Surprising behavioral and neurochemical enhancements in mice with combined mutations linked to Parkinson's disease

Neurobiology of Disease

Volumn 62, Issue , 2014, Pages 113-123

  Hennis, Meghan R ^a   Marvin, Marian A ^a   Taylor, Charles M ^a   Goldberg, Matthew S ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

DJ 1; Glutathione peroxidase; Knockout mice; Parkin; Parkinson's disease

Indexed keywords

DJ 1 PROTEIN; DOPAMINE; GLUTATHIONE PEROXIDASE 1; PARKIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LOSS OF FUNCTION MUTATION; MOUSE; NERVE PROJECTION; NEUROCHEMISTRY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; ROTAROD TEST; SEROTONIN BRAIN LEVEL; SEROTONINERGIC SYSTEM; SMELLING; STEREOLOGY;

DJ-1; GLUTATHIONE PEROXIDASE; KNOCKOUT MICE; PARKIN; PARKINSON'S DISEASE;

AGE FACTORS; ANIMALS; BIOGENIC MONOAMINES; CELL COUNT; CORPUS STRIATUM; DOPAMINE; DOPAMINERGIC NEURONS; GLUTATHIONE PEROXIDASE; HIPPOCAMPUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; ONCOGENE PROTEINS; PARKINSON DISEASE; SEROTONIN; UBIQUITIN-PROTEIN LIGASES;

EID: 84885452439     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.09.009     Document Type: Article

References (94)

