Gene expression analyses identify narp contribution in the development of L-DOPA-induced dyskinesia

Journal of Neuroscience

Volumn 35, Issue 1, 2015, Pages 96-111

  Charbonnier Beaupel, Fanny ^a,b,c   Malerbi, Marion ^a,b,c,d,e   Alcacer, Cristina ^a,d,e   Tahiri, Khadija ^a,b,c   Carpentier, Wassila ^a   Wang, Chuansong ^f   During, Matthew ^f   Xu, Desheng ^g   Worley, Paul F ^g   Girault, Jean Antoine ^a,d,e   Herve, Denis ^d,e   Corvol, Jean Christophe ^a,b,c  

^a SORBONNE UNIVERSITÉ   (France)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c CNRS   (France)

^d INSERM   (France)

^e INSTITUT DU FER À MOULIN   (France)

^f OHIO STATE UNIVERSITY   (United States)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

L DOPA induced dyskinesia; Narp; Parkinson s disease; Transcriptome

Indexed keywords

BENSERAZIDE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIMETHYL SULFOXIDE; FLUNIXIN MEGLUMINE; GLUTAMATE RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; NEURONAL PENTRAXIN II; PARVOVIRUS VECTOR; PEPTIDES AND PROTEINS; PHOSPHOPROTEIN DARPP 32; PHOSPHOPROTEIN PHOSPHATASE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; ANTIPARKINSON AGENT; C REACTIVE PROTEIN; LEVODOPA; NERVE PROTEIN; NEURONAL PENTRAXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MAPPING; CONTROLLED STUDY; CORPUS STRIATUM; CYLINDER TEST; DISEASE SEVERITY; DNA MICROARRAY; DOWN REGULATION; DYSKINESIA; ENZYME ACTIVITY; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; GENE; GENE EXPRESSION; GENE ONTOLOGY; IMMUNOREACTIVITY; INTRACELLULAR SIGNALING; L DOPA INDUCED DYSKINESIA; MALE; MOUSE; NONHUMAN; POSTOPERATIVE CARE; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA PROCESSING; SYNAPTIC TRANSMISSION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; TOXICITY;

ANIMALS; ANTIPARKINSON AGENTS; C-REACTIVE PROTEIN; DYSKINESIA, DRUG-INDUCED; FEMALE; GENE EXPRESSION REGULATION; LEVODOPA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS;

EID: 84920517665     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5231-13.2015     Document Type: Article

References (70)

