Striatal Molecular Signature of Subchronic Subthalamic Nucleus High Frequency Stimulation in Parkinsonian Rat

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Lortet, Sylviane ^a   Lacombe, Emilie ^a   Boulanger, Nicolas ^b   Rihet, Pascal ^b   Nguyen, Catherine ^b   Goff, Lydia Kerkerian Le ^a   Salin, Pascal ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b Aix Marseille university   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BENSERAZIDE; LEVODOPA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DRUG EFFECT; DYSKINESIA; GENE CONTROL; GENE EXPRESSION; NERVE CELL DIFFERENTIATION; NEUROSURGERY; NONHUMAN; PARKINSON DISEASE; RAT; SUBTHALAMIC NUCLEUS HIGH FREQUENCY STIMULATION; SYNAPTIC TRANSMISSION; THERAPY EFFECT;

ANIMALS; BEHAVIOR, ANIMAL; CLUSTER ANALYSIS; CORPUS STRIATUM; DEEP BRAIN STIMULATION; DENERVATION; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LEVODOPA; METABOLIC NETWORKS AND PATHWAYS; PARKINSON DISEASE; RATS; SUBTHALAMIC NUCLEUS;

PARKINSONIA; RATTUS;

EID: 84875915236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060447     Document Type: Article

References (85)

1. Dauer W, Przedborski S, (2003) Parkinson's disease: mechanisms and models. Neuron 39: 889-909.
2. DeLong M, Wichmann T, (2009) Update on models of basal ganglia function and dysfunction. Parkinsonism Relat Disord 15 (Suppl 3):: S237-S240.
3. Bezard E, Brotchie JM, Gross CE, (2001) Pathophysiology of levodopa-induced dyskinesia: potential for new therapies. Nat Rev Neurosci 2: 577-588.
4. Cenci MA, (2007) L-DOPA-induced dyskinesia: cellular mechanisms and approaches to treatment. Parkinsonism Relat Disord 13 (Suppl 3):: S263-S267.
5. Iravani MM, Jenner P, (2011) Mechanisms underlying the onset and expression of levodopa-induced dyskinesia and their pharmacological manipulation. J Neural Transm 118: 1661-1690.
6. Gottwald MD, Aminoff MJ, (2011) Therapies for dopaminergic-induced dyskinesias in Parkinson disease. Ann Neurol 69: 919-927.
7. Benabid AL, Chabardes S, Mitrofanis J, Pollak P, (2009) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol 8: 67-81.
8. Katayama Y, Oshima H, Kano T, Kobayashi K, Fukaya C, et al. (2006) Direct effect of subthalamic nucleus stimulation on levodopa-induced peak-dose dyskinesia in patients with Parkinson's disease. Stereotact Funct Neurosurg 84: 176-179.
9. Gubellini P, Eusebio A, Oueslati A, Melon C, Kerkerian-Le GL, et al. (2006) Chronic high-frequency stimulation of the subthalamic nucleus and L-DOPA treatment in experimental parkinsonism: effects on motor behaviour and striatal glutamate transmission. Eur J Neurosci 24: 1802-1814.
10. Oueslati A, Sgambato-Faure V, Melon C, Kachidian P, Gubellini P, et al. (2007) High-frequency stimulation of the subthalamic nucleus potentiates L-DOPA-induced neurochemical changes in the striatum in a rat model of Parkinson's disease. J Neurosci 27: 2377-2386.
11. Lacombe E, Carcenac C, Boulet S, Feuerstein C, Bertrand A, et al. (2007) High-frequency stimulation of the subthalamic nucleus prolongs the increase in striatal dopamine induced by acute l-3,4-dihydroxyphenylalanine in dopaminergic denervated rats. Eur J Neurosci 26: 1670-1680.
12. Gubellini P, Salin P, Kerkerian-Le GL, Baunez C, (2009) Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog Neurobiol 89: 79-123.
