Optogenetic activation of striatal cholinergic interneurons regulates L-dopa-induced dyskinesias

Neurobiology of Disease

Volumn 91, Issue , 2016, Pages 47-58

  Bordia, Tanuja ^a   Perez, Xiomara A ^a   Heiss, Jaime E ^a   Zhang, Danhui ^a   Quik, Maryka ^a  

^a SRI INTERNATIONAL   (United States)

Author keywords

ChAT Cre; ChR2; Dyskinesias; Nicotinic; Optogenetics; Parkinson's disease; Striatum

Indexed keywords

ATROPINE; CHOLINE ACETYLTRANSFERASE; CRE RECOMBINASE; MECAMYLAMINE; NICOTINE; OXIDOPAMINE; PROTEIN C FOS; RHODOPSIN; LEVODOPA; NICOTINIC AGENT;

ADENO ASSOCIATED VIRUS 5; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CHOLINERGIC SYSTEM; CHOLINERGIC TRANSMISSION; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; IN VIVO STUDY; INTERNEURON; LEVODOPA-INDUCED DYSKINESIA; MALE; MOTOR DYSFUNCTION; MOUSE; NERVE CELL STIMULATION; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; VIRUS EXPRESSION; ANIMAL; DRUG EFFECTS; DYSKINESIA; METABOLISM; NEOSTRIATUM; PROCEDURES;

ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CORPUS STRIATUM; DYSKINESIA, DRUG-INDUCED; INTERNEURONS; LEVODOPA; MICE; NEOSTRIATUM; NICOTINE; NICOTINIC AGONISTS; OPTOGENETICS;

EID: 84959449767     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.02.019     Document Type: Article

References (85)

