Selective Inactivation of Striatal FosB/ΔFosB-Expressing Neurons Alleviates L-DOPA–Induced Dyskinesia

Biological Psychiatry

Volumn 79, Issue 5, 2016, Pages 354-361

  Engeln, Michel ^a,b   Bastide, Matthieu F ^a,b   Toulmé, Estelle ^a,b   Dehay, Benjamin ^a,b   Bourdenx, Mathieu ^a,b   Doudnikoff, Evelyne ^a,b   Li, Qin ^c   Gross, Christian E ^a,b   Boué Grabot, Eric ^a,b   Pisani, Antonio ^d   Bezard, Erwan ^a,b   Fernagut, Pierre Olivier ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CNRS   (France)

^c INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

^d IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Daun02; Dyskinesia; Electrophysiology; FosB; Monkey; Parkinson's disease

Indexed keywords

BETA GALACTOSIDASE; DOPAMINE 1 RECEPTOR; LEVODOPA; TRANSCRIPTION FACTOR DELTA FOSB; TRANSCRIPTION FACTOR FOSB; ANTIPARKINSON AGENT; DAUNORUBICIN; N-(4''-(GALACTOPYRANOSYL)-3''-NITROBENZYLOXYCARBONYL)DAUNOMYCIN; OXIDOPAMINE; PROTEIN C FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCLING BEHAVIOR; CONTROLLED STUDY; DISEASE MARKER; DISEASE SEVERITY; LEVODOPA-INDUCED DYSKINESIA; MALE; MEMBRANE STEADY POTENTIAL; MONKEY MODEL; NERVE CELL DIFFERENTIATION; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; THERAPY EFFECT; ANALOGS AND DERIVATIVES; ANIMAL; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; DYSKINESIA, DRUG-INDUCED; MACACA FASCICULARIS; METABOLISM; NEOSTRIATUM; NERVE CELL; PARKINSON DISEASE; PATCH CLAMP TECHNIQUE; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIPARKINSON AGENTS; DAUNORUBICIN; DISEASE MODELS, ANIMAL; DYSKINESIA, DRUG-INDUCED; LEVODOPA; MACACA FASCICULARIS; MALE; NEOSTRIATUM; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; PATCH-CLAMP TECHNIQUES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1;

EID: 84905889160     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.07.007     Document Type: Article

References (56)

