Sustained resistance to acute MPTP toxicity by hypothalamic dopamine neurons following chronic neurotoxicant exposure is associated with sustained up-regulation of parkin protein

NeuroToxicology

Volumn 37, Issue , 2013, Pages 144-153

  Benskey, Matthew ^a   Lee, Ki Yong ^d   Parikh, Kevin ^c   Lookingland, Keith J ^a,b   Goudreau, John L ^a,b,c  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c East Lansing   (United States)

^d Korea University   (South Korea)

Author keywords

MPTP; Parkin; Parkinson disease; Recovery; Tuberoinfundibular; UCHL1

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE; DOPAMINE TRANSPORTER; PARKIN; TYROSINE 3 MONOOXYGENASE; UBIQUITIN CARBOXY TERMINAL HYDROLASE L 1; UBIQUITIN THIOLESTERASE; UNCLASSIFIED DRUG;

ACUTE TOXICITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; EXPOSURE; HYPOTHALAMIC TUBEROINFUNDIBULAR DOPAMINE NEURON; MALE; MIDBRAIN NIGROSTRIATAL DOPAMINE NEURON; MOUSE; NERVE ENDING; NERVE FIBER DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBSTANTIA NIGRA; UPREGULATION; WESTERN BLOTTING;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; HYPOTHALAMUS; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; MPTP POISONING; NERVE DEGENERATION; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; UBIQUITIN THIOLESTERASE; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION;

MUS;

EID: 84878872782     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2013.04.002     Document Type: Article

References (65)

