Effect of long-term treatment with pramipexole or levodopa on presynaptic markers assessed by longitudinal [123I]FP-CIT SPECT and histochemistry

NeuroImage

Volumn 79, Issue , 2013, Pages 191-200

  Depboylu, Candan ^a   Maurer, Lukas ^a   Matusch, Andreas ^b   Hermanns, Guido ^a   Windolph, Andrea ^a   Béhé, Martin ^c   Oertel, Wolfgang H ^a   Höglinger, Günter U ^a,d,e  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

^c ETH Zurich   (Switzerland)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Dopamine; Dopamine agonist; Neurodegeneration; Neuroimaging; Neuroregeneration; Parkinson disease

Indexed keywords

DOPAMINE TRANSPORTER; LEVODOPA; PRAMIPEXOLE; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC SYSTEM; DRUG EFFECT; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; MOUSE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SUBSTANTIA NIGRA;

ANIMALS; ANTIPARKINSON AGENTS; BENZOTHIAZOLES; DOPAMINE AGONISTS; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; LEVODOPA; LONGITUDINAL STUDIES; MALE; MICE; MICE, INBRED C57BL; NEURONAL PLASTICITY; PARKINSON DISEASE; PRESYNAPTIC TERMINALS; RADIOPHARMACEUTICALS; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; TREATMENT OUTCOME; TROPANES;

EID: 84878138194     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.04.076     Document Type: Article

References (53)