1. 1 Bezard, E., Brotchie, J.M., Gross, C.E., Pathophysiology of levodopa-induced dyskinesia: Potential for new therapies. Nat Rev Neurosci 2 (2001), 577–588.
2. 2 Jenner, P., Molecular mechanisms of L-DOPA-induced dyskinesia. Nat Rev Neurosci 9 (2008), 665–677.
3. 3 Cenci, M.A., Tranberg, A., Andersson, M., Hilbertson, A., Changes in the regional and compartmental distribution of FosB- and JunB-like immunoreactivity induced in the dopamine-denervated rat striatum by acute or chronic L-dopa treatment. Neuroscience 94 (1999), 515–527.
4. 4 Berton, O., Guigoni, C., Li, Q., Bioulac, B.H., Aubert, I., Gross, C.E., et al. Striatal overexpression of DeltaJunD resets L-DOPA-induced dyskinesia in a primate model of Parkinson disease. Biol Psychiatry 66 (2009), 554–561.
5. 5 Andersson, M., Hilbertson, A., Cenci, M.A., 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 (1999), 461–474.
6. 6 Porras, G., Berthet, A., Dehay, B., Li, Q., Ladepeche, L., Normand, E., et al. PSD-95 expression controls L-DOPA dyskinesia through dopamine D1 receptor trafficking. J Clin Invest 122 (2012), 3977–3989.
7. 7 Fasano, S., Bezard, E., D'Antoni, A., Francardo, V., Indrigo, M., Qin, L., et al. Inhibition of Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) signaling in the striatum reverts motor symptoms associated with L-dopa-induced dyskinesia. Proc Natl Acad Sci U S A 107 (2010), 21824–21829.
8. 8 Ahmed, M.R., Berthet, A., Bychkov, E., Porras, G., Li, Q., Bioulac, B.H., et al. Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med, 2, 2010, 28ra28.
9. 9 Santone, K.S., Oakes, S.G., Taylor, S.R., Powis, G., Anthracycline-induced inhibition of a calcium action potential in differentiated murine neuroblastoma cells. Cancer Res 46 (1986), 2659–2664.
10. 10 Koya, E., Golden, S.A., Harvey, B.K., Guez-Barber, D.H., Berkow, A., Simmons, D.E., et al. Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat Neurosci 12 (2009), 1069–1073.
11. 11 Bossert, J.M., Stern, A.L., Theberge, F.R., Cifani, C., Koya, E., Hope, B.T., Shaham, Y., Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat Neurosci 14 (2011), 420–422.
12. 12 Fanous, S., Goldart, E.M., Theberge, F.R., Bossert, J.M., Shaham, Y., Hope, B.T., Role of orbitofrontal cortex neuronal ensembles in the expression of incubation of heroin craving. J Neurosci 32 (2012), 11600–11609.
13. 13 Coulon, V., Chebli, K., Cavelier, P., Blanchard, J.M., A novel mouse c-fos intronic promoter that responds to CREB and AP-1 is developmentally regulated in vivo. PloS One, 5, 2010, e11235.
14. 14 Martin-Negrier, M.L., Charron, G., Bloch, B., Receptor recycling mediates plasma membrane recovery of dopamine D1 receptors in dendrites and axons after agonist-induced endocytosis in primary cultures of striatal neurons. Synapse 60 (2006), 194–204.
15. 15 Sciamanna, G., Bonsi, P., Tassone, A., Cuomo, D., Tscherter, A., Viscomi, M.T., et al. Impaired striatal D2 receptor function leads to enhanced GABA transmission in a mouse model of DYT1 dystonia. Neurobiol Dis 34 (2009), 133–145.
16. 16 Berthet, A., Bezard, E., Porras, G., Fasano, S., Barroso-Chinea, P., Dehay, B., et al. L-DOPA impairs proteasome activity in parkinsonism through D1 dopamine receptor. J Neurosci 32 (2012), 681–691.
17. 17 Berthet, A., Porras, G., Doudnikoff, E., Stark, H., Cador, M., Bezard, E., Bloch, B., Pharmacological analysis demonstrates dramatic alteration of D1 dopamine receptor neuronal distribution in the rat analog of L-DOPA-induced dyskinesia. J Neurosci 29 (2009), 4829–4835.
18. 18 Bastide, M.F., Dovero, S., Charron, G., Porras, G., Gross, C.E., Fernagut, P.O., Bézard, E., Immediate-early gene expression in structures outside the basal ganglia is associated to l-DOPA-induced dyskinesia. Neurobiol Dis 62 (2014), 179–192.
19. 19 Paxinos, G., Watson, C., The Rat Brain in Stereotaxic Coordinates, 6th ed., 2009, Elsevier, San Diego.