1. Andres-Mateos E., Perier C., Zhang L., Blanchard-Fillion B., Greco T.M., Thomas B., Ko H.S., Sasaki M., Ischiropoulos H., Przedborski S., Dawson T.M., Dawson V.L. DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:14807-14812.
2. Bensadoun J.C., Mirochnitchenko O., Inouye M., Aebischer P., Zurn A.D. Attenuation of 6-OHDA-induced neurotoxicity in glutathione peroxidase transgenic mice. Eur. J. Neurosci. 1998, 10:3231-3236.
3. Benzi G., Pastoris O., Marzatico F., Villa R.F. Cerebral enzyme antioxidant system. Influence of aging and phosphatidylcholine. J. Cereb. Blood Flow Metab. 1989, 9:373-380.
4. Bernheimer H., Birkmayer W., Hornykiewicz O., Jellinger K., Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 1973, 20:415-455.
5. 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 One 2012, 7:e39953.
6. Bonifati V. Genetics of parkinsonism. Parkinsonism Relat. Disord. 2007, 13(Suppl. 3):S233-S241.
7. Bonifati V., Rizzu P., van Baren M.J., Schaap O., Breedveld G.J., Krieger E., Dekker M.C., Squitieri F., Ibanez P., Joosse M., van Dongen J.W., Vanacore N., van Swieten J.C., Brice A., Meco G., van Duijn C.M., Oostra B.A., Heutink P. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 2003, 299:256-259.
8. Buhot M.C. Serotonin receptors in cognitive behaviors. Curr. Opin. Neurobiol. 1997, 7:243-254.
9. Canet-Aviles R.M., Wilson M.A., Miller D.W., Ahmad R., McLendon C., Bandyopadhyay S., Baptista M.J., Ringe D., Petsko G.A., Cookson M.R. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9103-9108.
10. Chandran J.S., Lin X., Zapata A., Hoke A., Shimoji M., Moore S.O., Galloway M.P., Laird F.M., Wong P.C., Price D.L., Bailey K.R., Crawley J.N., Shippenberg T., Cai H. Progressive behavioral deficits in DJ-1-deficient mice are associated with normal nigrostriatal function. Neurobiol. Dis. 2008, 29:505-514.
11. Choi J., Sullards M.C., Olzmann J.A., Rees H.D., Weintraub S.T., Bostwick D.E., Gearing M., Levey A.I., Chin L.S., Li L. Oxidative Damage of DJ-1 Is Linked to Sporadic Parkinson and Alzheimer Diseases. J. Biol. Chem. 2006, 281:10816-10824.
12. Cookson M.R. DJ-1, PINK1, and their effects on mitochondrial pathways. Mov. Disord. 2010, 25(Suppl. 1):S44-S48.
13. Corti O., Lesage S., Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 2011, 91:1161-1218.
14. Dawson T.M., Ko H.S., Dawson V.L. Genetic animal models of Parkinson's disease. Neuron 2010, 66:646-661.
15. Doty R.L., Deems D.A., Stellar S. Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 1988, 38:1237-1244.
16. Doty R.L., Stern M.B., Pfeiffer C., Gollomp S.M., Hurtig H.I. Bilateral olfactory dysfunction in early stage treated and untreated idiopathic Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 1992, 55:138-142.
17. Dunham N.W., Miya T.S. A note on a simple apparatus for detecting neurological deficit in rats and mice. J. Am. Pharm. Assoc. Am. Pharm. Assoc. (Baltim) 1957, 46:208-209.
18. Fleming S.M., Chesselet M.F. Behavioral phenotypes and pharmacology in genetic mouse models of Parkinsonism. Behav. Pharmacol. 2006, 17:383-391.
19. Fleming S.M., Fernagut P.O., Chesselet M.F. Genetic mouse models of parkinsonism: strengths and limitations. NeuroRx 2005, 2:495-503.
20. Frank-Cannon T.C., Tran T., Ruhn K.A., Martinez T.N., Hong J., Marvin M., Hartley M., Trevino I., O'Brien D.E., Casey B., Goldberg M.S., Tansey M.G. Parkin deficiency increases vulnerability to inflammation-related nigral degeneration. J. Neurosci. 2008, 28:10825-10834.
21. Goldberg M.S., Fleming S.M., Palacino J.J., Cepeda C., Lam H.A., Bhatnagar A., Meloni E.G., Wu N., Ackerson L.C., Klapstein G.J., Gajendiran M., Roth B.L., Chesselet M.F., Maidment N.T., Levine M.S., Shen J. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem. 2003, 278:43628-43635.
