Generation of a α-synuclein-based rat model of Parkinson's disease

Neurobiology of Disease

Volumn 30, Issue 1, 2008, Pages 8-18

  Recchia, Alessandra ^a   Rota, David ^a   Debetto, Patrizia ^a   Peroni, Daniele ^a   Guidolin, Diego ^a   Negro, Alessandro ^a   Skaper, Stephen D ^b   Giusti, Pietro ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Synuclein; Animal models; Dopaminergic loss; Fusion protein; Motor impairment; Neurodegeneration; Parkinson's disease; Substantia nigra pars compacta

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 3,4 DIHYDROXYPHENYLACETIC ACID; ALPHA SYNUCLEIN; DOPAMINE; HYBRID PROTEIN; TYROSINE 3 MONOOXYGENASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL MEMBRANE; CONTROLLED STUDY; DNA FOOTPRINTING; DOPAMINERGIC NERVE CELL; FUSION GENE; GENE MUTATION; GENETIC TRANSDUCTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; MALE; MOTOR PERFORMANCE; NEUROPATHOLOGY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; RAT; ROTAROD TEST; STEREOTACTIC TREATMENT; SUBSTANTIA NIGRA; WESTERN BLOTTING;

3,4-DIHYDROXYPHENYLACETIC ACID; ADRENERGIC AGENTS; ALPHA-SYNUCLEIN; ANALYSIS OF VARIANCE; ANIMALS; APOMORPHINE; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; GENE EXPRESSION REGULATION; GENE PRODUCTS, TAT; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MALE; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSON DISEASE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 40849094012     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.11.002     Document Type: Article

References (54)