20. 20 Olsson, M., Nikkhah, G., Bentlage, C., Bjorklund, A., Forelimb akinesia in the rat Parkinson model: Differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15 (1995), 3863–3875.
21. 21 Cenci, M.A., Lee, C.S., Bjorklund, A., L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur J Neurosci 10 (1998), 2694–2706.
22. 22 Charron, G., Doudnikoff, E., Laux, A., Berthet, A., Porras, G., Canron, M.H., et al. Endogenous morphine-like compound immunoreactivity increases in parkinsonism. Brain 134 (2011), 2321–2338.
23. 23 Bezard, E., Dovero, S., Prunier, C., Ravenscroft, P., Chalon, S., Guilloteau, D., et al. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J Neurosci 21 (2001), 6853–6861.
24. 24 Boraud, T., Bezard, E., Bioulac, B., Gross, C., Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alteration of pallidal neurons in the MPTP-treated monkey. Brain 124 (2001), 546–557.
25. 25 Bezard, E., Boraud, T., Bioulac, B., Gross, C., Involvement of the subthalamic nucleus in glutamatergic compensatory mechanisms. Eur J Neurosci 11 (1999), 2167–2170.
26. 26 Bezard, E., Boraud, T., Bioulac, B., Gross, C., Compensatory effects of glutamatergic inputs to the substantia nigra pars compacta in experimental parkinsonism. Neuroscience 81 (1997), 399–404.
27. 27 Fox, S.H., Johnston, T.H., Li, Q., Brotchie, J., Bezard, E., A critique of available scales and presentation of the Non-Human Primate Dyskinesia Rating Scale. Mov Disord 27 (2012), 1373–1378.
28. 28 Fernagut, P.O., Li, Q., Dovero, S., Chan, P., Wu, T., Ravenscroft, P., et al. Dopamine transporter binding is unaffected by L-DOPA administration in normal and MPTP-treated monkeys. PloS One, 5, 2010, e14053.
29. 29 Bourdenx, M., Nilsson, A., Wadensten, H., Falth, M., Li, Q., Crossman, A.R., et al. Abnormal structure-specific peptide transmission and processing in a primate model of Parkinson's disease and l-DOPA-induced dyskinesia. Neurobiol Dis 62 (2014), 307–312.
30. 30 Aubert, I., Guigoni, C., Li, Q., Dovero, S., Bioulac, B.H., Gross, C.E., et al. Enhanced preproenkephalin-B-derived opioid transmission in striatum and subthalamic nucleus converges upon globus pallidus internalis in L-dopa-induced dyskinesia. Biol Psychiatry 61 (2007), 836–844.
31. 31 Guigoni, C., Li, Q., Aubert, I., Dovero, S., Bioulac, B.H., Bloch, B., et al. Involvement of sensorimotor, limbic, and associative basal ganglia domains in L-3,4-dihydroxyphenylalanine-induced dyskinesia. J Neurosci 25 (2005), 2102–2107.
32. 32 Engeln, M., Ahmed, S.H., Vouillac, C., Tison, F., Bezard, E., Fernagut, P.O., Reinforcing properties of Pramipexole in normal and parkinsonian rats. Neurobiol Dis 49C (2012), 79–86.
33. 33 Ajit, K., Ghosh, S.K., Marini, F., Nelson, J.A., Farquhar, D., A daunorubicin b-galactoside prodrug for use in conjunction with gene-directed enzyme prodrug therapy. Tetrahedron Letters 41 (2000), 4871–4874.
34. 34 Calabresi, P., Misgeld, U., Dodt, H.U., Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity. Neuroscience 20 (1987), 293–303.
35. 35 Falk, T., Zhang, S., Erbe, E.L., Sherman, S.J., Neurochemical and electrophysiological characteristics of rat striatal neurons in primary culture. J Comp Neurol 494 (2006), 275–289.
36. 36 Kowalski, C., Crest, M., Vuillet, J., Pin, T., Gola, M., Nieoullon, A., Emergence of a synaptic neuronal network within primary striatal cultures seeded in serum-free medium. Neuroscience 64 (1995), 979–993.
37. 37 Saka, E., Elibol, B., Erdem, S., Dalkara, T., Compartmental changes in expression of c-Fos and FosB proteins in intact and dopamine-depleted striatum after chronic apomorphine treatment. Brain Res 825 (1999), 104–114.
38. 38 Hope, B.T., Nye, H.E., Kelz, M.B., Self, D.W., Iadarola, M.J., Nakabeppu, Y., et al. Induction of a long-lasting AP-1 complex composed of altered Fos-like proteins in brain by chronic cocaine and other chronic treatments. Neuron 13 (1994), 1235–1244.