22. Goldberg M.S., Pisani A., Haburcak M., Vortherms T.A., Kitada T., Costa C., Tong Y., Martella G., Tscherter A., Martins A., Bernardi G., Roth B.L., Pothos E.N., Calabresi P., Shen J. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron 2005, 45:489-496.
23. Graham D.R., Sidhu A. Mice expressing the A53T mutant form of human alpha-synuclein exhibit hyperactivity and reduced anxiety-like behavior. J. Neurosci. Res. 2010, 88:1777-1783.
24. Hattori N. Autosomal dominant parkinsonism: its etiologies and differential diagnoses. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S1-S3.
25. Hauser D.N., Hastings T.G. Mitochondrial dysfunction and oxidative stress in Parkinson's disease and monogenic parkinsonism. Neurobiol. Dis. 2013, 51:35-42.
26. Hayashi T., Ishimori C., Takahashi-Niki K., Taira T., Kim Y.C., Maita H., Maita C., Ariga H., Iguchi-Ariga S.M. DJ-1 binds to mitochondrial complex I and maintains its activity. Biochem. Biophys. Res. Commun. 2009, 390:667-672.
27. Holmes A., Murphy D.L., Crawley J.N. Reduced aggression in mice lacking the serotonin transporter. Psychopharmacology (Berl) 2002, 161:160-167.
28. Horowitz M.P., Greenamyre J.T. Gene-environment interactions in Parkinson's disease: the importance of animal modeling. Clin. Pharmacol. Ther. 2010, 88:467-474.
29. Itier J.M., Ibanez P., Mena M.A., Abbas N., Cohen-Salmon C., Bohme G.A., Laville M., Pratt J., Corti O., Pradier L., Ret G., Joubert C., Periquet M., Araujo F., Negroni J., Casarejos M.J., Canals S., Solano R., Serrano A., Gallego E., Sanchez M., Denefle P., Benavides J., Tremp G., Rooney T.A., Brice A., Garcia de Yebenes J. Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum. Mol. Genet. 2003, 12:2277-2291.
30. Jiang H., Jiang Q., Feng J. Parkin increases dopamine uptake by enhancing the cell surface expression of dopamine transporter. J. Biol. Chem. 2004, 279:54380-54386.
31. Junn E., Jang W.H., Zhao X., Jeong B.S., Mouradian M.M. Mitochondrial localization of DJ-1 leads to enhanced neuroprotection. J. Neurosci. Res. 2009, 87:123-129.
32. Kawajiri S., Saiki S., Sato S., Sato F., Hatano T., Eguchi H., Hattori N. PINK1 is recruited to mitochondria with parkin and associates with LC3 in mitophagy. FEBS Lett. 2010, 584:1073-1079.
33. Kim R.H., Smith P.D., Aleyasin H., Hayley S., Mount M.P., Pownall S., Wakeham A., You-Ten A.J., Kalia S.K., Horne P., Westaway D., Lozano A.M., Anisman H., Park D.S., Mak T.W. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5215-5220.
34. Kish S.J., Tong J., Hornykiewicz O., Rajput A., Chang L.J., Guttman M., Furukawa Y. Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 2008, 131:120-131.
35. Kitada T., Asakawa S., Hattori N., Matsumine H., Yamamura Y., Minoshima S., Yokochi M., Mizuno Y., Shimizu N. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998, 392:605-608.
36. Kitada T., Tong Y., Gautier C.A., Shen J. Absence of nigral degeneration in aged parkin/DJ-1/PINK1 triple knockout mice. J. Neurochem. 2009, 111:696-702.
37. Klivenyi P., Andreassen O.A., Ferrante R.J., Dedeoglu A., Mueller G., Lancelot E., Bogdanov M., Andersen J.K., Jiang D., Beal M.F. Mice deficient in cellular glutathione peroxidase show increased vulnerability to malonate, 3-nitropropionic acid, and 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. J. Neurosci. 2000, 20:1-7.
38. Kubo S.I., Kitami T., Noda S., Shimura H., Uchiyama Y., Asakawa S., Minoshima S., Shimizu N., Mizuno Y., Hattori N. Parkin is associated with cellular vesicles. J. Neurochem. 2001, 78:42-54.
39. Kuhn K., Zhu X.R., Lubbert H., Stichel C.C. Parkin expression in the developing mouse. Brain Res. Dev. Brain Res. 2004, 149:131-142.
40. Lee C.S., Sauer H., Bjorklund A. Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by instrastriatal 6-hydroxydopamine in the rat. Neuroscience 1996, 72:641-653.