1. Antoniou K., et al. Differential effects of the neuropeptide galanin on striatal acetylcholine release in anaesthetized and awake rats. Br. J. Pharmacol. 1997, 121:1180-1186.
2. Aosaki T., et al. Temporal and spatial characteristics of tonically active neurons of the primate's striatum. J. Neurophysiol. 1995, 73:1234-1252.
3. Artymyshyn R., et al. The use of 3H standards in 125I autoradiography. J. Neurosci. Methods 1990, 32:185-192.
4. Bido S., et al. Differential involvement of Ras-GRF1 and Ras-GRF2 in L-DOPA-induced dyskinesia. Ann. Clin. Transl. Neurol. 2015, 2:662-678.
5. Bishop C., et al. Contribution of the striatum to the effects of 5-HT1A receptor stimulation in L-DOPA-treated hemiparkinsonian rats. J. Neurosci. Res. 2009, 87:1645-1658.
6. Blandini F., Armentero M.T. New pharmacological avenues for the treatment of L-DOPA-induced dyskinesias in Parkinson's disease: targeting glutamate and adenosine receptors. Expert Opin. Investig. Drugs. 2012, 21:153-168.
7. Bonsi P., et al. Centrality of striatal cholinergic transmission in Basal Ganglia function. Front. Neuroanat. 2011, 5:6.
8. Bordia T., et al. Continuous and intermittent nicotine treatment reduces L-3,4-dihydroxyphenylalanine (L-DOPA)-induced dyskinesias in a rat model of Parkinson's disease. J. Pharmacol. Exp. Ther. 2008, 327:239-247.
9. Bordia T., et al. Nicotinic receptor-mediated reduction in L-dopa-induced dyskinesias may occur via desensitization. J. Pharmacol. Exp. Ther. 2010, 333:929-938.
10. Bordia T., et al. Evidence for a role for alpha6(*) nAChRs in l-dopa-induced dyskinesias using parkinsonian alpha6(*) nAChR gain-of-function mice. Neuroscience 2015, 295:187-197.
11. Cachope R., et al. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2012, 2:33-41.
12. Calon F., et al. Molecular basis of levodopa-induced dyskinesias. Ann. Neurol. 2000, 47:S70-S78.
13. Carta M., Bezard E. Contribution of pre-synaptic mechanisms to l-DOPA-induced dyskinesia. Neuroscience 2011, 198:245-251.
14. Cenci M.A. Dopamine dysregulation of movement control in L-DOPA-induced dyskinesia. Trends Neurosci. 2007, 30:236-243.
15. Cenci M.A., Konradi C. Maladaptive striatal plasticity in l-DOPA-induced dyskinesia. Prog. Brain Res. 2010, 183C:209-233.
16. Cenci M., Lindgren H. Advances in understanding l-DOPA-induced dyskinesia. Curr. Opin. Neurobiol. 2007, 17:665-671.
17. Cenci M.A., Lundblad M. Ratings of L-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr. Protoc. Neurosci. 2007, Chapter 9:1-23.
18. Consolo S., et al. Determination of endogenous acetylcholine release in freely moving rats by transstriatal dialysis coupled to a radioenzymatic assay: effect of drugs. J. Neurochem. 1987, 48:1459-1465.
19. Crosby N.J., et al. Amantadine for dyskinesia in Parkinson's disease. Cochrane Database Syst. Rev. 2003.
20. Ding Y., et al. Enhanced striatal cholinergic neuronal activity mediates L-DOPA-induced dyskinesia in parkinsonian mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:340-345.
21. Duty S. Targeting glutamate receptors to tackle the pathogenesis, clinical symptoms and levodopa-induced dyskinesia associated with Parkinson's disease. CNS Drugs 2012, 26:1017-1032.
22. Ebihara K., et al. Differential expression of FosB, c-Fos, and Zif268 in forebrain regions after acute or chronic L-DOPA treatment in a rat model of Parkinson's disease. Neurosci. Lett. 2011, 496:90-94.
23. Engeln M., et al. Widespread monoaminergic dysregulation of both motor and non-motor circuits in parkinsonism and dyskinesia. Cereb. Cortex 2015, 25:2783-2792.
24. Feyder M., et al. L-DOPA-induced dyskinesia and abnormal signaling in striatal medium spiny neurons: focus on dopamine D1 receptor-mediated transmission. Front. Behav. Neurosci. 2011, 5:71.
25. Freeze B.S., et al. Control of basal ganglia output by direct and indirect pathway projection neurons. J. Neurosci. 2013, 33:18531-18539.
26. Gasparini, F., et al., 2013. Metabotropic glutamate receptors for Parkinson's disease therapy. Parkinsons Dis. 2013, 196028.
27. Giniatullin R., et al. Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci. 2005, 28:371-378.
28. Gonzales K.K., Smith Y. Cholinergic interneurons in the dorsal and ventral striatum: anatomical and functional considerations in normal and diseased conditions. Ann. N. Y. Acad. Sci. 2015, 1349:1-45.