1. Albani D., Peverelli E., Rametta R., Batelli S., Veschini L., Negro A., and Forloni G. Protective effect of TAT-delivered α-synuclein: relevance of the C-terminal domain and involvement of HSP70. FASEB J. 18 (2004) 1713-1715
2. Becker-Hapak M., McAllister S.S., and Dowdy S.F. TAT-mediated protein transduction into mammalian cells. Methods 24 (2001) 247-256
3. Berrios G.E., Campbell C., and Politynska B.E. Autonomic failure, depression and anxiety in Parkinson's disease. Br. J. Psychiatry 166 (1995) 789-792
4. Biere A.L., Wood S.J., Wypych J., Steavenson S., Jiang Y., Anafi D., Jacobsen F.W., Jarosinski M.A., Wu G.-M., Louis J.-C., Martin F., Narhi L.O., and Citron M. Parkinson's disease-associated α-synuclein is more fibrillogenic than β- and γ-synuclein and cannot cross-seed its homologs. J. Biol. Chem. 275 (2000) 34574-34579
5. Bonifati V., Rizzu P., van Baren M.J., Schaap O., Breedveld G.J., Krieger E., Dekker M.C., Squitieri F., Ibanez P., Joosse M., van Dongen J.W., Vanacore N., van Swieten J.C., Brice A., Meco G., van Duijn C.M., Oostra B.A., and Heutink P. Mutations in the DJ-1 gene associated with autosomal recessive early-onset parkinsonism. Science 299 (2003) 256-259
6. Bonifati V., Rohé C.F., Breedveld G.J., Fabrizio E., De Mari M., Tassorelli A., Tavella R., Marconi D., Nicholl D.J., Chien H.F., Fincati E., Abbruzzese G., Marini P., De Gaetano A., Horstink M.W., Maat-Kievit J.A., Sampaio C., Antonini A., Stocchi P., Montagna P., Toni V., Guidi M., Dalla Libera A., Tinazzi M., De Pandis F., Fabbrini G., Goldwurm S., de Klein A., Barbosa E., Lopiano L., Martignoni E., Lamberti P., Vanacore N., Meco G., Oostra B.A., and and the Italian Parkinson Genetics Network. Early-onset parkinsonism associated with PINK1 mutations: frequency, genotypes, and phenotypes. Neurology 65 (2005) 87-95
7. Carman L.S., Gage F.H., and Shults C.W. Partial lesion of the substantia nigra: relation between extent of lesion and rotational behavior. Brain Res. 553 (1991) 275-283
8. Conway K.A., Harper J.D., and Lansbury P.T. Accelerated in vitro fibril formation by a mutant α-synuclein linked to early-onset Parkinson's disease. Nat. Med. 11 (1998) 1318-1320
9. Conway K.A., Harper J.D., and Lansburry Jr. P.T. Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid. Biochemistry 39 (2000) 2552-2563
10. Conway K.A., Lee S.-J., Rochet J.-C., Ding T.T., Williamson R.E., and Lansbury Jr. P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 571-576
11. Dawson T.M., and Dawson V.L. Molecular pathways of neurodegeneration in Parkinson's disease. Science 302 (2003) 819-822
12. Dawson T.M., Mandir A.S., and Lee M.K. Animal models of PD: pieces of the same puzzle?. Neuron 35 (2002) 219-222
13. Feany M.B., and Bender W.W. A Drosophila model of Parkinson's disease. Nature (London) 404 (2000) 394-398
14. Forno L.S. Neuropathology of Parkinson's disease. J. Neuropathol. Exp. Neurol. 55 (1996) 259-272
15. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat. Rev., Neurosci. 2 (2001) 492-501
16. Gómez-Tortosa E., Newell K., Irizarry M.C., Albert M., Growdon J.H., and Hyman B.T. Clinical and quantitative pathologic correlates of dementia with Lewy bodies. Neurology 53 (1999) 1284-1291
17. Greenbaum E.A., Graves C.L., Mishizen-Eberz A.J., Lupoli M.A., Lynch D.R., Englander S.W., Axelsen P.H., and Giasson B.I. The E46K mutation in α-synuclein increases amyloid fibril formation. J. Biol. Chem. 280 (2006) 7800-7807
18. Guidolin, D., Zunarelli, E., Genedani, S., Trentini, G.P., De Gaetani, C., Fuxe, K., Benegiamo, C., Agnati, L.F., in press. Opposite patterns of age-associated changes in neurons and glial cells of the thalamus of human brain. Neurobiol. Aging. doi:10.1016/j.neurobiolaging.2006.12.015.
19. Hamm R.J., Pike B.R., O'Dell D.M., Lyeth B.G., and Jenkins L.W. The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J. Neurotrauma 11 (1994) 187-196
20. Kirik D., Rosenblad C., Burger C., Lundberg C., Johansen T.E., Muzyczka M., Mandel R.J., and Björklund A. Parkinson-like neurodegeneration induced by targeted overexpression of α-synuclein in the nigrostriatal system. J. Neurosci. 22 (2002) 2780-2791
21. Kirik D., Annett L.E., Burger C., Muzyczka N., Mandel R.J., and Björklund A. Nigrostriatal α-synucleinopathy induced by viral vector-mediated overexpression of human αsynuclein: a new primate model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 2884-2889
22. Klapdor K., Dulfer B.G., Hammann A., and Van der Staay F.J. A low cost method to analyse footprint patterns. J. Neurosci. Methods 75 (1997) 49-54
23. Klein R.L., King M.A., Hamby M.E., and Meyer E.M. Dopaminergic cell loss induced by human A30P α-synuclein gene transfer to the rat substantia nigra. Hum. Gene Ther. 13 (2002) 605-612
24. Krüger R., Kuhn W., Müller T., Woitalla D., Graeber M., Kösel S., Przuntek H., Epplen J.T., Schöls L., and Riess O. Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat. Genet. 18 (1998) 106-108
25. Kshirsager A.M. Multivariate Analysis (1972), Dekker, New York
26. Lauwers E., Bequé D., Van Laere K., Nuyts J., Bormans G., Mortelmans L., Casteels C., Vercammen L., Bockstael O., Nuttin B., Debyser Z., and Baekelandt V. Non-invasive imaging of neuropathology in a rat model of alpha-synuclein overexpression. Neurobiol. Aging 28 (2007) 248-257