41. Lev N., Ickowicz D., Melamed E., Offen D. Oxidative insults induce DJ-1 upregulation and redistribution: Implications for neuroprotection. Neurotoxicology 2008, 29:397-405.
42. Liddell J.R., Robinson S.R., Dringen R., Bishop G.M. Astrocytes retain their antioxidant capacity into advanced old age. Glia 2010, 58:1500-1509.
43. Lo Bianco C., Schneider B.L., Bauer M., Sajadi A., Brice A., Iwatsubo T., Aebischer P. Lentiviral vector delivery of parkin prevents dopaminergic degeneration in an alpha-synuclein rat model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:17510-17515.
44. Lopez G., Sidransky E. Autosomal recessive mutations in the development of Parkinson's disease. Biomark. Med 2010, 4:713-721.
45. Manning-Bog A.B.., Caudle W.M., Perez X.A., Reaney S.H., Paletzki R., Isla M.Z., Chou V.P., McCormack A.L., Miller G.W., Langston J.W., Gerfen C.R., Dimonte D.A. Increased vulnerability of nigrostriatal terminals in DJ-1-deficient mice is mediated by the dopamine transporter. Neurobiol. Dis. 2007, 27:141-150.
46. McFadyen M.P., Kusek G., Bolivar V.J., Flaherty L. Differences among eight inbred strains of mice in motor ability and motor learning on a rotorod. Genes Brain Behav. 2003, 2:214-219.
47. Menzies F.M., Yenisetti S.C., Min K.T. Roles of Drosophila DJ-1 in survival of dopaminergic neurons and oxidative stress. Curr. Biol. 2005, 15:1578-1582.
48. Meulener M., Whitworth A.J., Armstrong-Gold C.E., Rizzu P., Heutink P., Wes P.D., Pallanck L.J., Bonini N.M. Drosophila DJ-1 mutants are selectively sensitive to environmental toxins associated with Parkinson's disease. Curr. Biol. 2005, 15:1572-1577.
49. Moore D.J., Zhang L., Troncoso J., Lee M.K., Hattori N., Mizuno Y., Dawson T.M., Dawson V.L. Association of DJ-1 and parkin mediated by pathogenic DJ-1 mutations and oxidative stress. Hum. Mol. Genet. 2005, 14:71-84.
50. Morelli E., Moore H., Rebello T.J., Gray N., Steele K., Esposito E., Gingrich J.A., Ansorge M.S. Chronic 5-HT transporter blockade reduces DA signaling to elicit basal ganglia dysfunction. J. Neurosci. 2011, 31:15742-15750.
51. Muftuoglu M., Elibol B., Dalmizrak O., Ercan A., Kulaksiz G., Ogus H., Dalkara T., Ozer N. Mitochondrial complex I and IV activities in leukocytes from patients with parkin mutations. Mov. Disord. 2004, 19:544-548.
52. Mullett S.J., Hinkle D.A. DJ-1 deficiency in astrocytes selectively enhances mitochondrial Complex I inhibitor-induced neurotoxicity. J. Neurochem. 2011, 117:375-387.
53. Narendra D., Tanaka A., Suen D.F., Youle R.J. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J. Cell Biol. 2008, 183:795-803.
54. Palacino J.J., Sagi D., Goldberg M.S., Krauss S., Motz C., Wacker M., Klose J., Shen J. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J. Biol. Chem. 2004, 279:18614-18622.
55. Paterna J.C., Leng A., Weber E., Feldon J., Bueler H. DJ-1 and Parkin modulate dopamine-dependent behavior and inhibit MPTP-induced nigral dopamine neuron loss in mice. Mol. Ther. 2007, 15:698-704.
56. Pellicano C., Benincasa D., Pisani V., Buttarelli F.R., Giovannelli M., Pontieri F.E. Prodromal non-motor symptoms of Parkinson's disease. Neuropsychiatr. Dis. Treat. 2007, 3:145-152.
57. Perez F.A., Palmiter R.D. Parkin-deficient mice are not a robust model of parkinsonism. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2174-2179.
58. Perez F.A., Curtis W.R., Palmiter R.D. Parkin-deficient mice are not more sensitive to 6-hydroxydopamine or methamphetamine neurotoxicity. BMC Neurosci. 2005, 6:71.
59. Pham T.T., Giesert F., Rothig A., Floss T., Kallnik M., Weindl K., Holter S.M., Ahting U., Prokisch H., Becker L., Klopstock T., Hrabe de Angelis M., Beyer K., Gorner K., Kahle P.J., Vogt Weisenhorn D.M., Wurst W. DJ-1-deficient mice show less TH-positive neurons in the ventral tegmental area and exhibit non-motoric behavioural impairments. Genes Brain Behav. 2010, 9:305-317.
