Amphetamine-induced abnormal movements occur independently of both transplant- and host-derived serotonin innervation following neural grafting in a rat model of Parkinson's disease

Neurobiology of Disease

Volumn 35, Issue 1, 2009, Pages 42-51

  Lane, Emma Louise ^a   Brundin, Patrik ^a   Cenci, M Angela ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

5,7 DHT; 6 OHDA; Graft induced dyskinesia; Transplantation; Ventral mesencephalon

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 5,7 DIHYDROXYTRYPTAMINE; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; AMPHETAMINE; DOPAMINE RECEPTOR; LEVODOPA; OXIDOPAMINE; RACLOPRIDE; SEROTONIN; SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXIAL DYSKINESIA; CELL COUNT; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; DYSKINESIA; FEMALE; GRAFT VERSUS HOST REACTION; INNERVATION; LIMB DISEASE; LIMB DYSKINESIA; LOCOMOTOR DYSKINESIA; MESENCEPHALON; MOUTH DISEASE; NERVE TRANSPLANTATION; NEUROMODULATION; NONHUMAN; OROLINGUAL DYSKINESIA; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SCORING SYSTEM; SEROTONINERGIC NERVE CELL; TONGUE DISEASE;

5,7-DIHYDROXYTRYPTAMINE; ADRENERGIC AGENTS; AMPHETAMINE; ANIMALS; ANTIPARKINSON AGENTS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; DYSKINESIAS; EMBRYO, MAMMALIAN; FEMALE; LEVODOPA; MESENCEPHALON; OXIDOPAMINE; PARKINSON DISEASE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SEROTONIN AGENTS; TRANSPLANTS; TYROSINE 3-MONOOXYGENASE;

EID: 67349211457     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2009.03.014     Document Type: Article

References (55)