27. Leroy E., Boyer R., Auburger G., Leube B., Ulm G., Mezey E., Harta G., Brownstein M.J., Jonnalagada S., Chernova T., Dehejia A., Lavedan C., Gasser T., Steinbach P.J., Wilkinson K.D., and Polymeropoulos M.H. The ubiquitin pathway in Parkinson's disease. Nature (London) 395 (1998) 451-452
28. Lo Bianco C., Ridet J.-L., Schneider B.L., Déglon N., and Aebischer P. α-Synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 10813-10818
29. Lotharius J., and Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and α-synuclein. Nat. Rev., Neurosci. 3 (2002) 932-942
30. Negro A., Grassato L., Polverino De Laureto P., and Skaper S.D. Genetic construction, properties and application of a green fluorescent protein-tagged ciliary neurotrophic factor. Protein Eng. 10 (1997) 1077-1083
31. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd Ed. (1986), Academic Press, Sydney, Australia
32. Periquet M., Fulga T., Myllykangas L., Schlossmacher M.G., and Feany M.B. Aggregated α-synuclein mediates dopaminergic neurotoxicity in vivo. J. Neurosci. 27 (2007) 3338-3346
33. Polymeropoulos M.H., Lavadan C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzarini A.M., Duvoisin R.C., Di Iorio G., Golbe L.I., and Nussbaum R.L. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276 (1997) 2045-2047
34. Pycock C.J. Turning behaviour in animals. Neuroscience 5 (1980) 461-514
35. Recchia A., Debetto P., Negro A., Guidolin D., Skaper S.D., and Giusti P. α-Synuclein and Parkinson's disease. FASEB J. 18 (2004) 617-626
36. Schapira A.H.V., Bezard E., Brotchie J., Calon F., Collingridge G.L., Ferger B., Hengerer B., Hirsch E., Jenner P., Le Novère N., Obeso J.A., Schwarzschild M.A., Spampinato U., and Davidai G. Novel pharmacological targets for the treatment of Parkinson's disease. Nat. Rev. Drug Discov. 5 (2006) 845-854
37. Schwarze S.R., Ho A., Vocero-Akbani A., and Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285 (2000) 1569-1572
38. Serpell L.C., Berriman J., Jakes R., Goedert M., and Crowther R.A. Fiber diffraction of synthetic α-synuclein filaments shows amyloid-like cross-β conformation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 4897-4902
39. Shimura H., Schlossmacher M.G., Hattori N., Frosch M.P., Trockenbacher A., Schneider R., Mizuno Y., Kosik K.S., and Selkoe D.J. Ubiquitination of a new form of α-synuclein by parkin from human brain: implications for Parkinson's disease. Science 293 (2001) 263-269
40. Shults C.W. Lewy bodies. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1661-1668
41. Siderowf A., and Stern M. Update on Parkinson disease. Ann. Intern. Med. 138 (2003) 651-658
42. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M.R., Muenter M., Baptista M., Miller D., Blancato J., Hardy J., and Gwinn-Hardy K. α-Synuclein locus triplication causes Parkinson's disease. Science 302 (2003) 841
43. Singleton A., Myers A., and Hardy J. The law of mass action applied to neurodegenerative disease: a hypothesis concerning the etiology and pathogenesis of complex diseases. Hum. Mol. Genet. 13 Spec No 1 (2004) R123-R126
44. Stiasny-Kolster K., Doerr Y., Möller J.C., Höffken H., Behr T.M., Oertel W.H., and Mayer G. Combination of 'idiopathic' REM sleep behaviour disorder and olfactory dysfunction as possible indicator for α-synucleinopathy demonstrated by dopamine transporter FP-CIT-SPECT. Brain 128 (2005) 126-137
45. Strauss K.M., Martins L.M., Plun-Favreau H., Marx F.P., Kautzmann S., Berg D., Gasser T., Wszolek Z., Müller T., Bornemann A., Wolburg H., Downward J., Riess O., Schulz J.B., and Krüger R. Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum. Med. Genet. 14 (2005) 2099-2111
46. Tanner C.M. Occupational and environmental causes of parkinsonism. Occup. Med. 7 (1992) 503-513
47. Ungerstedt U. Postsynaptic supersensitivity after 6-hydroxy-dopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol. Scand., Suppl. 367 (1971) 69-93
48. Volles M.J., and Lansbury Jr. P.T. Vesicle permeabilization by protofibrillar α-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41 (2002) 4595-4602
49. von Bohlen und Halbach O. Animal models of Parkinson's disease. Neurodegenerative Dis. 2 (2005) 313-320
50. Warner T.T., and Schapira A.H.V. Genetic and environmental factors in the cause of Parkinson's disease. Ann. Neurol. 53 Suppl. 3 (2003) S16-S25
51. Whishaw I.Q., Li K., Whishaw P.A., Gorny B., and Metz G.A. Distinct forelimb and hindlimb impairments in unilateral dopamine-depleted rats: use of the rotarod as a method for the qualitative analysis of skilled walking. J. Neurosci. Methods 126 (2003) 13-23
52. Wood S.J., Wypych J., Steavenson S., Louis J.-C., Citron M., and Biere A.L. α-Synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274 (1999) 19509-19512
53. Zimprich A., Biskup S., Leitner P., Lichtner P., Farrer M., Lincoln S., Kachergus J., Hulihan M., Uitti R.J., Calne D.B., Stoessl A.J., Pfeiffer R.F., Patenge N., Carbajal I.C., Vieregge P., Asmus F., Müller-Myhsok B., Dickson D.W., Meitinger T., Strom T.M., Wszolek Z.K., and Gasser T. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44 (2004) 601-607
54. Zoli M., Guidolin D., and Agnati L.F. Morphometric evaluation of populations of neuronal profiles (cell bodies, dendrites and nerve terminals) in the central nervous system. Microsc. Res. Tech. 21 (1992) 315-337