Levodopa-induced dyskinesia is associated with increased thyrotropin releasing hormone in the dorsal striatum of hemi-parkinsonian rats

PLoS ONE

Volumn 5, Issue 11, 2010, Pages

  Cantuti Castelvetri, Ippolita ^a   Hernandez, Ledia F ^b   Keller Mcgandy, Christine E ^b   Kett, Lauren R ^a   Landy, Alex ^a   Hollingsworth, Zane R ^a   Saka, Esen ^c   Crittenden, Jill R ^b   Nillni, Eduardo A ^e   Young, Anne B ^a   Standaert, David G ^d   Graybiel, Ann M ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HACETTEPE UNIVERSITY   (Turkey)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; HORMONE PRECURSOR; LEVODOPA; MESSENGER RNA; MU OPIATE RECEPTOR; MU OPIOID RECEPTOR 1; PREPROTHYROTROPIN RELEASING HORMONE; PROTEIN CALDAG GEFII; PROTIRELIN; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; ANTIPARKINSON AGENT; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; CAUDOPUTAMEN; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE SEVERITY; DRUG INDUCED DISEASE; DYSKINESIA; ENTOPEDUNCULAR NUCLEUS; GENE EXPRESSION; GENETIC TRANSCRIPTION; GLOBUS PALLIDUS; IMMUNOHISTOCHEMISTRY; MALE; MOTOR DYSFUNCTION; NERVE FIBER; NEUROPIL; NONHUMAN; PARKINSONISM; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RADIOIMMUNOASSAY; RAT; RATING SCALE; REAL TIME POLYMERASE CHAIN REACTION; SENSORIMOTOR CORTEX; STRIOSOME; SUBSTANTIA NIGRA; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECT; GENETICS; METABOLISM; PARKINSON DISEASE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT;

ANIMALIA; PARKINSONIA; RATTUS;

ANALYSIS OF VARIANCE; ANIMALS; ANTIPARKINSON AGENTS; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DOPAMINE; DYSKINESIA, DRUG-INDUCED; IMMUNOHISTOCHEMISTRY; LEVODOPA; MALE; PARKINSON DISEASE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYROTROPIN-RELEASING HORMONE;

EID: 78649723150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013861     Document Type: Article

References (67)