39. 39 Cenci, M.A., Whishaw, I.Q., Schallert, T., Animal models of neurological deficits: How relevant is the rat?. Nat Rev Neurosci 3 (2002), 574–579.
40. 40 Darmopil, S., Martin, A.B., De Diego, I.R., Ares, S., Moratalla, R., Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol Psychiatry 66 (2009), 603–613.
41. 41 Rylander, D., Parent, M., O'Sullivan, S.S., Dovero, S., Lees, A.J., Bezard, E., et al. Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia. Ann Neurol 68 (2010), 619–628.
42. 42 Palfi, S., Gurruchaga, J.M., Ralph, G.S., Lepetit, H., Lavisse, S., Buttery, P.C., et al. Long-term safety and tolerability of ProSavin, a lentiviral vector-based gene therapy for Parkinson's disease: A dose escalation, open-label, phase 1/2 trial. Lancet 383 (2014), 1138–1146.
43. 43 Mitchell, I.J., Boyce, S., Sambrook, M.A., Crossman, A.R., A 2-deoxyglucose study of the effects of dopamine agonists on the parkinsonian primate brain. Implications for the neural mechanisms that mediate dopamine agonist-induced dyskinesia. Brain 115 (1992), 809–824.
44. 44 Vila, M., Levy, R., Herrero, M.T., Ruberg, M., Faucheux, B., Obeso, J.A., et al. Consequences of nigrostriatal denervation on the functioning of the basal ganglia in human and nonhuman primates: An in situ hybridization study of cytochrome oxidase subunit I mRNA. J Neurosci 17 (1997), 765–773.
45. 45 Hutchinson, W.D., Levy, R., Dostrovsky, J.O., Lozano, A.M., Lang, A.E., Effects of apomorphine on globus pallidus neurons in parkinsonian patients. Ann Neurol 42 (1997), 767–775.
46. 46 Boraud, T., Bezard, E., Bioulac, B., Gross, C.E., Dopamine agonist-induced dyskinesias are correlated to both firing pattern and frequency alterations of pallidal neurones in the MPTP-treated monkey. Brain 124 (2001), 546–557.
47. 47 Nicholas, A.P., Lubin, F.D., Hallett, P.J., Vattem, P., Ravenscroft, P., Bezard, E., et al. Striatal histone modifications in models of levodopa-induced dyskinesia. J Neurochem 106 (2008), 486–494.
48. 48 Tekumalla, P.K., Calon, F., Rahman, Z., Birdi, S., Rajput, A.H., Hornykiewicz, O., et al. Elevated levels of DeltaFosB and RGS9 in striatum in Parkinson's disease. Biol Psychiatry 50 (2001), 813–816.
49. 49 Rascol, O., Medical treatment of levodopa-induced dyskinesias. Ann Neurol 47 (2000), S179–S188.
50. 50 Prashanth, L.K., Fox, S., Meissner, W.G., l-Dopa-induced dyskinesia-clinical presentation, genetics, and treatment. Int Rev Neurobiol 98 (2011), 31–54.
51. 51 Rylander, D., Iderberg, H., Li, Q., Dekundy, A., Zhang, J., Li, H., et al. A mGluR5 antagonist under clinical development improves L-DOPA-induced dyskinesia in parkinsonian rats and monkeys. Neurobiol Dis 39 (2010), 352–361.
52. 52 Bezard, E., Tronci, E., Pioli, E.Y., Li, Q., Porras, G., Bjorklund, A., Carta, M., Study of the antidyskinetic effect of eltoprazine in animal models of levodopa-induced dyskinesia. Mov Disord 28 (2013), 1088–1096.
53. 53 Aubert, I., Guigoni, C., Hakansson, K., Li, Q., Dovero, S., Barthe, N., et al. Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol 57 (2005), 17–26.
54. 54 Grueter, B.A., Robison, A.J., Neve, R.L., Nestler, E.J., Malenka, R.C., FosB differentially modulates nucleus accumbens direct and indirect pathway function. Proc Natl Acad Sci U S A 110 (2013), 1923–1928.
55. 55 Robison, A.J., Vialou, V., Mazei-Robison, M., Feng, J., Kourrich, S., Collins, M., et al. Behavioral and structural responses to chronic cocaine require a feedforward loop involving DeltaFosB and calcium/calmodulin-dependent protein kinase II in the nucleus accumbens shell. J Neurosci 33 (2013), 4295–4307.
56. 56 Picconi, B., Centonze, D., Hakansson, K., Bernardi, G., Greengard, P., Fisone, G., et al. Loss of bidirectional striatal synaptic plasticity in L-DOPA-induced dyskinesia. Nat Neurosci 6 (2003), 501–506.