1. Alvarez-Fischer D., Blessmann G., Trosowski C., Béhé M., Schurrat T., Hartmann A., Behr T.M., Oertel W.H., Höglinger G.U., Höffken H. Quantitative [(123)I]FP-CIT pinhole SPECT imaging predicts striatal dopamine levels, but not number of nigral neurons in different mouse models of Parkinson's disease. NeuroImage 2007, 38:5-12.
2. Alvarez-Fischer D., Henze C., Strenzke C., Westrich J., Ferger B., Höglinger G.U., Oertel W.H., Hartmann A. Characterization of the striatal 6-OHDA model of Parkinson's disease in wild type and alpha-synuclein-deleted mice. Exp. Neurol. 2008, 210:182-193.
3. Benamer H.T., Patterson J., Wyper D.J., Hadley D.M., Macphee G.J., Grosset D.G. Correlation of Parkinson's disease severity and duration with 123I-FP-CIT SPECT striatal uptake. Mov. Disord. 2000, 15:692-698.
4. Bernheimer H., Birkmayer W., Hornykiewicz O., Jellinger K., Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 1973, 20:415-455.
5. Bezard E., Dovero S., Imbert C., Boraud T., Gross C.E. Spontaneous long-term compensatory dopaminergic sprouting in MPTP-treated mice. Synapse 2000, 38:363-368.
6. Chen J.F., Qin Z.H., Szele F., Bai G., Weiss B. Neuronal localization and modulation of the D2 dopamine receptor mRNA in brain of normal mice and mice lesioned with 6-hydroxydopamine. Neuropharmacology 1991, 30:927-941.
7. Datla K.P., Blunt S.B., Dexter D.T. Chronic L-DOPA administration is not toxic to the remaining dopaminergic nigrostriatal neurons, but instead may promote their functional recovery, in rats with partial 6-OHDA or FeCl(3) nigrostriatal lesions. Mov. Disord. 2001, 16:424-434.
8. Eisensehr I., Wetter T.C., Linke R., Noachtar S., von Lindeiner H., Gildehaus F.J., Trenkwalder C., Tatsch K. Normal IPT and IBZM SPECT in drug-naive and levodopa-treated idiopathic restless legs syndrome. Neurology 2001, 57:1307-1309.
9. Eriksen J., Jørgensen T.N., Gether U. Regulation of dopamine transporter function by protein-protein interactions: new discoveries and methodological challenges. J. Neurochem. 2010, 113:27-41.
10. Fahn S., Oakes D., Shoulson I., Kieburtz K., Rudolph A., Lang A., Olanow C.W., Tanner C., Marek K., Parkinson Study Group Levodopa and the progression of Parkinson's disease. N. Engl. J. Med. 2004, 351:2498-2508.
11. Fang C., Yin J., Xu Z., Wang Y., Xu H., Zhou H., Gao C. Striatal dopaminergic fiber recovery after acute L-DOPA treatment in 6-hydroxydopamine (6-OHDA) lesioned rats. Cell Biochem. Biophys. 2011, 59:49-56.
12. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 1991, 114:2283-2301.
13. Franklin K.B.J., Paxinos G. The Mouse Brain in Stereotactic Coordinates 1997, Academic Press, San Diego, CA, USA.
14. Grånäs C., Ferrer J., Loland C.J., Javitch J.A., Gether U. N-terminal truncation of the dopamine transporter abolishes phorbol ester- and substance P receptor-stimulated phosphorylation without impairing transporter internalization. J. Biol. Chem. 2003, 278:4990-5000.
15. Guttman M., Stewart D., Hussey D., Wilson A., Houle S., Kish S. Influence of L-dopa and pramipexole on striatal dopamine transporter in early PD. Neurology 2001, 56:1559-1564.
16. Hagenah J., Klein C., Sieberer M., Vieregge P. Exogenous levodopa is not toxic to elderly subjects with non-Parkinsonian movement disorders: further clinical evidence. J. Neural Transm. 1999, 106:301-307.
17. Hirsch E., Graybiel A.M., Agid Y.A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 1988, 334:345-348.
18. Höglinger G.U., Rizk P., Muriel M.P., Duyckaerts C., Oertel W.H., Caille I., Hirsch E.C. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 2004, 7:726-735.
19. Iranzo A., Valldeoriola F., Lomeña F., Molinuevo J.L., Serradell M., Salamero M., Cot A., Ros D., Pavía J., Santamaria J., Tolosa E. Serial dopamine transporter imaging of nigrostriatal function in patients with idiopathic rapid-eye-movement sleep behaviour disorder: a prospective study. Lancet Neurol. 2011, 10:797-805.
20. Izumi Y., Sawada H., Yamamoto N., Kume T., Katsuki H., Shimohama S., Akaike A. Novel neuroprotective mechanisms of pramipexole, an anti-Parkinson drug, against endogenous dopamine-mediated excitotoxicity. Eur. J. Pharmacol. 2007, 557:132-140.
21. Joyce J.N., Woolsey C., Ryoo H., Borwege S., Hagner D. Low dose pramipexole is neuroprotective in the MPTP mouse model of Parkinson's disease, and downregulates the dopamine transporter via the D3 receptor. BMC Biol. 2004, 2:22.
22. Kemmerer E.S., Desmond T.J., Albin R.L., Kilbourn M.R., Frey K.A. Treatment effects on nigrostriatal projection integrity in partial 6-OHDA lesions: comparison of L-DOPA and pramipexole. Exp. Neurol. 2003, 183:81-86.
23. Kokoshka J.M., Vaughan R.A., Hanson G.R., Fleckenstein A.E. Nature of methamphetamine-induced rapid and reversible changes in dopamine transporters. Eur. J. Pharmacol. 1998, 361:269-275.
24. Li C., Guo Y., Xie W., Li X., Janokovic J., Le W. Neuroprotection of pramipexole in UPS impairment induced animal model of Parkinson's disease. Neurochem. Res. 2010, 35:1546-1556.
25. Ma Y., Smith D., Hof P.R., Foerster B., Hamilton S., Blackband S.J., Yu M., Benveniste H. In vivo 3D digital atlas database of the adult C57Bl/6J mouse brain by magnetic resonance microscopy. Front. Neuroanat. 2008, 2:1.
26. Mann D.M., Yates P.O. Possible role of neuromelanin in the pathogenesis of Parkinson's disease. Mech. Ageing Dev. 1983, 21:193-203.
