmann R.G. Extracellular signal-regulated kinase activation mediates mitochondrial dysfunction and necrosis induced by hydrogen peroxide in renal proximal tubular cells. J. Pharmacol. Exp. Ther. 325 (2008) 732-740
183. Zigmond M.J., and Keefe K.A. 6-Hydroxydopamine as a tool for studying catecholamines in adult animals. In: Selective H., and Kostrzewa R.M. (Eds). Neurotoxins: Basic, Clinical Applications (1997), Humana Press, Inc., Totowa, NJ 75-107