1. Ahlskog J.E. Challenging conventional wisdom: the etiologic role of dopamine oxidative stress in Parkinson's disease. Mov Disord 2004, 20:271-282.
2. Behrouz B., Drolet R.E., Sayed Z.A., Lookingland K.J., Goudreau J.L. Unique responses to mitochondrial complex I inhibition in tuberoinfundibular dopamine neurons may impart resistance to toxic insult. Neuroscience 2007, 147:592-598.
3. Benskey M., Behrouz B., Sunryd J., Pappas S.S., Baek S.H., Huebner M., et al. Recovery of hypothalamic tuberoinfundibular dopamine neurons from acute toxicant exposure is dependent upon protein synthesis and associated with an increase in parkin and ubiquitin carboxy-terminal hydrolase-L1 expression. Neurotoxicology 2012, 33:321-331.
4. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat Neurosci 2000, 3:1301-1306.
5. Braak H., Braak E. Pathoanatomy of Parkinson's disease. J Neurol 2000, 247.
6. Braak H., Tredici K.D., Rub U., de Vos R.A.I., Jansen Steur E.N.H., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003, 24:197-211.
7. Chan P., DeLanney L.E., Irwin I., Langston J.W., Monte D. Rapid ATP loss caused by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mouse brain. J Neurochem 2006, 57:348-351.
8. Chung K.K.K., Thomas B., Li X., Pletnikova O., Troncoso J.C., Marsh L., et al. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 2004, 304:1328-1331.
9. Cookson M.R., Lockhart P.J., McLendon C., O'Farrell C., Schlossmacher M., Farrer M.J. RING finger 1 mutations in Parkin produce altered localization of the protein. Hum Mol Genet 2003, 12:2957-2965.
10. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39:889-909.
11. Demarest K., Moore K. Lack of a high affinity transport system for dopamine in the median eminence and posterior pituitary. Brain Res 1979, 171:545-551.
12. DeMaria J.E., Nagy G.M., Lerant A.A., Fekete M.I.E., Levenson C.W., Freeman M.E. Dopamine transporters participate in the physiological regulation of prolactin. Endocrinology 2000, 141:366-374.
13. +) cause rapid ATP depletion in isolated hepatocytes. Biochem Biophys Res Commun 1986, 137:310-315.
14. Fahn S. Description of Parkinson's disease as a clinical syndrome. Ann NY Acad Sci 2003, 991:1-14.
15. Fornai F., Schluter O.M., Lenzi P., Gesi M., Ruffoli R., Ferrucci M., et al. Parkinson-like syndrome induced by continuous MPTP infusion: convergent roles of the ubiquitin-proteasome system and α-synuclein. Proc Natl Acad Sci USA 2005, 102:3413-3418.
16. Greenamyre J.T., MacKenzie G., Peng T.I., Stephans S.E. Mitochondrial dysfunction in Parkinson's disease. Biochem Soc Symp 1999, 66:85-97.
17. Gundersen H., Jensen E. The efficiency of systematic sampling in stereology and its prediction. J Microsc 2011, 147:229-263.
18. +) induces NADH-dependent superoxide formation and enhances NADH-dependent lipid peroxidation in bovine heart submitochondrial particles. Biochem Biophys Res Commun 1990, 170:1049-1055.
19. Hoglinger G.U., Carrard G., Michel P.P., Medja F., Lombes A., Ruberg M., et al. Dysfunction of mitochondrial complex I and the proteasome: interactions between two biochemical deficits in a cellular model of Parkinson's disease. J Neurochem 2003, 86:1297-1307.
20. Hung H.C., Lee E.H.Y. MPTP produces differential oxidative stress and antioxidative responses in the nigrostriatal and mesolimbic dopaminergic pathways. Free Radic Biol Med 1998, 24:76-84.
21. Jackson-Lewis V., Jakowec M., Burke R.E., Przedborski S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 1995, 4:257-269.
22. Jenner P. Oxidative stress in Parkinson's disease. Ann Neurol 2003, 53:S26-S38.
23. Jiang H., Ren Y., Zhao J., Feng J. Parkin protects human dopaminergic neuroblastoma cells against dopamine-induced apoptosis. Hum Mol Genet 2004, 13:1745-1754.
24. Langston J.W., Forno L.S. The hypothalamus in Parkinson disease. Ann Neurol 2004, 3:129-133.
25. Lookingland K.J., Moore K.E. Chapter VIII: Functional neuroanatomy of hypothalamic dopaminergic neuroendocrine systems. Handbook of chemical neuroanatomy 2005, vol. 21:435-523. Elsevier, Philadelphia.
26. Lotharius J., O'Malley K.L. The parkinsonism-inducing drug 1-methyl-4-phenylpyridinium triggers intracellular dopamine oxidation. J Biol Chem 2000, 275:38581-38588.
27. Manfredsson F.P., Burger C., Sullivan L.F., Muzyczka N., Lewin A.S., Mandel R.J. rAAV-mediated nigral human parkin over-expression partially ameliorates motor deficits via enhanced dopamine neurotransmission in a rat model of Parkinson's disease. Exp Neurol 2007, 207:289-301.
28. McNaught K.S.P., Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci Lett 2001, 297:191-194.
29. Meredith G.E., Totterdell S., Potashkin J.A., Surmeier D.J. Modeling PD pathogenesis in mice: advantages of a chronic MPTP protocol. Parkinsonism Relat Disord 2008, 14:S112-S115.
30. Mogi M., Harada M., Kojima K., Kiuchi K., Nagatsu T. Effects of systemic administration of 1-methyl-4-phenyl-1,2,3,6-tetrahydro-pyridine to mice on tyrosine hydroxylase, l-3,4-dihydroxyphenylalanine decarboxylase, dopamine beta-hydroxylase, and mono-amine oxidase activities in the striatum and hypothalamus. J Neurochem 1988, 50:1053-1056.
31. Moore K.E., Lookingland K. Dopaminergic neuronal systems in the hypothalamus. Psychopharmacology: the fourth generation of progress 1995, 245-256. Springer, New York, Heidelberg.
32. Moriyama Y., Amakatsu K., Futai M. Uptake of the neurotoxin, 4-methylphenylpyridinium, into chromaffin granules and synaptic vesicles: a proton gradient drives its uptake through monoamine transporter. Arch Biochem Biophys 1993, 305:271-277.
33. 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.
34. Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 1973, 59:449-450.