1. Andersson, M., Hilbertson, A., Cenci, M.A., 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.
2. Antonelli T., Fuxe K., Tomasini M.C., Bartoszyk G.D., Seyfried C.A., Tanganelli S., and Ferraro L. Effects of sarizotan on the corticostriatal glutamate pathways. Synapse 58 (2005) 193-199
3. Bara-Jimenez W., Bibbiani F., Morris M.J., Dimitrova T., Sherzai A., Mouradian M.M., and Chase T.N. Effects of serotonin 5-HT1A agonist in advanced Parkinson's disease. Mov. Disord. 20 (2005) 932-936
4. Bedard P.J., Gomez-Mancilla B., Blanchette P., Gagnon C., Falardeau P., and DiPaolo T. Role of selective D1 and D2 agonists in inducing dyskinesia in drug-naive MPTP monkeys. Adv. Neurol. 60 (1993) 113-118
5. Bibbiani F., Oh J.D., and Chase T.N. Serotonin 5-HT1A agonist improves motor complications in rodent and primate parkinsonian models. Neurology 57 (2001) 1829-1834
6. Braak H., and Del Tredici K. Assessing fetal nerve cell grafts in Parkinson's disease. Nat. Med. 14 (2008) 483-485
7. Brundin P., Pogarell O., Hagell P., Piccini P., Widner H., Schrag A., Kupsch A., Crabb L., Odin P., Gustavii B., Bjorklund A., Brooks D.J., Marsden C.D., Oertel W.H., Quinn N.P., Rehncrona S., and Lindvall O. Bilateral caudate and putamen grafts of embryonic mesencephalic tissue treated with lazaroids in Parkinson's disease. Brain 123 Pt 7 (2000) 1380-1390
8. Carlsson T., Winkler C., Lundblad M., Cenci M.A., Bjorklund A., and Kirik D. Graft placement and uneven pattern of reinnervation in the striatum is important for development of graft-induced dyskinesia. Neurobiol. Dis. 21 (2006) 657-668
9. Carlsson T., Carta M., Winkler C., Bjorklund A., and Kirik D. Serotonin neuron transplants exacerbate L-DOPA-induced dyskinesias in a rat model of Parkinson's disease. J. Neurosci. 27 (2007) 8011-8022
10. Carta M., Carlsson T., Kirik D., and Bjorklund A. Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130 (2007) 1819-1833
11. Cenci M.A., Lee C.S., and 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
12. Cragg, S.J., Clarke, D.J., Greenfield, S.A., 2000. Real-time dynamics of dopamine released from neuronal transplants in experimental Parkinson's disease. Exp. Neurol. 164, 145-153.
13. Cumming P., Ljubic-Thibal V., Laliberte C., and Diksic M. The effect of unilateral neurotoxic lesions to serotonin fibres in the medial forebrain bundle on the metabolism of [3H]DOPA in the telencephalon of the living rat. Brain Res. 747 (1997) 60-69
14. Defer G.L., Geny C., Ricolfi F., Fenelon G., Monfort J.C., Remy P., Villafane G., Jeny R., Samson Y., Keravel Y., Gaston A., Degos J.D., Peschanski M., Cesaro P., and Nguyen J.P. Long-term outcome of unilaterally transplanted parkinsonian patients. I. Clinical approach. Brain 119 Pt 1 (1996) 41-50
15. Dekundy A., Lundblad M., Danysz W., and Cenci M.A. Modulation of L-DOPA-induced abnormal involuntary movements by clinically tested compounds: further validation of the rat dyskinesia model. Behav. Brain Res. 179 (2007) 76-89
16. Dijk S.N., Francis P.T., Stratmann G.C., and Bowen D.M. NMDA-induced glutamate and aspartate release from rat cortical pyramidal neurones: evidence for modulation by a 5-HT1A antagonist. Br. J. Pharmacol. 115 (1995) 1169-1174
17. Dupre K.B., Eskow K.L., Negron G., and Bishop C. The differential effects of 5-HT(1A) receptor stimulation on dopamine receptor-mediated abnormal involuntary movements and rotations in the primed hemiparkinsonian rat. Brain Res. 1158 (2007) 135-143
18. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., and Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344 (2001) 710-719
19. Gomez-Mancilla B., and Bedard P.J. Effect of D1 and D2 agonists and antagonists on dyskinesia produced by L-DOPA in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated monkeys. J. Pharmacol. Exp. Ther. 259 (1991) 409-413