13. Khaindrava V, Salin P, Melon C, Ugrumov M, Kerkerian-Le-Goff L, et al. (2011) High frequency stimulation of the subthalamic nucleus impacts adult neurogenesis in a rat model of Parkinson's disease. Neurobiol Dis 42: 284-291.
14. Konradi C, Westin JE, Carta M, Eaton ME, Kuter K, et al. (2004) Transcriptome analysis in a rat model of L-DOPA-induced dyskinesia. Neurobiol Dis 17: 219-236.
15. El Atifi-Borel M, Buggia-Prevot V, Platet N, Benabid AL, Berger F, et al. (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.
16. Grunblatt E, Schmidt WJ, Scheller DK, Riederer P, Gerlach M, (2011) Transcriptional alterations under continuous or pulsatile dopaminergic treatment in dyskinetic rats. J Neural Transm 118: 1717-1725.
17. Naydenov AV, Vassoler F, Luksik AS, Kaczmarska J, Konradi C, (2010) Mitochondrial abnormalities in the putamen in Parkinson's disease dyskinesia. Acta Neuropathol 120: 623-631.
18. Ferrario JE, Taravini IR, Mourlevat S, Stefano A, Delfino MA, et al. (2004) Differential gene expression induced by chronic levodopa treatment in the striatum of rats with lesions of the nigrostriatal system. J Neurochem 90: 1348-1358.
19. De Groot J (1959) The rat forebrain in stereotaxic coordinates. AFD Natuurkunde N. V. Noord-Hallandsche Wetgevers Maatschappij. Amsterdam: Verhandelingen der Koninklijke Nederlandse Akademic van Wetenschappen.
20. Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates. Academic Press., New York.
21. Robelet S, Melon C, Guillet B, Salin P, Kerkerian-Le GL, (2004) Chronic L-DOPA treatment increases extracellular glutamate levels and GLT1 expression in the basal ganglia in a rat model of Parkinson's disease. Eur J Neurosci 20: 1255-1266.
22. Cenci MA, Lee CS, Bjorklund A, (1998) L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur J Neurosci 10: 2694-2706.
23. Salin P, Manrique C, Forni C, Kerkerian-Le GL, (2002) High-frequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci 22: 5137-5148.
24. Kerr MK, Martin M, Churchill GA, (2000) Analysis of variance for gene expression microarray data. J Comput Biol 7: 819-837.
25. Reiner A, Yekutieli D, Benjamini Y, (2003) Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19: 368-375.
26. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: 3.
27. Lacombe E, Khaindrava V, Melon C, Oueslati A, Kerkerian-Le GL, et al. (2009) Different functional basal ganglia subcircuits associated with anti-akinetic and dyskinesiogenic effects of antiparkinsonian therapies. Neurobiol Dis 36: 116-125.
28. Aviles-Olmos I, Limousin P, Lees A, Foltynie T, (2012) Parkinson's disease, insulin resistance and novel agents of neuroprotection. Brain doi: 10.1093/brain/aws009.
29. Li X, Masliah E, Reixach N, Buxbaum JN, (2011) Neuronal production of transthyretin in human and murine Alzheimer's disease: is it protective? J Neurosci 31: 12483-12490.
30. Brouillette J, Quirion R, (2008) Transthyretin: a key gene involved in the maintenance of memory capacities during aging. Neurobiol Aging 29: 1721-1732.
31. Toresson H, Mata de UA, Fagerstrom C, Perlmann T, Campbell K, (1999) Retinoids are produced by glia in the lateral ganglionic eminence and regulate striatal neuron differentiation. Development 126: 1317-1326.
32. Wang TW, Zhang H, Parent JM, (2005) Retinoic acid regulates postnatal neurogenesis in the murine subventricular zone-olfactory bulb pathway. Development 132: 2721-2732.