60. Pham A.H., Meng S., Chu Q.N., Chan D.C. Loss of Mfn2 results in progressive, retrograde degeneration of dopaminergic neurons in the nigrostriatal circuit. Hum. Mol. Genet. 2012, 21:4817-4826.
61. Politis M., Wu K., Loane C., Kiferle L., Molloy S., Brooks D.J., Piccini P. Staging of serotonergic dysfunction in Parkinson's disease: an in vivo 11C-DASB PET study. Neurobiol. Dis. 2010, 40:216-221.
62. Politis M., Wu K., Loane C., Turkheimer F.E., Molloy S., Brooks D.J., Piccini P. Depressive symptoms in PD correlate with higher 5-HTT binding in raphe and limbic structures. Neurology 2010, 75:1920-1927.
63. Ridet J.L., Bensadoun J.C., Deglon N., Aebischer P., Zurn A.D. Lentivirus-mediated expression of glutathione peroxidase: neuroprotection in murine models of Parkinson's disease. Neurobiol. Dis. 2006, 21:29-34.
64. Rodriguez-Navarro J.A., Casarejos M.J., Menendez J., Solano R.M., Rodal I., Gomez A., Yebenes J.G., Mena M.A. Mortality, oxidative stress and tau accumulation during ageing in parkin null mice. J. Neurochem. 2007, 103:98-114.
65. Roselli F., Pisciotta N.M., Pennelli M., Aniello M.S., Gigante A., De Caro M.F., Ferrannini E., Tartaglione B., Niccoli-Asabella A., Defazio G., Livrea P., Rubini G. Midbrain SERT in degenerative parkinsonisms: a 123I-FP-CIT SPECT study. Mov. Disord. 2010, 25:1853-1859.
66. Rousseaux M.W., Marcogliese P.C., Qu D., Hewitt S.J., Seang S., Kim R.H., Slack R.S., Schlossmacher M.G., Lagace D.C., Mak T.W., Park D.S. Progressive dopaminergic cell loss with unilateral-to-bilateral progression in a genetic model of Parkinson disease. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15918-15923.
67. Sato S., Chiba T., Nishiyama S., Kakiuchi T., Tsukada H., Hatano T., Fukuda T., Yasoshima Y., Kai N., Kobayashi K., Mizuno Y., Tanaka K., Hattori N. Decline of striatal dopamine release in parkin-deficient mice shown by ex vivo autoradiography. J. Neurosci. Res. 2006, 84:1350-1357.
68. Scatton B., Javoy-Agid F., Rouquier L., Dubois B., Agid Y. Reduction of cortical dopamine, noradrenaline, serotonin and their metabolites in Parkinson's disease. Brain Res. 1983, 275:321-328.
69. Shang H., Lang D., Jean-Marc B., Kaelin-Lang A. Localization of DJ-1 mRNA in the mouse brain. Neurosci. Lett. 2004, 367:273-277.
70. Shimura H., Hattori N., Kubo S., Yoshikawa M., Kitada T., Matsumine H., Asakawa S., Minoshima S., Yamamura Y., Shimizu N., Mizuno Y. Immunohistochemical and subcellular localization of Parkin protein: absence of protein in autosomal recessive juvenile parkinsonism patients. Ann. Neurol. 1999, 45:668-672.
71. Shimura H., Hattori N., Kubo S., Mizuno Y., Asakawa S., Minoshima S., Shimizu N., Iwai K., Chiba T., Tanaka K., Suzuki T. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 2000, 25:302-305.
72. Shin J.H., Ko H.S., Kang H., Lee Y., Lee Y.I., Pletinkova O., Troconso J.C., Dawson V.L., Dawson T.M. PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 2011, 144:689-702.
73. Shulman J.M., De Jager P.L., Feany M.B. Parkinson's disease: genetics and pathogenesis. Annu. Rev. Pathol. 2011, 6:193-222.
74. Stichel C.C., Augustin M., Kuhn K., Zhu X.R., Engels P., Ullmer C., Lubbert H. Parkin expression in the adult mouse brain. Eur. J. Neurosci. 2000, 12:4181-4194.
75. Taira T., Saito Y., Niki T., Iguchi-Ariga S.M., Takahashi K., Ariga H. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep. 2004, 5:213-218.
76. Thomas K.J., McCoy M.K., Blackinton J., Beilina A., van der Brug M., Sandebring A., Miller D., Maric D., Cedazo-Minguez A., Cookson M.R. DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum. Mol. Genet. 2011, 20:40-50.
