Increased expression of the dopamine transporter leads to loss of dopamine neurons, oxidative stress and l-DOPA reversible motor deficits

Neurobiology of Disease

Volumn 74, Issue , 2015, Pages 66-75

  Masoud, S T ^a   Vecchio, L M ^a   Bergeron, Y ^b   Hossain, M M ^c   Nguyen, L T ^a   Bermejo, M K ^a   Kile, B ^d   Sotnikova, T D ^e,f   Siesser, W B ^g   Gainetdinov, R R ^e,f,h   Wightman, R M ^d   Caron, M G ^g   Richardson, J R ^c   Miller, G W ^i,j   Ramsey, A J ^a   Cyr, M ^b   Salahpour, A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITÉ DU QUÉBEC À TROIS RIVIÈRES   (Canada)

^c RUTGERS UNIVERSITY   (United States)

^d University of North Carolina at Chapel Hill   (United States)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^f ST PETERSBURG STATE UNIVERSITY   (Russian Federation)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

^h SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

ⁱ EMORY UNIVERSITY   (United States)

^j EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

more..

Author keywords

Cytosolic dopamine; Dopamine neuron loss; Dopamine transporter; L DOPA; Motor deficits; MPTP; Oxidative stress; Parkinson's disease; Transgenic mice

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; CYSTEINYLDOPA; DOPAMINE; DOPAMINE TRANSPORTER; LEVODOPA; NEUROTRANSMITTER; ANTIPARKINSON AGENT; SLC18A2 PROTEIN, MOUSE; VESICULAR MONOAMINE TRANSPORTER;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; CYTOSOL; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; EXTRACELLULAR SPACE; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; METABOLITE; MOTOR DYSFUNCTION; MOUSE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CELL DEATH; DRUG EFFECTS; GENETICS; METABOLISM; MOTOR PERFORMANCE; MOVEMENT DISORDERS; PARKINSONISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

3,4-DIHYDROXYPHENYLACETIC ACID; ANIMALS; ANTI-DYSKINESIA AGENTS; CELL DEATH; CYTOSOL; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; DOPAMINERGIC NEURONS; LEVODOPA; MESENCEPHALON; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR SKILLS; MOVEMENT DISORDERS; OXIDATIVE STRESS; PARKINSONIAN DISORDERS; VESICULAR MONOAMINE TRANSPORT PROTEINS;

EID: 84912000258     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.10.016     Document Type: Article

References (67)