29. Hiroi N., et al. Molecular dissection of dopamine receptor signaling. J. Chem. Neuroanat. 2002, 23:237-242.
30. Huang L., et al. Nicotine reduces L-Dopa-induced dyskinesias by acting at 2 nicotinic receptors. J. Pharmacol. Exp. Ther. 2011, 338:932-941.
31. Huot P., et al. Anatomically selective serotonergic type 1A and serotonergic type 2A therapies for Parkinson's disease: an approach to reducing dyskinesia without exacerbating parkinsonism?. J. Pharmacol. Exp. Ther. 2011, 339:2-8.
32. Huot P., et al. The pharmacology of L-DOPA-induced dyskinesia in Parkinson's disease. Pharmacol. Rev. 2013, 65:171-222.
33. Iravani M.M., et al. Striatal plasticity in Parkinson's disease and L-DOPA induced dyskinesia. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S123-S125.
34. Kaneko S., et al. Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. Science 2000, 289:633-637.
35. Kawashima K., et al. Determination of acetylcholine release in the striatum of anesthetized rats using in vivo microdialysis and a radioimmunoassay. J. Neurochem. 1991, 57:882-887.
36. Kishore A., Popa T. Cerebellum in levodopa-induced dyskinesias: the unusual suspect in the motor network. Front. Neurol. 2014, 5:157.
37. Kishore A., et al. Cerebellar sensory processing alterations impact motor cortical plasticity in Parkinson's disease: clues from dyskinetic patients. Cereb. Cortex 2014, 24:2055-2067.
38. Koos T., Tepper J.M. Dual cholinergic control of fast-spiking interneurons in the neostriatum. J. Neurosci. 2002, 22:529-535.
39. Kravitz A.V., et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
40. Lim S.A., et al. Striatal cholinergic interneuron regulation and circuit effects. Front. Synaptic Neurosci. 2014, 6:22.
41. Lim S.A., et al. Enhanced histamine H2 excitation of striatal cholinergic interneurons in L-DOPA-induced dyskinesia. Neurobiol. Dis. 2015, 76C:67-76.
42. Luginger E., et al. Beneficial effects of amantadine on L-dopa-induced dyskinesias in Parkinson's disease. Mov. Disord. 2000, 15:873-878.
43. Maurice N., et al. Striatal cholinergic interneurons control motor behavior and basal ganglia function in experimental parkinsonism. Cell Rep. 2015, 13:657-666.
44. Meissner W.G., et al. Priorities in Parkinson's disease research. Nat. Rev. Drug Discov. 2011, 10:377-393.
45. Millar N.S., Gotti C. Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 2009, 56:237-246.
46. Mohr F., et al. Dysfunctional presynaptic M2 receptors in the presence of chronically high acetylcholine levels: data from the PRiMA knockout mouse. PLoS ONE 2015, 10.
47. Nelson A.B., et al. Striatal cholinergic interneurons Drive GABA release from dopamine terminals. Neuron 2014, 82:63-70.
48. Nguyen H.N., et al. Activation of the mouse primary visual cortex by medial prefrontal subregion stimulation is not mediated by cholinergic basalo-cortical projections. Front. Syst. Neurosci. 2015, 9:1.
49. Obeso J.A., et al. Missing pieces in the Parkinson's disease puzzle. Nat. Med. 2010, 16:653-661.
50. Pakhotin P., Bracci E. Cholinergic interneurons control the excitatory input to the striatum. J. Neurosci. 2007, 27:391-400.
51. Paradiso K.G., Steinbach J.H. Nicotine is highly effective at producing desensitization of rat alpha4beta2 neuronal nicotinic receptors. J. Physiol. 2003, 553:857-871.
52. Paul M.L., et al. D1-like and D2-like dopamine receptors synergistically activate rotation and c-fos expression in the dopamine-depleted striatum in a rat model of Parkinson's disease. J. Neurosci. 1992, 12:3729-3742.
53. Picciotto M.R., et al. It is not "either/or": activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog. Neurobiol. 2008, 84:329-342.
54. Quik M., Wonnacott S. α6β2* and α4β2* nicotinic acetylcholine receptors as drug targets for Parkinson's disease. Pharmacol. Rev. 2011, 63:938-966.
55. Quik M., et al. Differential declines in striatal nicotinic receptor subtype function after nigrostriatal damage in mice. Mol. Pharmacol. 2003, 63:1169-1179.
56. Quik M., et al. Nicotine reduces levodopa-induced dyskinesias in lesioned monkeys. Ann. Neurol. 2007, 62:588-596.
57. Quik M., et al. Nicotine and Parkinson's disease: implications for therapy. Mov. Disord. 2008, 23:1641-1652.