1. Fabbrini G, Brotchie JM, Grandas F, Nomoto M, Goetz CG (2007) Levodopa-induced dyskinesias. Mov Disord 22: 1379-1389.
2. Obeso JA, Olanow CW, Nutt JG (2000) Levodopa motor complications in Parkinson's disease. Trends Neurosci 23: S2-7.
3. Obeso JA, Marin C, Rodriguez-Oroz C, Blesa J, Benitez-Temino B, et al. (2008) The basal ganglia in Parkinson's disease: current concepts and unexplained observations. Ann Neurol 64(Suppl 2): S30-46.
4. Bezard E, Brotchie JM, Gross CE (2001) Pathophysiology of levodopa-induced dyskinesia: potential for new therapies. Nat Rev Neurosci 2: 577-588.
5. Calabresi P, Di Filippo M, Ghiglieri V, Picconi B (2008) Molecular mechanisms underlying levodopa-induced dyskinesia. Mov Disord 23(Suppl 3): S570-579.
6. Dunah AW, Yasuda RP, Luo J, Wang Y, Prybylowski KL, et al. (1999) Biochemical studies of the structure and function of the N-methyl-D-aspartate subtype of glutamate receptors. Mol Neurobiol 19: 151-179.
7. Grace AA (2008) Physiology of the normal and dopamine-depleted basal ganglia: insights into levodopa pharmacotherapy. Mov Disord 23(Suppl 3): S560-569.
8. Graybiel AM, Canales JJ, Capper-Loup C (2000) Levodopa-induced dyskinesias and dopamine-dependent stereotypies: a new hypothesis. Trends Neurosci 23: S71-77.
9. Crittenden JR, Cantuti-Castelvetri I, Saka E, Keller-McGandy CE, Hernandez LF, et al. (2009) Dysregulation of CalDAG-GEFI and CalDAG-GEFII predicts the severity of motor side-effects induced by anti-parkinsonian therapy. Proc Natl Acad Sci U S A 106: 2892-2896.
10. Nillni EA, Sevarino KA (1999) The biology of pro-thyrotropin-releasing hormone-derived peptides. Endocr Rev 20: 599-648.
11. Young B, Driedger A, Wojcik J (2007) Autoimmune thyroid disease and segmental myoclonus. Mov Disord 22: 434-436.
12. Isaacs JD, Rakshi J, Baker R, Brooks DJ, Warrens AN (2005) Chorea associated with thyroxine replacement therapy. Mov Disord 20: 1656-1657.
13. Ristic AJ, Svetel M, Dragasevic N, Zarkovic M, Koprivsek K, et al. (2004) Bilateral chorea-ballism associated with hyperthyroidism. Mov Disord 19: 982-983.
14. Yen DJ, Shan DE, Lu SR (1998) Hyperthyroidism presenting as recurrent short paroxysmal kinesigenic dyskinesia. Mov Disord 13: 361-363.
15. Lavy S, Marks ES, Abramsky O (1974) Parkinsonism and hyperthyroidism. Eur Neurol 12: 20-27.
16. Verges B, Giroud M, Richard A, Giroud-Baleydier F, Vaillant G, et al. (1988) Parkinson's disease after antithyroid treatment. Lancet 2: 564.
17. Kim HT, Edwards MJ, Lakshmi Narsimhan R, Bhatia KP (2005) Hyperthy-roidism exaggerating parkinsonian tremor: a clinical lesson. Parkinsonism Relat Disord 11: 331-332.
18. Linazasoro G, Van Blercom N, Magarinos C (2006) Three in one: case report supporting different origins of essential and parkinsonian tremors. Eur Neurol 55: 108-109.
19. Caradoc-Davies TH (1986) Resolution of dyskinesia and the ''on-off'' phenomenon in thyrotoxic patients with Parkinson's disease after antithyroid treatment. Br Med J (Clin Res Ed) 293: 38-39.
20. Nillni EA, Friedman TC, Todd RB, Birch NP, Loh YP, et al. (1995) Pro-thyrotropin-releasing hormone processing by recombinant PC1. J Neurochem 65: 2462-2472.
21. Nillni EA, Luo LG, Jackson IM, McMillan P (1996) Identification of the thyrotropin-releasing hormone precursor, its processing products, and its coexpression with convertase 1 in primary cultures of hypothalamic neurons: anatomic distribution of PC1 and PC2. Endocrinology 137: 5651-5661.
22. Cenci MA (2002) Transcription factors involved in the pathogenesis of L-DOPA-induced dyskinesia in a rat model of Parkinson's disease. Amino Acids 23: 105-109.
23. Lee J, Zhu WM, Stanic D, Finkelstein DI, Horne MH, et al. (2008) Sprouting of dopamine terminals and altered dopamine release and uptake in Parkinsonian dyskinaesia. Brain 131: 1574-1587.
24. Lindgren HS, Rylander D, Ohlin KE, Lundblad M, Cenci MA (2007) The ''motor complication syndrome'' in rats with 6-OHDA lesions treated chronically with L-DOPA: relation to dose and route of administration. Behav Brain Res 177: 150-159.
