Enhanced striatal dopamine transmission and motor performance with LRRK2 overexpression in mice is eliminated by familial Parkinson's disease mutation G2019S

Journal of Neuroscience

Volumn 30, Issue 5, 2010, Pages 1788-1797

  Li, Xianting ^a   Patel, Jyoti C ^b   Wang, Jing ^a   Avshalumov, Marat V ^a,b   Nicholson, Charles ^b   Buxbaum, Joseph D ^a   Elder, Gregory A ^a,c   Rice, Margaret E ^b   Yue, Zhenyu ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; LEUCINE RICH REPEAT KINASE 2;

AGE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINE UPTAKE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; ENZYME ACTIVITY; FAMILIAL DISEASE; GENE; GENE MUTATION; HYPERACTIVITY; IN VITRO STUDY; LRRK2 GENE; MALE; MOTOR PERFORMANCE; MOUSE; MOUSE STRAIN; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRIATONIGRAL DEGENERATION; SUBSTANTIA NIGRA; TISSUE LEVEL; TRANSGENIC MOUSE; WILD TYPE;

AGING; ANIMALS; CORPUS STRIATUM; DOPAMINE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MOTOR SKILLS; MUTATION; PARKINSON DISEASE; PROTEIN-SERINE-THREONINE KINASES;

EID: 76149134717     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5604-09.2010     Document Type: Article

References (51)