1. Adriani W., Boyer F., Gioiosa L., Macrì S., Dreyer J.L., Laviola G. Increased impulsive behavior and risk proneness following lentivirus-mediated dopamine transporter over-expression in rats' nucleus accumbens. Neuroscience 2009, 159(1):47-58. (Mar 3).
2. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12(10):366-375. (Oct).
3. Beal M.F. Parkinson's disease: a model dilemma. Nature 2010, 466(7310):S8-S10. (Aug 26).
4. Bennett B.A., Wichems C.H., Hollingsworth C.K., Davies H.M.L., Thornley C., Sexton T., Childers S.R. Novel 2-substituted cocaine analogs: uptake and ligand binding studies at dopamine, serotonin, and norepinephrine transport sites in the rat brain. J. Pharmacol. Exp. Ther. 1995, 272:1176-1186.
5. 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(4):415-455. (Dec).
6. Bezard E., Gross C.E., Fournier M.C., Dovero S., Bloch B., Jaber M. Absence of MPTP-induced neuronal death in mice lacking the dopamine transporter. Exp. Neurol. 1999, 155(2):268-273. (Feb).
7. Bezard E., Yue Z., Kirik D., Spillantini M.G. Animal models of Parkinson's disease: limits and relevance to neuroprotection studies. Mov. Disord. 2013, 28(1):61-70. (Jan).
8. Blanchard V., Raisman-Vozari R., Vyas S., Michel P.P., Javoy-Agid F., Uhl G., Agid Y. Differential expression of tyrosine hydroxylase and membrane dopamine transporter genes in subpopulations of dopaminergic neurons of the rat mesencephalon. Brain Res. Mol. Brain Res. 1994, 22(1-4):29-38. (Mar).
9. Calipari E.S., Ferris M.J., Salahpour A., Caron M.G., Jones S.R. Methylphenidate amplifies the potency and reinforcing effects of amphetamines by increasing dopamine transporter expression. Nat. Commun. 2013, 4:2720.
10. Cannon J.R., Greenamyre J.T. Gene-environment interactions in Parkinson's disease: specific evidence in humans and mammalian models. Neurobiol. Dis. 2013, 57:38-46. (Sep).
11. Caudle W.M., Richardson J.R., Wang M.Z., Taylor T.N., Guillot T.S., McCormack A.L., Colebrooke R.E., Di Monte D.A., Emson P.C., Miller G.W. Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J. Neurosci. 2007, 27:8138-8148.
12. Chen L., Ding Y., Cagniard B., Van Laar A.D., Mortimer A., Chi T., Hastings T.G., Kang U.J., Zhuang X. Unregulated cytosolic dopamine causes neurodegeneration associated with oxidative stress in mice. J. Neurosci. 2008, 28:425-433.
13. Chiba K., Peterson L.A., Castagnoli K.P., Trevor A.J., Castagnoli N. Studies on the molecular mechanism of bioactivation of the selective nigrostriatal toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Drug Metab. Dispos. 1985, 13:342-347.
14. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39(6):889-909.
15. Di Monte D.A., DeLanney L.E., Irwin I., Royland J.E., Chan P., Jakowec M.W., Langston J.W. Monoamine oxidase-dependent metabolism of dopamine in the striatum and substantia nigra of l-DOPA-treated monkeys. Brain Res. 1996, 738(1):53-59. (Oct 28).
16. Donovan D.M., Miner L.L., Perry M.P., Revay R.S., Sharpe L.G., Przedborski S., Kostic V., Philpot R.M., Kirstein C.L., Rothman R.B., Schindler C.W., Uhl G.R. Cocaine reward and MPTP toxicity: alteration by regional variant dopamine transporter overexpression. Brain Res. Mol. Brain Res. 1999, 73(1-2):37-49. (Nov 10).
17. Drucker-Colín R., García-Hernández F. A new motor test sensitive to aging and dopaminergic function. J. Neurosci. Methods 1991, 39(2):153-161. (Sep).
18. Fahn S. Description of Parkinson's disease as a clinical syndrome. Ann. N. Y. Acad. Sci. 2003, 991:1-14.
19. Fahn S., Cohen G. The oxidant stress hypothesis in Parkinson's disease: evidence supporting it. Ann. Neurol. 1992, 32:804-812.
20. Fleming S.M., Salcedo J., Fernagut P.O., Rockenstein E., Masliah E., Levine M.S., Chesselet M.F. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J. Neurosci. 2004, 24(42):9434-9440. (Oct 20).
21. Fornstedt B., Carlsson A. A marked rise in 5-S-cysteinyl-dopamine levels in guinea-pig striatum following reserpine treatment. J. Neural Transm. 1989, 76(2):155-161.
22. Gainetdinov R.R., Fumagalli F., Jones S.R., Caron M.G. Dopamine transporter is required for in vivo MPTP neurotoxicity: evidence from mice lacking the transporter. J. Neurochem. 1997, 69(3):1322-1325.
23. Ghisi V., Ramsey A.J., Masri B., Gainetdinov R.R., Caron M.G., Salahpour A. Reduced D2-mediated signaling activity and trans-synaptic upregulation of D1 and D2 dopamine receptors in mice overexpressing the dopamine transporter. Cell. Signal. 2009, 21(1):87-94. (Jan).