77. Ulusoy A., Kirik D. Can overexpression of parkin provide a novel strategy for neuroprotection in Parkinson's disease?. Exp. Neurol. 2008, 212:258-260.
78. Usami Y., Hatano T., Imai S., Kubo S., Sato S., Saiki S., Fujioka Y., Ohba Y., Sato F., Funayama M., Eguchi H., Shiba K., Ariga H., Shen J., Hattori N. DJ-1 associates with synaptic membranes. Neurobiol. Dis. 2011, 43:651-662.
79. Varcin M., Bentea E., Michotte Y., Sarre S. Oxidative stress in genetic mouse models of Parkinson's disease. Oxidative Med. Cell. Longev. 2012, 2012:624925.
80. Venkateshappa C., Harish G., Mythri R.B., Mahadevan A., Bharath M.M., Shankar S.K. Increased oxidative damage and decreased antioxidant function in aging human substantia nigra compared to striatum: implications for Parkinson's disease. Neurochem. Res. 2012, 37:358-369.
81. Vercammen L., Van der Perren A., Vaudano E., Gijsbers R., Debyser Z., Van den Haute C., Baekelandt V. Parkin protects against neurotoxicity in the 6-hydroxydopamine rat model for Parkinson's disease. Mol. Ther. 2006, 14:716-723.
82. Vincent A., Briggs L., Chatwin G.F., Emery E., Tomlins R., Oswald M., Middleton C.A., Evans G.J., Sweeney S.T., Elliott C.J. Parkin-induced defects in neurophysiology and locomotion are generated by metabolic dysfunction and not oxidative stress. Hum. Mol. Genet. 2012, 21:1760-1769.
83. Vincow E.S., Merrihew G., Thomas R.E., Shulman N.J., Beyer R.P., Maccoss M.J., Pallanck L.J. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6400-6405.
84. Vinish M., Anand A., Prabhakar S. Altered oxidative stress levels in Indian Parkinson's disease patients with PARK2 mutations. Acta Biochim. Pol. 2011, 58:165-169.
85. Von Coelln R., Thomas B., Savitt J.M., Lim K.L., Sasaki M., Hess E.J., Dawson V.L., Dawson T.M. Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10744-10749.
86. Xie Z., Zhuang X., Chen L. DJ-1 mRNA anatomical localization and cell type identification in the mouse brain. Neurosci. Lett. 2009, 465:214-219.
87. Yamakado H., Moriwaki Y., Yamasaki N., Miyakawa T., Kurisu J., Uemura K., Inoue H., Takahashi M., Takahashi R. alpha-Synuclein BAC transgenic mice as a model for Parkinson's disease manifested decreased anxiety-like behavior and hyperlocomotion. Neurosci. Res. 2012, 73:173-177.
88. Yang Y., Gehrke S., Haque M.E., Imai Y., Kosek J., Yang L., Beal M.F., Nishimura I., Wakamatsu K., Ito S., Takahashi R., Lu B. Inactivation of Drosophila DJ-1 leads to impairments of oxidative stress response and phosphatidylinositol 3-kinase/Akt signaling. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13670-13675.
89. Yang W., Chen L., Ding Y., Zhuang X., Kang U.J. Paraquat induces dopaminergic dysfunction and proteasome impairment in DJ-1-deficient mice. Hum. Mol. Genet. 2007, 16:2900-2910.
90. Yokota T., Sugawara K., Ito K., Takahashi R., Ariga H., Mizusawa H. Down regulation of DJ-1 enhances cell death by oxidative stress, ER stress, and proteasome inhibition. Biochem. Biophys. Res. Commun. 2003, 312:1342-1348.
91. Zhang J., Graham D.G., Montine T.J., Ho Y.S. Enhanced N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity in mice deficient in CuZn-superoxide dismutase or glutathione peroxidase. J. Neuropathol. Exp. Neurol. 2000, 59:53-61.
92. Zhang L., Shimoji M., Thomas B., Moore D.J., Yu S.W., Marupudi N.I., Torp R., Torgner I.A., Ottersen O.P., Dawson T.M., Dawson V.L. Mitochondrial localization of the Parkinson's disease related protein DJ-1: implications for pathogenesis. Hum. Mol. Genet. 2005, 14:2063-2073.
93. Zhou W., Freed C.R. DJ-1 up-regulates glutathione synthesis during oxidative stress and inhibits A53T alpha-synuclein toxicity. J. Biol. Chem. 2005, 280:43150-43158.
94. Zhu X.R., Maskri L., Herold C., Bader V., Stichel C.C., Gunturkun O., Lubbert H. Non-motor behavioural impairments in parkin-deficient mice. Eur. J. Neurosci. 2007, 26:1902-1911.