33. Plane JM, Whitney JT, Schallert T, Parent JM, (2008) Retinoic acid and environmental enrichment alter subventricular zone and striatal neurogenesis after stroke. Exp Neurol 214: 125-134.
34. Liz MA, Leite SC, Juliano L, Saraiva MJ, Damas AM, et al. (2012) Transthyretin is a metallopeptidase with an inducible active site. Biochem J 443: 769-778.
35. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC, (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18: 527-535.
36. Cannizzaro C, Tel BC, Rose S, Zeng BY, Jenner P, (2003) Increased neuropeptide Y mRNA expression in striatum in Parkinson's disease. Brain Res Mol Brain Res 110: 169-176.
37. Kerkerian L, Bosler O, Pelletier G, Nieoullon A, (1986) Striatal neuropeptide Y neurones are under the influence of the nigrostriatal dopaminergic pathway: immunohistochemical evidence. Neurosci Lett 66: 106-112.
38. Lindefors N, Brene S, Herrera-Marschitz M, Persson H, (1990) Neuropeptide gene expression in brain is differentially regulated by midbrain dopamine neurons. Exp Brain Res 80: 489-500.
39. Bassilana F, Mace N, Li Q, Stutzmann JM, Gross CE, et al. (2005) Unraveling substantia nigra sequential gene expression in a progressive MPTP-lesioned macaque model of Parkinson's disease. Neurobiol Dis 20: 93-103.
40. Cabeza-Arvelaiz Y, Fleming SM, Richter F, Masliah E, Chesselet MF, et al. (2011) Analysis of striatal transcriptome in mice overexpressing human wild-type alpha-synuclein supports synaptic dysfunction and suggests mechanisms of neuroprotection for striatal neurons. Mol Neurodegener 6: 83.
41. Li MD, Kane JK, Matta SG, Blaner WS, Sharp BM, (2000) Nicotine enhances the biosynthesis and secretion of transthyretin from the choroid plexus in rats: implications for beta-amyloid formation. J Neurosci 20: 1318-1323.
42. Quik M, Huang LZ, Parameswaran N, Bordia T, Campos C, et al. (2009) Multiple roles for nicotine in Parkinson's disease. Biochem Pharmacol 78: 677-685.
43. Fernandez AM, Torres-Aleman I, (2012) The many faces of insulin-like peptide signalling in the brain. Nat Rev Neurosci 13: 225-239.
44. Bracko O, Singer T, Aigner S, Knobloch M, Winner B, et al. (2012) Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci 32: 3376-3387.
45. Vazin T, Becker KG, Chen J, Spivak CE, Lupica CR, et al. (2009) A novel combination of factors, termed SPIE, which promotes dopaminergic neuron differentiation from human embryonic stem cells. PLoS One 4: e6606.
46. Schmeisser MJ, Baumann B, Johannsen S, Vindedal GF, Jensen V, et al. (2012) IkappaB kinase/nuclear factor kappaB-dependent insulin-like growth factor 2 (Igf2) expression regulates synapse formation and spine maturation via Igf2 receptor signaling. J Neurosci 32: 5688-5703.
47. Smith Y, Villalba RM, Raju DV, (2009) Striatal spine plasticity in Parkinson's disease: pathological or not? Parkinsonism Relat Disord 15 (Suppl 3):: S156-S161.
48. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, et al. (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28: 713-726.
49. Chmielnicki E, Benraiss A, Economides AN, Goldman SA, (2004) Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci 24: 2133-2142.
50. Maxwell MA, Muscat GE, (2006) The NR4A subgroup: immediate early response genes with pleiotropic physiological roles. Nucl Recept Signal 4: e002.
51. Werme M, Ringholm A, Olson L, Brene S, (2000) Differential patterns of induction of NGFI-B, Nor1 and c-fos mRNAs in striatal subregions by haloperidol and clozapine. Brain Res 863: 112-119.