1. Alcacer C, Santini E, Valjent E, Gaven F, Girault JA, Herve D (2012) Ga(olf)muta-tion allows parsing the role of cAMP-dependent and extracellular signal-regulated kinase-dependent signaling in L-34-dihydroxyphenylalanine-induced dyskinesia. J Neurosci 32:5900–5910.
2. Andersson M, Hilbertson A, Cenci MA (1999) Striatal fosB expression is causally linked with l-DOPA-induced abnormal involuntary movements and the associated upregulation of striatal prodynorphin mRNA in a rat model of Parkinson’s disease. Neurobiol Dis 6:461–474.
3. Andersson M, Westin JE, Cenci MA (2003) Time course of striatal DeltaFosB-like immunoreactivity and prodynorphin mRNA levels after discontinuation of chronic dopaminomimetic treatment. Eur J Neurosci 17:661–666.
4. Aubert I, Guigoni C, Håkansson K, Li Q, Dovero S, Barthe N, Bioulac BH, Gross CE, Fisone G, Bloch B, Bezard E (2005) Increased D1 dopamine receptor signalingin levodopa-induced dyskinesia. Ann Neurol 57:17–26.
5. Bateup HS, Santini E, Shen W, Birnbaum S, Valjent E, Surmeier DJ, Fisone G, Nestler EJ, Greengard P (2010) Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci U S A 107:14845–14850.
6. Berke JD, Paletzki RF, Aronson GJ, Hyman SE, Gerfen CR (1998) A complex program of striatal gene expression induced by dopaminergic stimulation. J Neurosci 18:5301–5310.
7. Berthet A, Bezard E, Porras G, Fasano S, Barroso-Chinea P, Dehay B, Martinez A, Thiolat ML, Nosten-Bertrand M, Giros B, Baufreton J, Li Q, Bloch B, Martin-Negrier ML (2012) L-DOPA impairs proteasome activity in parkinsonism through D1 dopamine receptor. J Neurosci 32:681–691.
8. Berton O, Guigoni C, Li Q, Bioulac BH, Aubert I, Gross CE, Dileone RJ, Nestler EJ, Bezard E (2009) Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 66:554–561.
9. Bjartmar L, Huberman AD, Ullian EM, Rentería RC, Liu X, Xu W, Prezioso J, Susman MW, Stellwagen D, Stokes CC, Cho R, Worley P, Malenka RC, Ball S, Peachey NS, Copenhagen D, Chapman B, Nakamoto M, Barres BA, Perin MS (2006) Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 26:6269–6281.
10. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, Greengard P (2000) Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20:8443–8451.
11. Calabresi P, Picconi B, Tozzi A, Di Filippo M (2007) Dopamine-mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci 30:211-219.
12. Calon F, Hadj Tahar A, Blanchet PJ, Morissette M, Grondin R, Goulet M, Doucet JP, Robertson GS, Nestler E, Di Paolo T, Bédard PJ (2000) Dopamine-receptor stimulation: biobehavioral and biochemical consequences. Trends Neurosci 23:S92–S100.
13. Cao X, Yasuda T, Uthayathas S, Watts RL, Mouradian MM, Mochizuki H, Papa SM (2010) Striatal overexpression of DeltaFosB reproduces chronic levodopa-induced involuntary movements. J Neurosci 30:7335-7343.
14. Cenci MA, Konradi C (2010) Maladaptive striatal plasticity in L-DOPA-induced dyskinesia. Prog Brain Res 183:209–233.
15. Cenci MA, Tranberg A, Andersson M, Hilbertson A (1999) Changes in the regional and compartmental distribution of FosB- and JunB-like immu-noreactivity induced inthe dopamine-denervated rat striatum byacute or chronic L-DOPA treatment. Neuroscience 94:515–527.
16. Cerovic M, Bagetta V, Pendolino V, Ghiglieri V, Fasano S, Morella I, Hardingham N, Heuer A, Papale A, Marchisella F, Giampà C, Calabresi P, Picconi B, Brambilla R (2014) Derangement of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and extracellular signal-regulated kinase (ERK) dependent striatal plasticity in L-DOPA-induced dyskinesia. Biol Psychiatry. Advance online publication. doi:10.1016/j.biopsych.2014.04.002.