25. Paille V, Henry V, Lescaudron L, Brachet P, Damier P (2007) Rat model of Parkinson's disease with bilateral motor abnormalities, reversible with levodopa, and dyskinesias. Mov Disord 22: 533-539.
26. Winkler C, Kirik D, Bjorklund A, Cenci MA (2002) 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: 165-186.
27. Cantuti-Castelvetri I, Klucken J, Ingelsson M, Ramasamy K, McLean PJ, et al. (2005) Alpha-Synuclein and Chaperones in Dementia With Lewy Bodies. J Neuropathol Exp Neurol 64: 1058-1066.
28. Schaner P, Todd RB, Seidah NG, Nillni EA (1997) Processing of prothyro-tropin-releasing hormone by the family of prohormone convertases. J Biol Chem 272: 19958-19968.
29. Cruz IP, Nillni EA (1996) Intracellular sites of prothyrotropin-releasing hormone processing. J Biol Chem 271: 22736-22745.
30. Nillni EA, Sevarino KA, Wu P, Jackson IM (1991) Assays for the biosynthesis of thryotropin releasing hormone. In: Conn PM, ed. Methods in Neurosciences: Neuropeptide technology. San Diego: Academic Press. pp 51-69.
31. Nillni EA, Sevarino KA, Jackson IM (1993) Identification of the thyrotropin-releasing hormone-prohormone and its posttranslational processing in a transfected AtT20 tumoral cell line. Endocrinology 132: 1260-1270.
32. Friedman TC, Loh YP, Cawley NX, Birch NP, Huang SS, et al. (1995) Processing of prothyrotropin-releasing hormone (Pro-TRH) by bovine intermediate lobe secretory vesicle membrane PC1 and PC2 enzymes. Endocrinology 136: 4462-4472.
33. Jackson IM, Wu P, Lechan RM (1985) Immunohistochemical localization in the rat brain of the precursor for thyrotropin-releasing hormone. Science 229: 1097-1099.
34. Lechan RM, Jackson IM (1982) Immunohistochemical localization of thyrotro-pin-releasing hormone in the rat hypothalamus and pituitary. Endocrinology 111: 55-65.
35. Lechan RM, Wu P, Jackson IM (1986) Immunolocalization of the thyrotropin-releasing hormone prohormone in the rat central nervous system. Endocrinology 119: 1210-1216.
36. Lechan RM, Wu P, Jackson IM, Wolf H, Cooperman S, et al. (1986) Thyrotropin-releasing hormone precursor: characterization in rat brain. Science 231: 159-161.
37. Wu P, Jackson IM (1988) Post-translational processing of thyrotropin-releasing hormone precursor in rat brain: identification of 3 novel peptides derived from proTRH. Brain Res 456: 22-28.
38. Wu P, Jackson IM (1991) Detection and Purification of Thyrotropin-Releasing Hormone Precursor Peptides Using Antisera Generated Against Synthetic Peptides. In: Conn PM, ed. Methods in Neurosciences. San Diego: Academic Press. pp 337-354.
39. Faiz M, Acarin L, Castellano B, Gonzalez B (2005) Proliferation dynamics of germinative zone cells in the intact and excitotoxically lesioned postnatal rat brain. BMC Neurosci 6: 26.
40. Richardson RM, Broaddus WC, Holloway KL, Fillmore HL (2005) Grafts of adult subependymal zone neuronal progenitor cells rescue hemiparkinsonian behavioral decline. Brain Res 1032: 11-22.
41. Johansson PA, Andersson M, Andersson KE, Cenci MA (2001) Alterations in cortical and basal ganglia levels of opioid receptor binding in a rat model of l-DOPA-induced dyskinesia. Neurobiol Dis 8: 220-239.
42. Pierret P, Mechawar N, Vallee A, Patel J, Priestley JV, et al. (2002) Presence of Ras guanyl nucleotide-releasing protein in striosomes of the mature and developing rat. Neuroscience 111: 83-94.
43. Cenci MA, Tranberg A, Andersson M, Hilbertson A (1999) Changes in the regional and compartmental distribution of FosB- and JunB-like immunoreac-tivity induced in the dopamine-denervated rat striatum by acute or chronic L-dopa treatment. Neuroscience 94: 515-527.
44. 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.
45. Saka E, Elibol B, Erdem S, Dalkara T (1999) Compartmental changes in expression of c-Fos and FosB proteins in intact and dopamine-depleted striatum after chronic apomorphine treatment. Brain Res 825: 104-114.