52. Eells JB, Wilcots J, Sisk S, Guo-Ross SX, (2012) NR4A gene expression is dynamically regulated in the ventral tegmental area dopamine neurons and is related to expression of dopamine neurotransmission genes. J Mol Neurosci 46: 545-553.
53. Garcia-Dominguez M, Poquet C, Garel S, Charnay P, (2003) Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Development 130: 6013-6025.
54. Lobo MK, Karsten SL, Gray M, Geschwind DH, Yang XW, (2006) FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat Neurosci 9: 443-452.
55. Bruet N, Windels F, Bertrand A, Feuerstein C, Poupard A, et al. (2001) High frequency stimulation of the subthalamic nucleus increases the extracellular contents of striatal dopamine in normal and partially dopaminergic denervated rats. J Neuropathol Exp Neurol 60: 15-24.
56. Meissner W, Harnack D, Reese R, Paul G, Reum T, et al. (2003) High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J Neurochem 85: 601-609.
57. Zhao XD, Cao YQ, Liu HH, Li FQ, You BM, et al. (2009) Long term high frequency stimulation of STN increases dopamine in the corpus striatum of hemiparkinsonian rhesus monkey. Brain Res 1286: 230-238.
58. Jin H, Kanthasamy A, Anantharam V, Rana A, Kanthasamy AG, (2011) Transcriptional regulation of pro-apoptotic protein kinase Cdelta: implications for oxidative stress-induced neuronal cell death. J Biol Chem 286: 19840-19859.
59. Hanrott K, Gudmunsen L, O'Neill MJ, Wonnacott S, (2006) 6-hydroxydopamine-induced apoptosis is mediated via extracellular auto-oxidation and caspase 3-dependent activation of protein kinase Cdelta. J Biol Chem 281: 5373-5382.
60. Zhang D, Anantharam V, Kanthasamy A, Kanthasamy AG, (2007) Neuroprotective effect of protein kinase C delta inhibitor rottlerin in cell culture and animal models of Parkinson's disease. J Pharmacol Exp Ther 322: 913-922.
61. Steckley D, Karajgikar M, Dale LB, Fuerth B, Swan P, et al. (2007) Puma is a dominant regulator of oxidative stress induced Bax activation and neuronal apoptosis. J Neurosci 27: 12989-12999.
62. Gomez-Lazaro M, Galindo MF, Concannon CG, Segura MF, Fernandez-Gomez FJ, et al. (2008) 6-Hydroxydopamine activates the mitochondrial apoptosis pathway through p38 MAPK-mediated, p53-independent activation of Bax and PUMA. J Neurochem 104: 1599-1612.
63. Gertz M, Steegborn C, (2010) Function and regulation of the mitochondrial sirtuin isoform Sirt5 in Mammalia. Biochim Biophys Acta 1804: 1658-1665.
64. Pfister JA, Ma C, Morrison BE, D'Mello SR, (2008) Opposing effects of sirtuins on neuronal survival: SIRT1-mediated neuroprotection is independent of its deacetylase activity. PLoS One 3: e4090.
65. Toulorge D, Guerreiro S, Hild A, Maskos U, Hirsch EC, et al. (2011) Neuroprotection of midbrain dopamine neurons by nicotine is gated by cytoplasmic Ca2+. FASEB J 25: 2563-2573.
66. Azam L, Winzer-Serhan U, Leslie FM, (2003) Co-expression of alpha7 and beta2 nicotinic acetylcholine receptor subunit mRNAs within rat brain cholinergic neurons. Neuroscience 119: 965-977.
67. Kita Y, Ago Y, Takano E, Fukada A, Takuma K, et al. (2012) Galantamine increases hippocampal insulin-like growth factor 2 expression via alpha7 nicotinic acetylcholine receptors in mice. Psychopharmacology (Berl).