17. Chang MC, Park JM, Pelkey KA, Grabenstatter HL, Xu D, Linden DJ, Sutula TP, McBain CJ, Worley PF (2010) Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons. Nat Neu-rosci 13:1090–1097.
18. Cho RW, Park JM, Wolff SB, Xu D, Hopf C, Kim JA, Reddy RC, Petralia RS, Perin MS, Linden DJ, Worley PF (2008) mGluR1/5-dependent long-term depression requires the regulated ectodomain cleavage of neuronal pentraxin NPR by TACE. Neuron 57:858–871.
19. Corvol JC, Muriel MP, Valjent E, Féger J, Hanoun N, Girault JA, Hirsch EC, Hervé D (2004) Persistent increase in olfactory type G-protein alpha subunit levels may underlie D1 receptor functional hypersensitivity in Parkinson disease. J Neurosci 24:7007–7014.
20. Darmopil S, Muñetón-Gómez VC, de Ceballos ML, Bernson M, Moratalla R (2008) Tyrosine hydroxylase cells appearing in the mouse striatum afterdopamine denervation are likely to be projection neurones regulated by L-DOPA. Eur J Neurosci 27:580–592.
21. Darmopil S, Martín AB, De Diego IR, Ares S, Moratalla R (2009) Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol Psychiatry 66:603–613.
22. Ding Y, Won L, Britt JP, Lim SA, McGehee DS, Kang UJ (2011) Enhanced striatal cholinergic neuronal activity mediates L-DOPA-induced dyskine-sia in parkinsonian mice. Proc Natl Acad Sci U S A 108:840–845.
23. During MJ, Young D, Baer K, Lawlor P, Klugmann M (2003) Development and optimization of adeno-asssociated virus vector transfer into the central nervous system. Methods Mol Med 76:221–236.
24. Duvoisin RC (1974) Variations in the “on-off” phenomenon. Adv Neurol 5:339–340.
25. El Atifi-Borel M, Buggia-Prevot V, Platet N, Benabid AL, Berger F, Sgambato-Faure V (2009) De novo and long-term l-Dopa induce both common and distinct striatal gene profiles in the hemiparkinsonian rat. Neurobiol Dis 34:340–350.
26. Fasano S, Bezard E, D’Antoni A, Francardo V, Indrigo M, Qin L, Doveró S, Cerovic M, Cenci MA, Brambilla R (2010) Inhibition of Ras-guanine nucleotide-releasing factor 1(Ras-GRF1) signalingin the striatum reverts motor symptoms associated with L-DOPA-induced dyskinesia. Proc Natl Acad Sci U S A 107:21824–21829.
27. Francardo V, Recchia A, Popovic N, Andersson D, Nissbrandt H, Cenci MA (2011) Impact of the lesion procedure on the profiles of motor impairment and molecular responsiveness to L-DOPA in the 6-hydroxydopamine mouse model of Parkinson’s disease. Neurobiol Dis 42:327–340.
28. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ Jr, Sibley DR (1990) D1 and D2 dopamine receptor-regulated gene expression of stria-tonigral and striatopallidal neurons. Science 250:1429–1432.
29. Gerfen CR, Miyachi S, Paletzki R, Brown P (2002) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2/MAP kinase. J Neurosci 22:5042–5054.
30. Gerfen CR, Paletzki R, Worley P (2008) Differences between dorsal and ventral striatum in Drd1a dopamine receptor coupling of dopamine- and cAMP-regulated phosphoprotein-32 to activation of extracellular signal-regulated kinase. J Neurosci 28:7113–7120.
31. Green CB, Douris N, Kojima S, Strayer CA, Fogerty J, Lourim D, Keller SR, Besharse JC (2007) Nocturnin, a circadian deadenylase, confers resistance to hepatic steatosis and diet-induced obesity. Proc Natl Acad Sci U S A 104:9888–9893.
32. Harvey KF, Kumar S (1999) Nedd4-like proteins: an emerging family of ubiquitin-protein ligases implicated in diverse cellular functions. Trends Cell Biol 9:166–169.
33. Heiman M, Heilbut A, Francardo V, Kulicke R, Fenster RJ, Kolaczyk ED, Mesirov JP, Surmeier DJ, Cenci MA, Greengard P (2014) Molecular adaptations of striatal spiny projection neurons during levodopa-induced dyskinesia. Proc Natl Acad Sci U S A 111:4578–4583.