1. Abeliovich A, Schmitz Y, Fariñas I, Choi-Lundberg D, Ho WH, Castillo PE, Shinsky N, Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, Rosenthal A (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25:239-252.
2. Adams JR, van Netten H, Schulzer M, Mak E, Mckenzie J, Strongosky A, Sossi V, Ruth TJ, Lee CS, Farrer M, Gasser T, Uitti RJ, Calne DB, Wszolek ZK, Stoessl AJ (2005) PET in LRRK2 mutations: comparison to sporadic Parkinson's disease and evidence for presymptomatic compensation. Brain 128:2777-2785.
3. 2. J Neurosci 23:2744-2750.
4. Avshalumov MV, Patel JC, Rice ME (2008) AMPA receptor-dependent H2O2 generation in striatal medium spiny neurons but not dopamine axons: one source of a retrograde signal that can inhibit dopamine release. J Neurophysiol 100:1590-1601.
5. Bosgraaf L, Van Haastert PJ (2003) Roc, a Ras/GTPase domain in complex proteins. Biochim Biophys Acta 1643:5-10.
6. Chen BT, Moran KA, Avshalumov MV, Rice ME (2006) Limited regulation of somatodendritic dopamine release by voltage-sensitive Ca channels contrasted with strong regulation of axonal dopamine release. J Neurochem 96:645- 655.
7. Chen L, Cagniard B, Mathews T, Jones S, Koh HC, Ding Y, Carvey PM, Ling Z, Kang UJ, Zhuang X (2005) Age-dependent motor deficits and dopaminergic dysfunction in DJ-1 null mice. J Biol Chem 280:21418-21426.
8. Fleming SM, Salcedo J, Fernagut PO, Rockenstein E, Masliah E, Levine MS, Chesselet MF (2004) Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J Neurosci 24:9434-9440.
9. Gloeckner CJ, Kinkl N, Schumacher A, Braun RJ, O'Neill E, Meitinger T, Kolch W, Prokisch H, Ueffing M (2006) The Parkinson disease causing LRRK2 mutation I2020T is associated with increased kinase activity.Hum Mol Genet 15:223-232.
10. Goldberg MS, Fleming SM, Palacino JJ, Cepeda C, Lam HA, Bhatnagar A, Meloni EG, Wu N, Ackerson LC, Klapstein GJ, Gajendiran M, Roth BL, Chesselet MF, Maidment NT, Levine MS, Shen J (2003) Parkindeficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem 278:43628-43635.
11. Greggio E, CooksonMR (2009) Leucine-rich repeat kinase 2 mutations and Parkinson's disease: three questions. ASN Neuro 1:e00002.
12. Greggio E, Jain S, Kingsbury A, Bandopadhyay R, Lewis P, Kaganovich A, van der Brug MP, Beilina A, Blackinton J, Thomas KJ, Ahmad R, Miller DW, Kesavapany S, Singleton A, Lees A, Harvey RJ, Harvey K, Cookson MR (2006) Kinase activity is required for the toxic effects of mutant LRRK2/ dardarin. Neurobiol Dis 23:329-341.
13. Guo L, Gandhi PN, Wang W, Petersen RB, Wilson-Delfosse AL, Chen SG (2007) The Parkinson's disease-associated protein, leucine-rich repeat kinase 2 (LRRK2), is an authentic GTPase that stimulates kinase activity. Exp Cell Res 313:3658-3670.
14. Hatano T, Kubo S, Imai S, Maeda M, Ishikawa K, Mizuno Y, Hattori N (2007) Leucine-rich repeat kinase 2 associates with lipid rafts. Hum Mol Genet 16:678-690.
15. Healy DG, Falchi M, O'Sullivan SS, Bonifati V, Durr A, Bressman S, Brice A, Aasly J, Zabetian CP, Goldwurm S, Ferreira JJ, Tolosa E, Kay DM, Klein C, Williams DR, Marras C, Lang AE, Wszolek ZK, Berciano J, Schapira AH, et al. (2008) Phenotype, genotype, and worldwide genetic penetrance of LRRK2-associated Parkinson's disease: a case-control study. Lancet Neurol 7:583-590.
16. Heintz N (2001) BAC to the future: the use of bac transgenic mice for neuroscience research. Nat Rev Neurosci 2:861- 870.
17. Imai Y, Gehrke S, Wang HQ, Takahashi R, Hasegawa K, Oota E, Lu B (2008) Phosphorylation of 4E-BP by LRRK2 affects the maintenance of dopaminergic neurons in Drosophila. EMBO J 27:2432-2443.
18. Ito G, Okai T, Fujino G, Takeda K, Ichijo H, Katada T, Iwatsubo T (2007) GTP binding is essential to the protein kinase activity of LRRK2, a causative gene product for familial Parkinson's disease. Biochemistry 46:1380-1388.
19. Jaleel M, Nichols RJ, Deak M, Campbell DG, Gillardon F, Knebel A, AlessiDR (2007) LRRK2 phosphorylates moesin at threonine-558: characterization of how Parkinson's disease mutants affect kinase activity. Biochem J 405:307-317.
20. John CE, Jones SR (2007) Voltammetric characterization of the effect of monoamine uptake inhibitors and releasers on dopamine and serotonin uptake in mouse caudate-putamen and substantia nigra slices. Neuropharmacology 52:1596-1605.
21. Jones SR, Gainetdinov RR, Jaber M, Giros B, Wightman RM, Caron MG (1998) Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc Natl Acad Sci U S A 95:4029-4034.
22. Kennedy RT, Jones SR, Wightman RM (1992) Dynamic observation of dopamine autoreceptor effects in rat striatal slices. J Neurochem 59:449- 455.
23. Khan HA (2004) Analytical characterization of a sensitive radioassay for tyrosine hydroxylase activity in rodent striatum. Neurochem Res 29:1467-1472.
24. Kitada T, Pisani A, Porter DR, Yamaguchi H, Tscherter A, Martella G, Bonsi P, Zhang C, Pothos EN, Shen J (2007) Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A 104:11441-11446.
25. Lee SB, Kim W, Lee S, Chung J (2007) Loss of LRRK2/PARK8 induces degeneration of dopaminergic neurons in Drosophila. Biochem Biophys Res Commun 358:534-539.
26. Li X, Tan YC, Poulose S, Olanow CW, Huang XY, Yue Z (2007) Leucinerich repeat kinase 2 (LRRK2)/PARK8 possesses GTPase activity that is altered in familial Parkinson's disease R1441C/G mutants. J Neurochem 103:238-247.