68. Roux PP, Barker PA, (2002) Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 67: 203-233.
69. Zhang SJ, Zou M, Lu L, Lau D, Ditzel DA, et al. (2009) Nuclear calcium signaling controls expression of a large gene pool: identification of a gene program for acquired neuroprotection induced by synaptic activity. PLoS Genet 5: e1000604.
70. Pfeiffer JR, McAvoy BL, Fecteau RE, Deleault KM, Brooks SA, (2011) CARHSP1 is required for effective tumor necrosis factor alpha mRNA stabilization and localizes to processing bodies and exosomes. Mol Cell Biol 31: 277-286.
71. Aubert I, Guigoni C, Li Q, Dovero S, Bioulac BH, et al. (2007) Enhanced preproenkephalin-B-derived opioid transmission in striatum and subthalamic nucleus converges upon globus pallidus internalis in L-3,4-dihydroxyphenylalanine-induced dyskinesia. Biol Psychiatry 61: 836-844.
72. Henry B, Duty S, Fox SH, Crossman AR, Brotchie JM, (2003) Increased striatal pre-proenkephalin B expression is associated with dyskinesia in Parkinson's disease. Exp Neurol 183: 458-468.
73. Lundblad M, Picconi B, Lindgren H, Cenci MA, (2004) A model of L-DOPA-induced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol Dis 16: 110-123.
74. Calabresi P, Giacomini P, Centonze D, Bernardi G, (2000) Levodopa-induced dyskinesia: a pathological form of striatal synaptic plasticity? Ann Neurol 47: S60-S68.
75. Sgambato-Faure V, Cenci MA, (2012) Glutamatergic mechanisms in the dyskinesias induced by pharmacological dopamine replacement and deep brain stimulation for the treatment of Parkinson's disease. Prog Neurobiol 96: 69-86.
76. Zeng BY, Dass B, Owen A, Rose S, Cannizzaro C, et al. (1999) Chronic L-DOPA treatment increases striatal cannabinoid CB1 receptor mRNA expression in 6-hydroxydopamine-lesioned rats. Neurosci Lett 276: 71-74.
77. Cantuti-Castelvetri I, Hernandez LF, Keller-McGandy CE, Kett LR, Landy A, et al. (2010) Levodopa-induced dyskinesia is associated with increased thyrotropin releasing hormone in the dorsal striatum of hemi-parkinsonian rats. PLoS One 5: e13861.
78. Fabbrini G, Brotchie JM, Grandas F, Nomoto M, Goetz CG, (2007) Levodopa-induced dyskinesias. Mov Disord 22: 1379-1389.
79. Nicholson SL, Brotchie JM, (2002) 5-hydroxytryptamine (5-HT, serotonin) and Parkinson's disease- opportunities for novel therapeutics to reduce the problems of levodopa therapy. Eur J Neurol 9 (Suppl 3):: 1-6.
80. 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.
81. Huang Y, Halliday GM, (2012) Aspects of innate immunity and Parkinson's disease. Front Pharmacol 3: 33.
82. Sarkar C, Basu B, Chakroborty D, Dasgupta PS, Basu S, (2010) The immunoregulatory role of dopamine: an update. Brain Behav Immun 24: 525-528.
83. Ding Y, Won L, Britt JP, Lim SA, McGehee DS, et al. (2011) Enhanced striatal cholinergic neuronal activity mediates L-DOPA-induced dyskinesia in parkinsonian mice. Proc Natl Acad Sci U S A 108: 840-845.
84. Pisani A, Bonsi P, Centonze D, Martorana A, Fusco F, et al. (2003) Activation of beta1-adrenoceptors excites striatal cholinergic interneurons through a cAMP-dependent, protein kinase-independent pathway. J Neurosci 23: 5272-5282.
85. Hara M, Fukui R, Hieda E, Kuroiwa M, Bateup HS, et al. (2010) Role of adrenoceptors in the regulation of dopamine/DARPP-32 signaling in neostriatal neurons. J Neurochem 113: 1046-1059.