34. Hervé D, Lévi-Strauss M, Marey-Semper I, Verney C, Tassin JP, Glowinski J, Girault JA (1993) G(olf) and Gs in rat basal ganglia: possible involvement of G(olf) in the coupling of dopamine D1 receptor with adenylyl cyclase. J Neurosci 13:2237–2248.
35. Huangda W, Sherman BT, Lempicki RA (2009a) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4:44–57.
36. Huang da W, Sherman BT, Lempicki RA (2009b) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13.
37. Huot P, Lévesque M, Parent A (2007) The fate of striatal dopaminergic neurons in Parkinson’s disease and Huntington’s chorea. Brain 130:222-232.
38. Jenner P (2008) Molecular mechanisms of L-DOPA-induced dyskinesia. Nat Rev Neurosci 9:665–677.
39. Kobylecki C, Cenci MA, Crossman AR, Ravenscroft P (2010) Calcium-permeable AMPA receptors are involved in the induction and expression of l-DOPA-induced dyskinesia in Parkinson’s disease. J Neurochem 114: 499–511.
40. Kreitzer AC, Malenka RC (2007) Endocannabinoid-mediated rescueofstri-atal LTD and motor deficits in Parkinson’s disease models. Nature 445: 643–647.
41. Lebel M, Chagniel L, Bureau G, Cyr M (2010) Striatal inhibition of PKA prevents levodopa-induced behavioural and molecular changes in the hemiparkinsonian rat. Neurobiol Dis 38:59–67.
42. Lindgren HS, Ohlin KE, Cenci MA (2009) Differential involvement of D1 and D2 dopamine receptors in L-DOPA-induced angiogenic activity in a rat model of Parkinson’s disease. Neuropsychopharmacology 34:2477-2488.
43. Lundblad M, Andersson M, Winkler C, Kirik D, Wierup N, Cenci MA (2002) Pharmacological validation of behavioural measures of akinesia and dys-kinesia in a rat model of Parkinson’s disease. Eur J Neurosci 15:120–132.
44. Lundblad M, Picconi B, Lindgren H, Cenci MA (2004) A model of L-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: rela-tiontomotor and cellular parametersof nigrostriatal function. Neurobiol Dis 16:110–123.
45. Lundblad M, Usiello A, Carta M, Håkansson K, Fisone G, Cenci MA (2005) Pharmacological validation of a mouse model of l-DOPA-induced dyski-nesia. Exp Neurol 194:66–75.
46. Meurers BH, Dziewczapolski G, Shi T, Bittner A, Kamme F, Shults CW (2009) Dopamine depletion induces distinct compensatory gene expression changes in DARPP-32 signal transduction cascades of striatonigral and striatopallidal neurons. J Neurosci 29:6828–6839.
47. Moran LB, Hickey L, Michael GJ, Derkacs M, Christian LM, Kalaitzakis ME, Pearce RK, Graeber MB (2008) Neuronal pentraxin II is highly upregu-lated in Parkinson’s disease and a novel component of Lewy bodies. Acta Neuropathol 115:471–478.
48. Nadjar A, Gerfen CR, Bezard E (2009) Priming for L-DOPA-induced dys-kinesia in Parkinson’s disease: a feature inherent to the treatment or the disease? Prog Neurobiol 87:1–9.
49. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, DeLong MR, Olanow CW (2000) Pathophysiology of levodopa-induced dyskinesias in Parkinson’s disease: problems with the current model. Ann Neurol 47:S22–S32; discussion S32–S34.
50. O’Brien R, Xu D, Mi R, Tang X, Hopf C, Worley P (2002) Synaptically targeted Narp plays an essential role in the aggregation of AMPA recep-torsatexcitatory synapsesin cultured spinal neurons. JNeurosci 22:4487-4498.
51. Pacchioni AM, Kalivas PW (2009a) The role of AMPAR trafficking mediated by neuronal pentraxins in cocaine-induced neuroadaptations. Mol Cell Pharmacol 1:183–192.
52. Pacchioni AM, Vallone J, Worley PF, Kalivas PW (2009b) Neuronal pen-traxins modulate cocaine-induced neuroadaptations. J Pharmacol Exp Ther 328:183–192.