24. Giros B., Jaber M., Jones S.R., Wightman R.M., Caron M.G. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 1996, 379(6566):606-612. (Feb 15).
25. Gispert S., et al. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One 2009, 4(6):e5777. (3).
26. 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(44):43628-43635.
27. Goldstein D.S., Sullivan P., Cooney A., Jinsmaa Y., Sullivan R., Gross D.J., Holmes C., Kopin I.J., Sharabi Y. Vesicular uptake blockade generates the toxic dopamine metabolite 3,4-dihydroxyphenylacetaldehyde in PC12 cells: relevance to the pathogenesis of Parkinson's disease. J. Neurochem. 2012, 123(6):932-943.
28. Graham D.G., Tiffany S.M., Bell W.R., Gutknecht W.F. Autoxidation versus covalent binding of quinones as the mechanism of toxicity of dopamine, 6-hydroxydopamine, and related compounds toward C1300 neuroblastoma cells in vitro. Mol. Pharmacol. 1978, 14:644-653.
29. Hardy J., Cai H., Cookson M.R., Gwinn-Hardy K., Singleton A. Genetics of Parkinson's disease and parkinsonism. Ann. Neurol. 2006, 60(4):389-398.
30. Hastings T.G., Zigmond M.J. Identification of catechol-protein conjugates in neostriatal slices incubated with [3H]dopamine: impact of ascorbic acid and glutathione. J. Neurochem. 1994, 63(3):1126-1132. (Sep).
31. Hastings T.G., Lewis D.A., Zigmond M.J. Role of oxidation in the neurotoxic effects of intrastriatal dopamine injections. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:1956-1961.
32. Hatcher J.M., Richardson J.R., Guillot T.S., McCormack A.L., Di Monte D.A., Jones D.P., Pennell K.D., Miller G.W. Dieldrin exposure induces oxidative damage in the mouse nigrostriatal dopamine system. Exp. Neurol. 2007, 204(2):619-630. (Apr).
33. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III - the final common pathway. Schizophr. Bull. 2009, 35(3):549-562.
34. Hwang D.Y., Fleming S.M., Ardayfio P., Moran-Gates T., Kim H., Tarazi F.I., Chesselet M.F., Kim K.S. 3,4 Dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: behavioral characterization of a novel genetic model of Parkinson's disease. J. Neurosci. 2005, 25(8):2132-2137. (Feb 23).
35. Jaber M., Dumartin B., Sagné C., Haycock J.W., Roubert C., Giros B., Bloch B., Caron M.G. Differential regulation of tyrosine hydroxylase in the basal ganglia of mice lacking the dopamine transporter. Eur. J. Neurosci. 1999, 11(10):3499-3511.
36. Javitch J.A., D'Amato R.J., Strittmatter S.M., Snyder S.H. Parkinsonism-inducing neurotoxin, N-methyl-4-phenyl-I,2,3,6-tetrahydropyridine: uptake of the metabolite N-methyl-4-phenylpyridine by dopamine neurons explains selective toxicity. Proc. Natl. Acad. Sci. U. S. A. 1985, 82:2173-2177.
37. Jones S.R., Gainetdinov R.R., Jaber M., Giros B., Wightman R.M., Caron M.G. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(7):4029-4034. (31).
38. Kile B.M., Walsh P.L., McElligott Z.A., Bucher E.S., Guillot T.S., Salahpour A., Caron M.G., Wightman R.M. Optimizing the temporal resolution of fast-scan cyclic voltammetry. ACS Chem. Neurosci. 2012, 3(4):285-292. (Apr 18).
39. Langston J.W., Ballard P., Tetrud J.W., Irwin I. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983, 219(4587):979-980.
40. Langston J.W., Irwin I., Langston E.B., Forno L.S. Pargyline prevents MPTP-induced parkinsonism in primates. Science 1984, 225(4669):1480-1482. (Sep 28).
41. Lohr K.M., Bernstein A.I., Stout K.A., Dunn A.R., Lazo C.R., Alter S.P., Wang M., Li Y., Fan X., Hess E.J., Yi H., Vecchio L.M., Goldstein D.S., Guillot T.S., Salahpour A., Miller G.W. Increased vesicular monoamine transporter enhances dopamine release and opposes Parkinson disease-related neurodegeneration in vivo. Proc Natl Acad Sci U S A 2014, 111(27):9977-9982. (Jul 8).
42. Luk K.C., Kehm V., Carroll J., Zhang B., O'Brien P., Trojanowski J.Q., Lee V.M. Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science 2012, 338(6109):949-953. (Nov 16).
43. Martin I., Dawson V.L., Dawson T.M. Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics Hum. Genet. 2011, 12:301-325.
44. Martres M.P., Demeneix B., Hanoun N., Hamon M., Giros B. Up- and down-expression of the dopamine transporter by plasmid DNA transfer in the rat brain. Eur. J. Neurosci. 1998, 10(12):3607-3616. (Dec).
