L-DOPA-induced dysregulation of extrastriatal dopamine and serotonin and affective symptoms in a bilateral rat model of Parkinson's disease

Neuroscience

Volumn 218, Issue , 2012, Pages 243-256

  Eskow Jaunarajs, K L ^a   George, J A ^a   Bishop, C ^a  

^a BINGHAMTON UNIVERSITY   (United States)

Author keywords

6 OHDA; Anxiety; Dopamine; L DOPA; Parkinson's disease; Serotonin

Indexed keywords

BENSERAZIDE; DOPAMINE; LEVODOPA; MONOAMINE; OXIDOPAMINE; SEROTONIN;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; DOPAMINE BRAIN LEVEL; DOPAMINE RELEASE; DORSAL RAPHE NUCLEUS; DRUG EFFICACY; DYSKINESIA; EMOTIONAL DISORDER; EXPERIMENTAL DESIGN; FORCED SWIMMING TEST; HIPPOCAMPUS; LOCOMOTION; MALE; MAZE TEST; MEDIAL FOREBRAIN BUNDLE; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SEROTONIN BRAIN LEVEL; SEROTONIN RELEASE; SOCIAL INTERACTION; SPRAGUE DAWLEY RAT; STRIATE CORTEX; SUBSTANTIA NIGRA PARS COMPACTA;

ADRENERGIC AGENTS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; DOPAMINE; LEVODOPA; MALE; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN;

EID: 84863776902     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.05.052     Document Type: Article

References (62)