53. Pavón N, Martín AB, Mendialdua A, Moratalla R (2006) ERK phosphorylation and FosB expression are associated with L-DOPA-induced dyskinesia in hemiparkinsonian mice. Biol Psychiatry 59:64–74.
54. Paxinos G, Franklin KBJ (2001) The mouse brainin stereotaxic coordinates, Ed 2. San Diego: Academic.
55. Picconi B, Centonze D, Håkansson K, Bernardi G, Greengard P, Fisone G, Cenci MA, Calabresi P (2003) Loss ofbidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 6:501–506.
56. Putterman DB, Munhall AC, Kozell LB, Belknap JK, Johnson SW (2007) Evaluation of levodopa dose and magnitude of dopamine depletion as risk factors for levodopa-induced dyskinesia in a rat model of Parkinson’s disease. J Pharmacol Exp Ther 323:277–284.
57. Rangel-Barajas C, Silva I, Lopéz-Santiago LM, Aceves J, Erlij D, Florán B (2011) L-DOPA-induced dyskinesia in hemiparkinsonian rats is associated with up-regulation of adenylyl cyclase type V/VI and increased GABA release in the substantia nigra reticulata. Neurobiol Dis 41:51–61.
58. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378.
59. Santini E, Valjent E, Usiello A, Carta M, Borgkvist A, Girault JA, Hervé D, Green-gard P, Fisone G (2007) Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J Neurosci 27:6995–7005.
60. Santini E, Alcacer C, Cacciatore S, Heiman M, Hervé D, Greengard P, Girault JA, Valjent E, Fisone G (2009a) L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J Neurochem 108:621–633.
61. Santini E, Heiman M, Greengard P, Valjent E, Fisone G (2009b) Inhibition of mTOR signaling in Parkinson’s disease prevents L-DOPA-induced dyskinesia. Sci Signal 2:ra36.
62. Santini E, Sgambato-Faure V, Li Q, Savasta M, Dovero S, Fisone G, Bezard E (2010) Distinct changes in cAMP and extracellular signal-regulated protein kinase signalling in L-DOPA-induced dyskinesia. PLoS One 5:e12322.
63. Santini E, Feyder M, Gangarossa G, Bateup HS, Greengard P, Fisone G (2012) Dopamine-and cAMP-regulated phosphoprotein of 32-kDa (DARPP-32)-dependent activation of extracellular signal-regulated kinase (ERK) and mammalian target of rapamycin complex 1 (mTORC1) signaling in experimental parkinsonism. J Biol Chem 287:27806–27812.
64. Schuster S, Nadjar A, Guo JT, Li Q, Ittrich C, Hengerer B, Bezard E (2008) The 3-hydroxy-3-methylglutaryl-CoA reductase inhibitor lovastatin reduces severity of L-DOPA-induced abnormal involuntary movements in experimental Parkinson’s disease. J Neurosci 28:4311–4316.
65. Shen W, Flajolet M, Greengard P, Surmeier DJ (2008) Dichotomous dopa-minergic control of striatal synaptic plasticity. Science 321:848–851.
66. Tashiro Y, Sugimoto T, Hattori T, Uemura Y, Nagatsu I, Kikuchi H, Mizuno N (1989) Tyrosine hydroxylase-like immunoreactive neurons in the striatum of the rat. Neurosci Lett 97:6–10.
67. Tsui CC, Copeland NG, Gilbert DJ, Jenkins NA, Barnes C, Worley PF (1996) Narp, a novel member of the pentraxin family, promotes neurite outgrowth and is dynamically regulated by neuronal activity. J Neurosci 16: 2463–2478.
68. Valjent E, Pascoli V, Svenningsson P, Paul S, Enslen H, Corvol JC, Stipanov-ich A, Caboche J, Lombroso PJ, Nairn AC, Greengard P, Herve´ D, Girault JA (2005) Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci U S A 102:491–496.
69. Westin JE, Vercammen L, Strome EM, Konradi C, Cenci MA (2007) Spa-tiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPA-induced dyskinesia and the role of dopamine D1 receptors. Biol Psychiatry 62:800–810.
70. Xu D, Hopf C, Reddy R, Cho RW, Guo L, Lanahan A, Petralia RS, Wenthold RJ, O’Brien RJ, Worley P (2003) Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity. Neuron 39:513–528.