45. Miller G.W., Staley J.K., Heilman C.J., Perez J.T., Mash D.C., Rye D.B., Levey A.I. Immunochemical analysis of dopamine transporter protein in Parkinson's disease. Ann. Neurol. 1997, 41(4):530-539.
46. Miller G.W., Erickson J.D., Perez J.T., Penland S.N., Mash D.C., Rye D.B., Levey A.I. Immunochemical analysis of vesicular monoamine transporter (VMAT2) protein in Parkinson's disease. Exp. Neurol. 1999, 156(1):138-148. (Mar).
47. Miller G.W., Gainetdinov R.R., Levey A.I., Caron M.G. Dopamine transporters and neuronal injury. Trends Pharmacol. Sci. 1999, 20(10):424-429. (Oct).
48. Mosharov E.V., Larsen K.E., Kanter E., Phillips K.A., Wilson K., Schmitz Y., Krantz D.E., Kobayashi K., Edwards R.H., Sulzer D. Interplay between cytosolic dopamine, calcium, and alpha-synuclein causes selective death of substantia nigra neurons. Neuron 2009, 62:218-229.
49. Oaks A.W., Frankfurt M., Finkelstein D.I., Sidhu A. Age dependent effects of A53T alpha-synuclein on behavior and dopaminergic function. PLoS One 2013, 8(4):e60378.
50. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, San Diego.
51. Priyadarshi A., Khuder S.A., Schaub E.A., Shrivastava S. A meta-analysis of Parkinson's disease and exposure to pesticides. Neurotoxicology 2000, 21:435-440.
52. Rabey J.M., Burns R.S. Dopamine metabolites. Parkinson's Disease: Diagnosis and Clinical Management 2002, 227-245. Demos Medical Publishing, New York. 2nd ed. S.A. Factor, W.J. Weiner (Eds.).
53. Ramkissoon A., Wells P.G. Human prostaglandin-H-synthase (hPHS)-1- and hPHS-2-dependent bioactivation, oxidative macromolecular damage, and cytotoxicity of dopamine, its precursor, and its metabolites. Free Radic. Biol. Med. 2011, 50(2):295-304.
54. Ramsay R.R., Dadgar J., Trevor A., Singer T.P. Energy-driven uptake of N-methyl-4 phenylpyridine by brain mitochondria mediates the neurotoxicity of MPTP. Life Sci. 1986, 39(7):581-588. (Aug 18).
55. Ritz B.R., Manthripragada A.D., Costello S., Lincoln S.J., Farrer M.J., Cockburn M., Bronstein J. Dopamine transporter genetic variants and pesticides in Parkinson's disease. Environ. Health Perspect. 2009, 117:964-969.
56. Salahpour A., Ramsey A.J., Medvedev I.O., Kile B., Sotnikova T.D., Holmstrand E., Ghisi V., Nicholls P.J., Wong L., Murphy K., Sesack S.R., Wightman R.M., Gainetdinov R.R., Caron M.G. Increased amphetamine-induced hyperactivity and reward in mice overexpressing the dopamine transporter. Proc. Natl. Acad. Sci. U. S. A. 2008, 205:4405-4410.
57. Schober A. Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res. 2004, 318:215-224.
58. Sotnikova T.D., Beaulieu J.M., Barak L.S., Wetsel W.C., Caron M.G., Gainetdinov R.R. Dopamine-independent locomotor actions of amphetamines in a novel acute mouse model of Parkinson disease. PLoS Biol. 2005, 3(8):e271. (Aug).
59. Spencer J.P., Jenner P., Daniel S.E., Lees A.J., Marsden D.C., Halliwell B. Conjugates of catecholamines with cysteine and GSH in Parkinson's disease: possible mechanisms of formation involving reactive oxygen species. J. Neurochem. 1998, 71(5):2112-2122. (Nov).
60. Spencer J.P., Whiteman M., Jenner P., Halliwell B. 5-s-Cysteinyl-conjugates of catecholamines induce cell damage, extensive DNA base modification and increases in caspase-3 activity in neurons. J. Neurochem. 2002, 81(1):122-129. (Apr).
61. Stokes A.H., Hastings T., Vrana K.E. Cytotoxic and genotoxic potential of dopamine. J. Neurosci. Res. 1999, 55:659-665.
62. Sulzer D. Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci. 2007, 30:244-250.
63. Volkow N.D., Fowler J.S., Wang G., Swanson J.M., Telang F. Dopamine in drug abuse and addiction: results of imaging studies and treatment implications. Arch. Neurol. 2007, 64(11):1575-1579.
64. Yamaguchi H., Shen J. Absence of dopaminergic neuronal degeneration and oxidative damage in aged DJ-1-deficient mice. Mol. Neurodegener. 2007, 2-10.
65. Zhai D., Li S., Zhao Y., Lin Z. SLC6A3 is a risk factor for Parkinson's disease: a meta-analysis of sixteen years' studies. Neurosci. Lett. 2014, 3(564):99-104. (Apr).
66. Zhou Q.Y., Palmiter R.D. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 1995, 83:1197-1209.
67. Zigmond M.J., Hastings T.G., Perez R.G. Increased dopamine turnover after partial loss of dopaminergic neurons: compensation or toxicity?. Parkinsonism Relat. Disord. 2002, 8(6):389-393.