35. Palkovits M., Brownstein M.J. Microdissection of brain areas by the punch technique. Brain microdissection techniques 1983, vol. 2:1-36. John Wiley and Sons, Chichester.
36. Petroske E., Meredith G., Callen S., Totterdell S., Lau Y.S. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 2001, 106:589-601.
37. Petrucelli L., O'Farrell C., Lockhart P.J., Baptista M., Kehoe K., Vink L., et al. Parkin protects against the toxicity associated with mutant α-synuclein: proteasome dysfunction selectively affects catecholaminergic neurons. Neuron 2002, 36:1007-1019.
38. Poole A.C., Thomas R.E., Andrews L.A., McBride H.M., Whitworth A.J., Pallanck L.J. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc Natl Acad Sci USA 2008, 105:1638-1643.
39. Priyadarshi A., Khuder S.A., Schaub E.A., Priyadarshi S.S. Environmental risk factors and Parkinson's disease: a metaanalysis. Environ Res 2001, 86:122-127.
40. Przedborski S., Ischiropoulos H. Reactive oxygen and nitrogen species: weapons of neuronal destruction in models of Parkinson's disease. Antioxid Redox Signal 2005, 7:685-693.
41. Przedborski S., Tieu K., Perier C., Vila M. MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J Bioenerg Biomembr 2004, 36:375-379.
42. Revay R., Vaughan R., Grant S., Kuhar M.J. Dopamine transporter immunohistochemistry in median eminence, amygdala, and other areas of the rat brain. Synapse 1996, 22:93-99.
43. +) but not 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) selectively destroys dopaminergic neurons in cultures of dissociated rat mesencephalic neurons. Neurosci Lett 1986, 72:215-220.
44. Sanchez-Ramos J.R., Michel P., Weiner W.J., Hefti F. Selective destruction of cultured dopaminergic neurons from fetal rat mesencephalon by 1-methyl-4-phenylpyridinium: cytochemical and morphological evidence. J Neurochem 2006, 50:1934-1944.
45. Scotcher K.P., Irwin I., DeLanney L.E., Langston J.W., Monte D. Effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine and 1-methyl-4-phenylpyridinium ion on ATP levels of mouse brain synaptosomes. J Neurochem 2006, 54:1295-1301.
46. Shahed J., Jankovic J. Motor symptoms in Parkinson's disease. Handbook of clinical neurology 2007, vol. 83:329-342. Elsevier, Philadelphia.
47. Shen H., Sikorska M., Leblanc J., Walker P., Liu Q. Oxidative stress regulated expression of ubiquitin carboxyl-terminal hydrolase-L1: role in cell survival. Apoptosis 2006, 11:1049-1059.
48. Sriram K., Pai K.S., Boyd M.R., Ravindranath V. Evidence for generation of oxidative stress in brain by MPTP: in vitro and in vivo studies in mice. Brain Res 1997, 749:44-52.
49. Sriram S.R., Li X., Ko H.S., Chung K.K.K., Wong E., Lim K.L., et al. Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of parkin. Hum Mol Genet 2005, 14:2571-2586.
50. Sulzer D. Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci 2007, 30:244-250.
51. Sundstrum E., Fredriksson A., Archer T. Chronic neurochemical and behavioral changes in MPTP-lesioned C57BL/6 mice: a model for Parkinson's disease. Brain Res 1990, 528:181-188.
52. Tatton N., Kish S. In situ detection of apoptotic nuclei in the substantia nigra compacta of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated mice using terminal deoxynucleotidyl transferase labelling and acridine orange staining. Neuroscience 1997, 77:1037-1048.
53. Tatton W.G., Kwan M.M., Verrier M.C., Seniuk N.A., Theriault E. MPTP produces reversible disappearance of tyrosine hydroxylase-containing retinal amacrine cells. Brain Res 1990, 527:21-31.
54. Timmerman W., Deinum M., Westerink B., Schuiling G. Lack of evidence for dopamine autoreceptors in the mediobasal hypothalamus: a microdialysis study in awake rats. Neurosci Lett 1995, 195:113-116.
55. Vercammen L., Van der Perren A., Vaudano E., Gijsbers R., Debyser Z., Van den Haute C., et al. Parkin protects against neurotoxicity in the 6-hydroxydopamine rat model for Parkinson's disease. Mol Ther 2006, 14:716-723.
56. Walker J.M. The bicinchoninic acid (BCA) assay for protein quantitation. Methods Mol Biol 1994, 32:5-8.
57. Wang C., Ko H.S., Thomas B., Tsang F., Chew K.C.M., Tay S.P., et al. Stress-induced alterations in parkin solubility promote parkin aggregation and compromise parkin's protective function. Hum Mol Genet 2005, 14:3885-3897.
58. Wang C., Tan J.M.M., Ho M.W.L., Zaiden N., Wong S.H., Chew C.L.C., et al. Alterations in the solubility and intracellular localization of parkin by several familial Parkinson's disease-linked point mutations. J Neurochem 2005, 93:422-431.
59. Willis G.L., Donnan G.A. Histochemical, biochemical and behavioural consequences of MPTP treatment in C-57 black mice. Brain Res 1987, 402:269-274.
60. Yamada M., Mizuno Y., Mochizuki H. Parkin gene therapy for α-synucleinopathy: a rat model of Parkinson's disease. Hum Gene Ther 2005, 16:262-270.
61. Yao D., Gu Z., Nakamura T., Shi Z.Q., Ma Y., Gaston B., et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA 2004, 101:10810-10814.
62. Yasuda T., Hayakawa H., Nihira T., Ren Y.R., Nakata Y., Nagai M., et al. Parkin-mediated protection of dopaminergic neurons in a chronic MPTP-minipump mouse model of Parkinson disease. J Neuropathol Exp Neurol 2011, 70:686-697.
63. Yokoyama H., Kuroiwa H., Yano R., Araki T. Targeting reactive oxygen species, reactive nitrogen species and inflammation in MPTP neurotoxicity and Parkinson's disease. Neurol Sci 2008, 29:293-301.
64. Yokoyama H., Takagi S., Watanabe Y., Kato H., Araki T. Role of reactive nitrogen and reactive oxygen species against MPTP neurotoxicity in mice. J Neural Transm 2008, 115:831-842.
65. Zang L.Y., Misra H. Generation of reactive oxygen species during the monoamine oxidase-catalyzed oxidation of the neurotoxicant, 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Biol Chem 1993, 268:16504-16512.