27. Meiergerd S.M., Patterson T.A., Schenk J.O. D2 receptors may modulate the function of the striatal transporter for dopamine: kinetic evidence from studies in vitro and in vivo. J. Neurochem. 1993, 61:764-767.
28. Mitsumoto Y., Watanabe A., Mori A., Koga N. Spontaneous regeneration of nigrostriatal dopaminergic neurons in MPTP-treated C57BL/6 mice. Biochem. Biophys. Res. Commun. 1998, 248:660-663.
29. Murer M.G., Dziewczapolski G., Menalled L.B., García M.C., Agid Y., Gershanik O., Raisman-Vozari R. Chronic levodopa is not toxic for remaining dopamine neurons, but instead promotes their recovery, in rats with moderate nigrostriatal lesions. Ann. Neurol. 1998, 43:561-575.
30. Narayanan N.S., Guarnieri D.J., DiLeone R.J. Metabolic hormones, dopamine circuits, and feeding. Front. Neuroendocrinol. 2010, 31:104-112.
31. Nirenberg M.J., Vaughan R.A., Uhl G.R., Kuhar M.J., Pickel V.M. The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. J. Neurosci. 1996, 16:436-447.
32. Pan T., Xie W., Jankovic J., Le W. Biological effects of pramipexole on dopaminergic neuron-associated genes: relevance to neuroprotection. Neurosci. Lett. 2005, 377:106-109.
33. Parkinson Study Group Dopamine transporter brain imaging to assess the effects of pramipexole vs levodopa on Parkinson disease progression. JAMA 2002, 287:1653-1661.
34. Parkkinen L., O'Sullivan S.S., Kuoppamäki M., Collins C., Kallis C., Holton J.L., Williams D.R., Revesz T., Lees A.J. Does levodopa accelerate the pathologic process in Parkinson disease brain?. Neurology 2011, 77:1420-1426.
35. Rajput A.H. The protective role of levodopa in the human substantia nigra. Adv. Neurol. 2001, 86:327-336.
36. Ravina B., Eidelberg D., Ahlskog J.E., Albin R.L., Brooks D.J., Carbon M., Dhawan V., Feigin A., Fahn S., Guttman M., Gwinn-Hardy K., McFarland H., Innis R., Katz R.G., Kieburtz K., Kish S.J., Lange N., Langston J.W., Marek K., Morin L., Moy C., Murphy D., Oertel W.H., Oliver G., Palesch Y., Powers W., Seibyl J., Sethi K.D., Shults C.W., Sheehy P., Stoessl A.J., Holloway R. The role of radiotracer imaging in Parkinson disease. Neurology 2005, 64:208-215.
37. Rousselet E., Joubert C., Callebert J., Parain K., Tremblay L., Orieux G., Launay J.M., Cohen-Salmon C., Hirsch E.C. Behavioral changes are not directly related to striatal monoamine levels, number of nigral neurons, or dose of Parkinsonian toxin MPTP in mice. Neurobiol. Dis. 2003, 14:218-228.
38. Rudow G., O'Brien R., Savonenko A.V., Resnick S.M., Zonderman A.B., Pletnikova O., Marsh L., Dawson T.M., Crain B.J., West M.J., Troncoso J.C. Morphometry of the human substantia nigra in ageing and Parkinson's disease. Acta Neuropathol. 2008, 115:461-470.
39. Sakai K., Gash D.M. Effect of bilateral 6-OHDA lesions of the substantia nigra on locomotor activity in the rat. Brain Res. 1994, 633:144-150.
40. Sauer H., Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 1994, 59:401-415.
41. Saunders C., Ferrer J.V., Shi L., Chen J., Merrill G., Lamb M.E., Leeb-Lundberg L.M., Carvelli L., Javitch J.A., Galli A. Amphetamine-induced loss of human dopamine transporter activity: an internalization-dependent and cocaine-sensitive mechanism. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6850-6855.
42. Schillaci O., Pierantozzi M., Filippi L., Manni C., Brusa L., Danieli R., Bernardi G., Simonetti G., Stanzione P. The effect of levodopa therapy on dopamine transporter SPECT imaging with (123)I-FP-CIT in patients with Parkinson's disease. Eur. J. Nucl. Med. Mol. Imaging 2005, 32:1452-1456.
43. Schmitt K.C., Reith M.E.A. Regulation of the dopamine transporter: aspects relevant to psychostimulant drugs of abuse. Ann. N. Y. Acad. Sci. 2010, 1187:316-340.
44. Shapira A.H. Neuroprotection and dopamine agonists. Neurology 2002, 58:9-18.
45. Stanic D., Finkelstein D.I., Bourke D.W., Drago J., Horne M.K. Timecourse of striatal re-innervation following lesions of dopaminergic SNpc neurons of the rat. Eur. J. Neurosci. 2003, 18:1175-1188.
46. Tompkins M.M., Basgall E.J., Zamrini E., Hill W.D. Apoptotic-like changes in Lewy-body-associated disorders and normal aging in substantia nigral neurons. Am. J. Pathol. 1997, 150:119-131.
47. Van Kampen J.M., Eckman C.B. Dopamine D3 receptor agonist delivery to a model of Parkinson's disease restores the nigrostriatal pathway and improves locomotor behavior. J. Neurosci. 2006, 26:7272-7280.
48. Winner B., Desplats P., Hagl C., Klucken J., Aigner R., Ploetz S., Laemke J., Karl A., Aigner L., Masliah E., Buerger E., Winkler J. Dopamine receptor activation promotes adult neurogenesis in an acute Parkinson model. Exp. Neurol. 2009, 219:543-552.
49. Winogrodzka A., Bergmans P., Booij J., van Royen E.A., Stoof J.C., Wolters E.C. [(123)I]beta-CIT SPECT is a useful method for monitoring dopaminergic degeneration in early stage Parkinson's disease. J. Neurol. Neurosurg Psychiatry 2003, 74:294-298.
50. Wolf M.E., Roth R.H. Autoreceptor regulation of dopamine synthesis. Ann. N. Y. Acad. Sci. 1990, 604:323-343.
51. Zhou Q.Y., Palmiter R.D. Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic. Cell 1995, 83:1197-1209.
52. Zigmond M.J., Stricker E.M. Recovery of feeding and drinking by rats after intraventricular 6-hydroxydopamine or lateral hypothalamic lesions. Science 1973, 182:717-720.
53. Zou L., Jankovic J., Rowe D.B., Xie W., Appel S.H., Le W. Neuroprotection by pramipexole against dopamine- and levodopa-induced cytotoxicity. Life Sci. 1999, 64:1275-1285.