1. Arai R., Karasawa N., Geffard M., Nagatsu I. L-DOPA is converted to dopamine in serotonergic fibers of the striatum of the rat: a double-labeling immunofluorescence study. Neurosci Lett 1995, 195:195-198.
2. Black K.J., Hershey T., Hartlein J.M., Carl J.L., Perlmutter J.S. Levodopa challenge neuroimaging of levodopa-related mood fluctuations in Parkinson's disease. Neuropsychopharmacology 2005, 30:590-601.
3. Bananej M., Karimi-Sori A., Zarrindast M.R., Ahmadi S. D1 and D2 dopaminergic systems in the rat basolateral amygdala are involved in anxiogenic-like effects induced by histamine. J Psychopharmacol 2012, 26:564-574.
4. Borah A., Mohanakumar K.P. Long-term L-DOPA treatment causes indiscriminate increase in dopamine levels at the cost of serotonin synthesis in discrete brain regions of rats. Cell Mol Neurobiol 2007, 27:985-996.
5. Branchi I., D'Andrea I., Armida M., Cassano T., Pezzola A., Potenza R.L., Morgese M.G., Popoli P., Alleva E. Nonmotor symptoms in Parkinson's disease: investigating early-phase onset of behavioral dysfunction in the 6-hydroxydopamine-lesioned rat model. J Neurosci Res 2008, 86:2050-2061.
6. Campbell B.M., Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 2003, 993:1-9.
7. Carta M., Carlsson T., Kirik D., Bjorklund A. Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 2007, 130:1819-1833.
8. Chaudhuri K.R., Odin P. The challenge of non-motor symptoms in Parkinson's disease. Prog Brain Res 2010, 184:325-341.
9. Christianson J.P., Ragole T., Amat J., Greenwood B.N., Strong P.V., Paul E.D., Fleshner M., Watkins L.R., Maier S.F. 5-Hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biol Psychiatry 2010, 67:339-345.
10. Cools R., Barker R.A., Sahakian B.J., Robbins T.W. L-DOPA medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson's disease. Neuropsychologia 2003, 41:1431-1441.
11. Cools R. Dopaminergic modulation of cognitive function-implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 2006, 30:1-23.
12. de la Mora M.P., Gallegos-Cari A., Arizmendi-Garcia Y., Marcellino D., Fuxe K. Role of dopamine receptor mechanisms in the amygdaloid modulation of fear and anxiety: structural and functional analysis. Prog Neurobiol 2010, 90:198-216.
13. Delaveau P., Salgado-Pineda P., Witjas T., Micallef-Roll J., Fakra E., Azulay J.P., Blin O. Dopaminergic modulation of amygdala activity during emotion recognition in patients with Parkinson disease. J Clin Psychopharm 2009, 29:548-554.
14. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic terminals. Psychopharmacology (Berl) 1995, 121:66-72.
15. Deumens R., Blokland A., Prickaerts J. Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol 2002, 175:303-317.
16. Di Giovanni G., Di Matteo V., Pierucci M., Esposito E. Serotonin-dopamine interaction: electrophysiological evidence. Prog Brain Res 2008, 172:45-71.
17. Doremus T.L., Varlinskaya E.I., Spear L.P. Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacol Biochem Behav 2006, 83:570-577.
18. El Gameyel G., Trouvin J.H., Prioux-Guyonneau M., Jacquot C., Cohen Y. Dopaminergic metabolism in various rat brain areas after L-DOPA loading. J Pharm Pharmacol 1986, 38:691-694.
19. Eskow Jaunarajs K.L., Angoa-Perez M., Kuhn D.M., Bishop C. Potential mechanisms underlying anxiety and depression in Parkinson's disease: consequences of l-DOPA treatment. Neurosci Biobehav Rev 2011, 35:556-564.
20. Eskow Jaunarajs K.L., Dupre K.B., Ostock C.Y., Button T., Bishop C. Behavioral and neurochemical effects of chronic L-DOPA treatment on non-motor sequelae in the hemiparkinsonian rat. Behav Pharmacol 2010, 21:627-637.
21. Eskow K.L., Dupre K.B., Barnum C.J., Dickinson S.O., Park J.Y., Bishop C. The role of the dorsal raphe nucleus in the development, expression, and treatment of L-DOPA-induced dyskinesia in hemiparkinsonian rats. Synapse 2009, 63:610-620.
22. Eskow K.L., Gupta V., Alam S., Park J.Y., Bishop C. The partial 5-HT(1A) agonist buspirone reduces the expression and development of l-DOPA-induced dyskinesia in rats and improves l-DOPA efficacy. Pharmacol Biochem Behav 2007, 87:306-314.
23. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114:2283-2301.
24. File S.E., Seth P. A review of 25years of the social interaction test. Eur J Pharmacol 2003, 463:35-53.
25. Gasbarri A., Sulli A., Packard M.G. The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 1997, 21:1-22.
26. Gotham A.M., Brown R.G., Marsden C.D. 'Frontal' cognitive function in patients with Parkinson's disease 'on' and 'off' levodopa. Brain 1988, 111:299-321.
27. Grace A.A., Rosenkranz J.A. Regulation of conditioned responses of basolateral amygdala neurons. Physiol Behav 2002, 77:489-493.
28. Guerra M.J., Liste I., Labandeira-Garcia J.L. Effects of lesions of the nigrostriatal pathway and of nigral grafts on striatal serotonergic innervation in adult rats. Neuroreport 1997, 8:3485-3488.
29. Guiard B.P., El Mansari M., Merali Z., Blier P. Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. Int J Neuropsychopharmacol 2008, 11:625-639.
30. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 1996, 54:21-30.
31. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiological Rev 1992, 72:165-229.
32. Kannari K., Shen H., Arai A., Tomiyama M., Baba M. Reuptake of L-DOPA-derived extracellular dopamine in the striatum with dopaminergic denervation via serotonin transporters. Neurosci Lett 2006, 402:62-65.