20. Grondin R., Doan V.D., Gregoire L., and Bedard P.J. D1 receptor blockade improves L-DOPA-induced dyskinesia but worsens parkinsonism in MPTP monkeys. Neurology 52 (1999) 771-776
21. Hagell P., and Cenci M.A. Dyskinesias and dopamine cell replacement in Parkinson's disease: a clinical perspective. Brain Res. Bull. 68 (2005) 4-15
22. Hagell P., Piccini P., Bjorklund A., Brundin P., Rehncrona S., Widner H., Crabb L., Pavese N., Oertel W.H., Quinn N., Brooks D.J., and Lindvall O. Dyskinesias following neural transplantation in Parkinson's disease. Nat. Neurosci. 5 (2002) 627-628
23. Hauser R.A., Freeman T.B., Snow B.J., Nauert M., Gauger L., Kordower J.H., and Olanow C.W. Long-term evaluation of bilateral fetal nigral transplantation in Parkinson disease. Arch. Neurol. 56 (1999) 179-187
24. Herzog J., Pogarell O., Pinsker M.O., Kupsch A., Oertel W.H., Lindvall O., Deuschl G., and Volkmann J. Deep brain stimulation in Parkinson's disease following fetal nigral transplantation. Mov. Disord. 23 (2008) 1293-1296
25. Kannari K., Shen H., Arai A., Tomiyama M., and Baba M. Reuptake of L-DOPA-derived extracellular dopamine in the striatum with dopaminergic denervation via serotonin transporters. Neurosci. Lett. 402 (2006) 62-65
26. Kuan, W.L., Lin, R., Tyers, P., Barker, R.A., 2007. The importance of A9 dopaminergic neurons in mediating the functional benefits of fetal ventral mesencephalon transplants and levodopa-induced dyskinesias. Neurobiol. Dis. 25, 594-608.
27. Lane E.L., Cheetham S., and Jenner P. Dopamine uptake inhibitor-induced rotation in 6-hydroxydopamine-lesioned rats involves both D1 and D2 receptors but is modulated through 5-hydroxytryptamine and noradrenaline receptors. J. Pharmacol. Exp. Ther. 312 (2005) 1124-1131
28. Lane E.L., Winkler C., Brundin P., and Cenci M.A. The impact of graft size on the development of dyskinesia following intrastriatal grafting of embryonic dopamine neurons in the rat. Neurobiol. Dis. 22 (2006) 334-345
29. Lane E.L., Soulet D., Vercammen L., Cenci M.A., and Brundin P. Neuroinflammation in the generation of post-transplantation dyskinesia in Parkinson's disease. Neurobiol. Dis. (2008)
30. Lundblad, M., Andersson, M., Winkler, C., Kirik, D., Wierup, N., Cenci, M.A., 2002. Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur. J. Neurosci. 15, 120-132.
31. Ma Y., Feigin A., Dhawan V., Fukuda M., Shi Q., Greene P., Breeze R., Fahn S., Freed C., and Eidelberg D. Dyskinesia after fetal cell transplantation for parkinsonism: a PET study. Ann. Neurol. 52 (2002) 628-634
32. Maeda T., Nagata K., Yoshida Y., and Kannari K. Serotonergic hyperinnervation into the dopaminergic denervated striatum compensates for dopamine conversion from exogenously administered l-DOPA. Brain Res. 1046 (2005) 230-233
33. Maries E., Kordower J.H., Chu Y., Collier T.J., Sortwell C.E., Olaru E., Shannon K., and Steece-Collier K. Focal not widespread grafts induce novel dyskinetic behavior in parkinsonian rats. Neurobiol. Dis. 21 (2006) 165-180
34. Mendez I., Vinuela A., Astradsson A., Mukhida K., Hallett P., Robertson H., Tierney T., Holness R., Dagher A., Trojanowski J.Q., and Isacson O. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat. Med. 14 (2008) 507-509
35. Mignon L., and Wolf W.A. Postsynaptic 5-HT(1A) receptors mediate an increase in locomotor activity in the monoamine-depleted rat. Psychopharmacology (Berl.) 163 (2002) 85-94
36. Mignon L.J., and Wolf W.A. 8-hydroxy-2-(di-n-propylamino)tetralin reduces striatal glutamate in an animal model of Parkinson's disease. Neuroreport 16 (2005) 699-703
37. Monville C., Torres E.M., and Dunnett S.B. Validation of the l-dopa-induced dyskinesia in the 6-OHDA model and evaluation of the effects of selective dopamine receptor agonists and antagonists. Brain Res. Bull. 68 (2005) 16-23
38. Mounir A., Chkirate M., Vallee A., Pierret P., Geffard M., and Doucet G. Host serotonin axons innervate intrastriatal ventral mesencephalic grafts after implantation in newborn rats. Eur. J. Neurosci. 6 (1994) 1307-1315