58. Quik M., et al. Role for α6 nicotinic receptors in L-dopa-induced dyskinesias in parkinsonian mice. Neuropharmacology 2012, 63:450-459.
59. Quik M., et al. α4β2 nicotinic receptors play a role in the nAChR-mediated decline in L-dopa-induced dyskinesias in parkinsonian rats. Neuropharmacology 2013, 71:191-203.
60. Quik M., et al. Role for the nicotinic cholinergic system in movement disorders; therapeutic implications. Pharmacol. Ther. 2014, 144:50-59.
61. Quik M., et al. Alpha7 nicotinic receptors as therapeutic targets for Parkinson's disease. Biochem. Pharmacol. 2015, 97:399-407.
62. Rangel-Barajas C., et al. 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. 2011, 41:51-61.
63. Raz A., et al. Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates. J. Neurophysiol. 1996, 76:2083-2088.
64. Richter U., et al. Mechanisms underlying cortical resonant states: implications for levodopa-induced dyskinesia. Rev. Neurosci. 2013, 24:415-429.
65. Robertson G.S., et al. L-dopa activates c-fos in the striatum ipsilateral to a 6-hydroxydopamine lesion of the substantia nigra. Eur. J. Pharmacol. 1989, 159:99-100.
66. Rodnitzky R.L., Narayanan N.S. Amantadine's role in the treatment of levodopa-induced dyskinesia. Neurology 2014, 82:288-289.
67. Rylander D. The serotonin system: a potential target for anti-dyskinetic treatments and biomarker discovery. Parkinsonism Relat. Disord. 2012, 18(Suppl. 1):S126-S128.
68. Santini E., et al. L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J. Neurochem. 2009, 108:621-633.
69. Schallert T., et al. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
70. Schapira A.H., Jenner P. Etiology and pathogenesis of Parkinson's disease. Mov. Disord. 2011, 26:1049-1055.
71. Thomas A., et al. Duration of amantadine benefit on dyskinesia of severe Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 2004, 75:141-143.
72. Threlfell S., Cragg S.J. Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons. Front. Syst. Neurosci. 2011, 5:11.
73. Threlfell S., et al. Striatal muscarinic receptors promote activity dependence of dopamine transmission via distinct receptor subtypes on cholinergic interneurons in ventral versus dorsal striatum. J. Neurosci. 2010, 30:3398-3408.
74. Threlfell S., et al. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 2012, 75:58-64.
75. Tozzi A., et al. The distinct role of medium spiny neurons and cholinergic interneurons in the D(2)/A(2)A receptor interaction in the striatum: implications for Parkinson's disease. J. Neurosci. 2011, 31:1850-1862.
76. Ueno T., et al. Morphological and electrophysiological changes in intratelencephalic-type pyramidal neurons in the motor cortex of a rat model of levodopa-induced dyskinesia. Neurobiol. Dis. 2014, 64:142-149.
77. Wilson C.J., et al. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J. Neurosci. 1990, 10:508-519.
78. Winkler C., et al. L-DOPA-induced dyskinesia in the intrastriatal 6-hydroxydopamine model of parkinson's disease: relation to motor and cellular parameters of nigrostriatal function. Neurobiol. Dis. 2002, 10:165-186.
79. Won L., et al. Striatal cholinergic cell ablation attenuates L-DOPA induced dyskinesia in parkinsonian mice. J. Neurosci. 2014, 34:3090-3094.
80. Yan Z., Surmeier D.J. Muscarinic (m2/m4) receptors reduce N- and P-type Ca2+ currents in rat neostriatal cholinergic interneurons through a fast, membrane-delimited G-protein pathway. J. Neurosci. 1996, 16:2592-2604.
81. Zhang F., et al. Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 2010, 5:439-456.
82. Zhang Y., et al. Aberrant restoration of spines and their synapses in L-DOPA-induced dyskinesia: involvement of corticostriatal but not thalamostriatal synapses. J. Neurosci. 2013, 33:11655-11667.
83. Zhang D., et al. ABT-089 and ABT-894 reduce levodopa-induced dyskinesias in a monkey model of Parkinson's disease. Mov. Disord. 2014, 29:508-517.
84. Zhang D., et al. The alpha7 nicotinic receptor agonist ABT-107 decreases L-Dopa-induced dyskinesias in parkinsonian monkeys. J. Pharmacol. Exp. Ther. 2014, 351:25-32.
85. Zhou F.M., et al. Cholinergic interneuron characteristics and nicotinic properties in the striatum. J. Neurobiol. 2002, 53:590-605.