33. Kilpatrick I.C., Jones M.W., Phillipson O.T. A semiautomated analysis method for catecholamines, indoleamines, and some prominent metabolites in microdissected regions of the nervous system: an isocratic HPLC technique employing coulometric detection and minimal sample preparation. J Neurochem 1986, 46:1865-1876.
34. Kish S.J., Shannak K., Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. NEJM 1988, 318:876-880.
35. Kish S.J., Tong J., Hornykiewicz O., Rajput A., Chang L.J., Guttman M., Furukawa Y. Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 2008, 131:120-131.
36. Kuhn D.M., Arthur R. Dopamine inactivates tryptophan hydroxylase and forms a redox-cycling quinoprotein: possible endogenous toxin to serotonin neurons. J Neurosci 1998, 18:7111-7117.
37. Kuhn D.M., Arthur R.E. L-DOPA-quinone inactivates tryptophan hydroxylase and converts the enzyme to a redox-cycling quinoprotein. Brain Res Mol Brain Res 1999, 73:78-84.
38. Kulisevsky J., Pascual-Sedano B., Barbanoj M., Gironell A., Pagonabarraga J., García-Sánchez C. Acute effects of immediate and controlled-release levodopa on mood in Parkinson's disease: a double-blind study. Mov Disord 2007, 22:62-67.
39. Lucki I. The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 1997, 8:523-532.
40. Maeda T., Kannari K., Shen H., Arai A., Tomiyama M., Matsunaga M., Suda T. Rapid induction of serotonergic hyperinnervation in the adult rat striatum with extensive dopaminergic denervation. Neurosci Lett 2003, 343:17-20.
41. Maeda T., Nagata K., Yoshida Y., Kannari K. Serotonergic hyperinnervation into the dopaminergic denervated striatum compensates for dopamine conversion from exogenously administered L-DOPA. Brain Res 2005, 1046:230-233.
42. Millan M.J. Serotonin 5-HT2C receptors as a target for the treatment of anxious and depressive states: focus on novel therapeutic strategies. Therapy 2005, 60:441-460.
43. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiological Rev 1998, 78:189-225.
44. Navailles S., Banzzouz A., Bioulac B., Gross C., De Deurwaerdere P. High-frequency stimulation of the subthalamic nucleus and L-3,4-dihydroxyphenylalanine inhibit in vivo serotonin release in the prefrontal cortex and hippocampus in a rat model of Parkinson's disease. J Neurosci 2010, 30:2356-2364.
45. Navailles S., Bioulac B., Gross C., De Deurwaerdere P. Serotonergic neurons mediate ectopic release of dopamine induced by L-DOPA in a rat model of Parkinson's disease. Neurobiol Dis 2010, 38:136-143.
46. Navailles S., Bioulac B., Gross C., De Deurwaerdere P. Chronic L-DOPA therapy alters central serotonergic function and L-DOPA-induced dopamine release in a region-dependent manner in a rat model of Parkinson's disease. Neurobiol Dis 2011, 41:585-590.
47. Obeso J.A., Rodriguez-Oroz M.C., Chana P., Lera G., Rodriguez M., Olanow C.W. The evolution and origin of motor complications in Parkinson's disease. Neurology 2000, 55:S13-20.
48. Paille V., Henry V., Lescaudron L., Brachet P., Damier P. Rat model of Parkinson's disease with bilateral motor abnormalities, reversible with levodopa, and dyskinesias. Mov Disord 2007, 22:533-539.
49. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Orlando. 4th ed.
50. Prut L., Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 2003, 463:3-33.
51. Ressler K.J., Nemeroff C.B. Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Dep Anx 2000, 12:S2-S19.
52. Richard I.H., Frank S., McDermott M.P., Wang H., Justus A.W., LaDonna K.A., Kurlan R. The ups and downs of Parkinson disease: a prospective study of mood and anxiety fluctuations. Cogn Behav Neurol 2005, 17:201-207.
53. Rosenkranz J.A., Grace A.A. Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 2001, 21:4090-4103.
54. Rozas G., Liste I., Guerra M.J., Labandeira-Garcia J.L. Sprouting of the serotonergic afferents into striatum after selective lesion of the dopaminergic system by MPTP in adult mice. Neurosci Lett 1998, 245:151-154.
55. Rylander D., Parent M., O'Sullivan S.S., Dovero S., Lees A.J., Bezard E., Descarries L., Cenci M.A. Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia. Ann Neurol 2010, 68:619-628.
56. Smith A.D., Almalric M., Koob G.F., Zigmond M.J. Effect of bilateral 6-OHDA lesions of the medial forebrain bundle on reaction time. Neuropsychopharmacology 2002, 26:756-764.
57. Tadaiesky M.T., Dombrowski P.A., Figueiredo C.P., Cargnin-Ferreira E., Da Cunha C., Takahashi R.N. Emotional, cognitive, and neurochemical alterations in a premotor stage model of Parkinson's disease. Neuroscience 2008, 156:830-840.
58. Truong L., Allbutt H., Kassiou M., Henderson J.M. Developing a preclinical model of Parkinson's disease: a study of behavior in rats with graded 6-OHDA lesions. Behav Brain Res 2006, 169:1-9.
59. Wallman M.J., Gagnon D., Parent M. Serotonin innervation of human basal ganglia. Eur J Neurosci 2011, 33:1519-1532.
60. Winter C., von Rumohr A., Mundt A., Petrus D., Klein J., Lee T., Morgenstern R., Kupsch A., Juckel G. Lesions of dopaminergic neurons in the substantia nigra pars compacta and in the ventral tegmental area enhance depressive-like behavior in rats. Behav Brain Res 2007, 184:133-141.
61. Yamada H., Aimi Y., Nagatsu I., Taki K., Kudo M., Arai R. Immunohistochemical detection of L-DOPA-derived dopamine within serotonergic fibers in the striatum and substantia nigra pars reticulate in Parkinsonian model rats. Neurosci Res 2007, 59:1-7.
62. Zeng B.Y., Iravani M.M., Jackson M.J., Rose S., Parent A., Jenner P. Morphological changes in serotoninergic neurites in the striatum and globus pallidus in levodopa primed MPTP treated common marmosets with dyskinesia. Neurobiol Dis 2010, 40:599-607.