46. Kish SJ, Shannak K, Hornykiewicz O (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 318: 876-880.
47. Santini E, Alcacer C, Cacciatore S, Heiman M, Herve D, et al. (2009) L-DOPA activates ERK signaling and phosphorylates histone H3 in the striatonigral medium spiny neurons of hemiparkinsonian mice. J Neurochem 108: 621-633.
48. Gerfen CR, Miyachi S, Paletzki R, Brown P (2002) D1 dopamine receptor supersensitivity in the dopamine-depleted striatum results from a switch in the regulation of ERK1/2/MAP kinase. J Neurosci 22: 5042-5054.
49. Canales JJ, Graybiel AM (2000) Patterns of gene expression and behavior induced by chronic dopamine treatments. Ann Neurol 47(4 Suppl 1): S53-59.
50. Canales JJ, Graybiel AM (2000) A measure of striatal function predicts motor stereotypy. Nat Neurosci 3: 377-383.
51. Sato K, Kaji R, Matsumoto S, Nagahiro S, Goto S (2007) Compartmental loss of striatal medium spiny neurons in multiple system atrophy of parkinsonian type. Mov Disord 22: 2365-2370.
52. Sato K, Sumi-Ichinose C, Kaji R, Ikemoto K, Nomura T, et al. (2008) Differential involvement of striosome and matrix dopamine systems in a transgenic model of dopa-responsive dystonia. Proc Natl Acad Sci U S A 105: 12551-12556.
53. Tippett LJ, Waldvogel HJ, Thomas SJ, Hogg VM, van Roon-Mom W, et al. (2007) Striosomes and mood dysfunction in Huntington's disease. Brain 130: 206-221.
54. Chase TN, Oh JD (2000) Striatal mechanisms and pathogenesis of parkinsonian signs and motor complications. Ann Neurol 47: S122-129; discussion S129-130.
55. Ahmed MR, Berthet A, Bychkov E, Porras G, Li Q, et al. (2010) Lentiviral overexpression of GRK6 alleviates L-dopa-induced dyskinesia in experimental Parkinson's disease. Sci Transl Med 2: 28:28.
56. Rylander D, Iderberg H, Li Q, Dekundy A, Zhang J, et al. (2010) A mGluR5 antagonist under clinical development improves L-DOPA-induced dyskinesia in parkinsonian rats and monkeys. Neurobiol Dis 39: 352-361.
57. Popoli P, Caporali MG, Scotti de Carolis A (1991) Interactions between dopamine D1 and D2 receptors in the model of thyrotropin-releasing hormone (TRH)-induced behaviour in rabbits. Eur J Pharmacol 201: 11-16.
58. Popoli P, Caporali MG, Scotti de Carolis A (1989) Effects of SCH 23390 on thyrotropin-releasing hormone-induced behaviour in rabbits. Eur J Pharmacol 173: 211-213.
59. Miwa Y, Koshikawa N, Miyata N, Koshida Y, Kobayashi M, et al. (1995) YM-14673, a thyrotropin-releasing hormone analogue, injected into the nucleus accumbens and the striatum produces repetitive jaw movements in rats. Eur J Pharmacol 277: 63-69.
60. Popoli P, Caporali MG (1993) Adenosine receptor agonists inhibit TRH-induced behaviour in rabbits: evidence for a main role of striatal A2 receptors. Behav Brain Res 57: 105-109.
61. Przegalinski E, Jaworska L, Konarska R, Golembiowska K (1991) The role of dopamine in regulation of thyrotropin-releasing hormone in the striatum and nucleus accumbens of the rat. Neuropeptides 19: 189-195.
62. Przegalinski E, Jaworska L, Budziszewska B (1993) The role of dopamine receptors in the release of thyrotropin-releasing hormone from the rat striatum and nucleus accumbens: an in vitro study. Neuropeptides 25: 277-282.
63. Jaworska-Feil L, Budziszewska B, Lason W (1997) Effects of repeated cocaine administration on the thyrotropin-releasing hormone level and receptors in the rat brain. Neuropeptides 31: 253-258.
64. Kreutz MR, Acworth IN, Lehnert H, Wurtman RJ (1990) Systemic administration of thyrotropin-releasing hormone enhances striatal dopamine release in vivo. Brain Res 536: 347-352.
65. Fink L, Seeger W, Ermert L, Hanze J, Stahl U, et al. (1998) Real-time quantitative RT-PCR after laser-assisted cell picking. Nat Med 4: 1329-1333.
66. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
67. Cantuti-Castelvetri I, Keller-McGandy CE, Albers DS, Beal MF, Vonsattel JP, et al. (2002) Expression and activity of antioxidants in the brain in progressive supranuclear palsy. Brain Res 930: 170-181.