39. Olanow C.W., Goetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., Shannon K.M., Nauert G.M., Perl D.P., Godbold J., and Freeman T.B. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann. Neurol. 54 (2003) 403-414
40. Olanow C.W., Gracies J.M., Goetz C.G., Stoessl A.J., Freeman T., Kordower J.H., Godbold J., and Obeso J.A. Clinical pattern and risk factors for dyskinesias following fetal nigral transplantation in Parkinson's disease: a double blind video-based analysis. Mov. Disord. 24 (2009) 336-343
41. Piccini P., Pavese N., Hagell P., Reimer J., Bjorklund A., Oertel W.H., Quinn N.P., Brooks D.J., and Lindvall O. Factors affecting the clinical outcome after neural transplantation in Parkinson's disease. Brain 128 (2005) 2977-2986
42. Rascol O., Brooks D.J., Korczyn A.D., De Deyn P.P., Clarke C.E., and Lang A.E. A five-year study of the incidence of dyskinesia in patients with early Parkinson's disease who were treated with ropinirole or levodopa. 056 Study Group. N. Engl. J. Med. 342 (2000) 1484-1491
43. Soderstrom K.E., Meredith G., Freeman T.B., McGuire S.O., Collier T.J., Sortwell C.E., Wu Q., and Steece-Collier K. The synaptic impact of the host immune response in a parkinsonian allograft rat model: influence on graft-derived aberrant behaviors. Neurobiol. Dis. (2008)
44. Strecker, R.E., Sharp, T., Brundin, P., Zetterstrom, T., Ungerstedt, U., Bjorklund, A., 1987. Autoregulation of dopamine release and metabolism by intrastriatal nigral grafts as revealed by intracerebral dialysis. Neuroscience 22, 169-178.
45. Tanaka H., Kannari K., Maeda T., Tomiyama M., Suda T., and Matsunaga M. Role of serotonergic neurons in L-DOPA-derived extracellular dopamine in the striatum of 6-OHDA-lesioned rats. Neuroreport 10 (1999) 631-634
46. Taylor J.L., Bishop C., and Walker P.D. Dopamine D1 and D2 receptor contributions to L-DOPA-induced dyskinesia in the dopamine-depleted rat. Pharmacol. Biochem. Behav. 81 (2005) 887-893
47. Tomiyama M., Kimura T., Maeda T., Kannari K., Matsunaga M., and Baba M. A serotonin 5-HT1A receptor agonist prevents behavioral sensitization to L-DOPA in a rodent model of Parkinson's disease. Neurosci. Res. 52 (2005) 185-194
48. Vinuela A., Hallett P.J., Reske-Nielsen C., Patterson M., Sotnikova T.D., Caron M.G., Gainetdinov R.R., and Isacson O. Implanted reuptake-deficient or wild-type dopaminergic neurons improve ON L-DOPA dyskinesias without OFF-dyskinesias in a rat model of Parkinson's disease. Brain 131 (2008) 3361-3379
49. Westin J.E., Lindgren H.S., Gardi J., Nyengaard J.R., Brundin P., Mohapel P., and Cenci M.A. Endothelial proliferation and increased blood-brain barrier permeability in the basal ganglia in a rat model of 3,4-dihydroxyphenyl-L-alanine-induced dyskinesia. J. Neurosci. 26 (2006) 9448-9461
50. Westin J.E., Vercammen L., Strome E.M., Konradi C., and Cenci M.A. Spatiotemporal 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 (2007) 800-810
51. Winkler C., Kirik D., Bjorklund A., and Cenci M.A. 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. 10 (2002) 165-186
52. Winkler C., Kirik D., and Bjorklund A. Cell transplantation in Parkinson's disease: how can we make it work?. Trends Neurosci. 28 (2005) 86-92
53. Yamada H., Aimi Y., Nagatsu I., Taki K., Kudo M., and Arai R. Immunohistochemical detection of L-DOPA-derived dopamine within serotonergic fibers in the striatum and the substantia nigra pars reticulata in Parkinsonian model rats. Neurosci. Res. 59 (2007) 1-7
54. Yamato H., Kannari K., Shen H., Suda T., and Matsunaga M. Fluoxetine reduces L-DOPA-derived extracellular DA in the 6-OHDA-lesioned rat striatum. Neuroreport 12 (2001) 1123-1126
55. Zetterstrom, T., Herrera-Marschitz, M., Ungerstedt, U., 1986. Simultaneous measurement of dopamine release and rotational behaviour in 6-hydroxydopamine denervated rats using intracerebral dialysis. Brain Res. 376, 1-7.