27. Li Y, Liu W, Oo TF, Wang L, Tang Y, Jackson-Lewis V, Zhou C, Geghman K, Bogdanov M, Przedborski S, Beal MF, Burke RE, Li C (2009) Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat Neurosci 12:826-828.
28. Limberger N, Trout SJ, Kruk ZL, Starke K (1991) "Real time" measurement of endogenous dopamine release during short trains of pulses in slices of rat neostriatum and nucleus accumbens: role of autoinhibition. Naunyn Schmiedebergs Arch Pharmacol 344:623- 629.
29. Liu Z, Wang X, Yu Y, Li X, Wang T, Jiang H, Ren Q, Jiao Y, Sawa A, Moran T, Ross CA, Montell C, SmithWW (2008) A Drosophila model for LRRK2-linked parkinsonism. Proc Natl Acad Sci U S A 105:2693-2698.
30. MacLeod D, Dowman J, Hammond R, Leete T, Inoue K, AbeliovichA (2006) The familial Parkinsonism gene LRRK2 regulates neurite process morphology. Neuron 52:587-593.
31. Nandhagopal R, Mak E, Schulzer M, McKenzie J, McCormick S, Sossi V, Ruth TJ, Strongosky A, Farrer MJ, Wszolek ZK, Stoessl AJ (2008) Progression of dopaminergic dysfunction in a LRRK2 kindred: a multitracer PET study. Neurology 71:1790-1795.
32. Ng CH, Mok SZ, Koh C, Ouyang X, Fivaz ML, Tan EK, Dawson VL, Dawson TM, Yu F, Lim KL (2009) Parkin protects against LRRK2 G2019S mutant-induced dopaminergic neurodegeneration in Drosophila. J Neurosci 29:11257-11262.
33. Nicholson C (1995) Interaction between diffusion and Michaelis-Menten uptake of dopamine after iontophoresis in striatum. Biophys J 68:1699-1715.
34. Paisán-Ruíz C, Jain S, Evans EW, Gilks WP, Simón J, van der Brug M, López de Munain A, Aparicio S, Gil AM, Khan N, Johnson J, Martinez JR, Nicholl D, Carrera IM, Pena AS, de Silva R, Lees A, Martí-Massó JF, Pérez-Tur J, Wood NW, et al. (2004) Cloning of the gene containing mutations that cause PARK8-linked Parkinson's disease. Neuron 44:595- 600.
35. Patel J, Trout SJ, Kruk ZL (1992) Regional differences in evoked dopamine efflux in brain slices of rat anterior and posterior caudate putamen. Naunyn Schmiedebergs Arch Pharmacol 346:267-276.
36. Patel JC, Witkovsky P, Avshalumov MV, Rice ME (2009) Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J Neurosci 29:6568-6579.
37. Phillips PE, Hancock PJ, Stamford JA (2002) Time window of autoreceptor-mediated inhibition of limbic and striatal dopamine release. Synapse 44:15-22.
38. Sakaguchi-Nakashima A, Meir JY, Jin Y, Matsumoto K, Hisamoto N (2007) LRK-1, a C. elegans PARK8-related kinase, regulates axonal-dendritic polarity of SV proteins. Curr Biol 17:592-598.
39. Schmitz Y, Lee CJ, Schmauss C, Gonon F, Sulzer D (2001) Amphetamine distorts stimulation-dependent dopamine overflow: effects on D2 autoreceptors, transporters, and synaptic vesicle stores. J Neurosci 21:5916-5924.
40. Schönfuss D, Reum T, Olshausen P, Fischer T, Morgenstern R (2001) Modelling constant potential amperometry for investigations of dopaminergic neurotransmission kinetics in vivo. J Neurosci Methods 112:163-172.
41. SmithWW,Pei Z, Jiang H, Moore DJ, Liang Y, West AB, Dawson VL, Dawson TM, Ross CA (2005) Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration. Proc Natl Acad Sci U S A 102:18676-18681.
42. Smith WW, Pei Z, Jiang H, Dawson VL, Dawson TM, Ross CA (2006) Kinase activity of mutant LRRK2 mediates neuronal toxicity. Nat Neurosci 9:1231-1233.
43. Tong Y, Pisani A, Martella G, Karouani M, Yamaguchi H, Pothos EN, Shen J (2009) R1441C mutation in LRRK2 impairs dopaminergic neurotransmission in mice. Proc Natl Acad Sci U S A 106:14622-14627.
44. Wang D, Tang B, Zhao G, Pan Q, Xia K, Bodmer R, Zhang Z (2008) Dispensable role of Drosophila ortholog of LRRK2 kinase activity in survival of dopaminergic neurons. Mol Neurodegener 3:3.
45. West AB, Moore DJ, Biskup S, Bugayenko A, Smith WW, Ross CA, Dawson VL, Dawson TM (2005) Parkinson's disease-associated mutations in leucine-rich repeat kinase 2 augment kinase activity. Proc Natl Acad Sci U S A 102:16842-16847.
46. West AB, Moore DJ, Choi C, Andrabi SA, Li X, Dikeman D, Biskup S, Zhang Z, Lim KL, Dawson VL, Dawson TM (2007) Parkinson's disease-associated mutations in LRRK2 link enhanced GTP-binding and kinase activities to neuronal toxicity. Hum Mol Genet 16:223-232.
47. Wolozin B, Saha S, Guillily M, Ferree A, Riley M (2008) Investigating convergent actions of genes linked to familial Parkinson's disease. Neurodegener Dis 5:182-185.
48. Wu Q, Reith ME, Wightman RM, Kawagoe KT, Garris PA (2001) Determination of release and uptake parameters from electrically evoked dopamine dynamics measured by real-time voltammetry. J Neurosci Methods 112:119-133.
49. Zhou W, Milder JB, Freed CR (2008) Transgenic mice overexpressing tyrosine-to-cysteine mutant human alpha-synuclein: a progressive neurodegenerative model of diffuse Lewy body disease. J Biol Chem 283: 9863-9870.
50. Zigmond MJ, Abercrombie ED, Berger TW, Grace AA, Stricker EM (1990) Compensations after lesions of central dopaminergic neurons: some clinical and basic implications. Trends Neurosci 13:290-296.
51. Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, Kachergus J, Hulihan M, Uitti RJ, Calne DB, Stoessl AJ, Pfeiffer RF, Patenge N, Carbajal IC, Vieregge P, Asmus F,Müller-Myhsok B, Dickson DW, Meitinger T, Strom TM, et al. (2004) Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44:601-607.