The ultrastructural distribution of alpha-synuclein-like protein in normal mouse brain

Brain Research

Volumn 1004, Issue 1-2, 2004, Pages 61-72

  Totterdell, Susan ^a   Hanger, Diane ^b   Meredith, Gloria E ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

Basal ganglia; Degenerative disease: Parkinson's; Disorders of the nervous system; Electron microscope; Hippocampus; Immunocytochemistry; Substantia nigra; Synaptic

Indexed keywords

ALPHA SYNUCLEIN;

ARTICLE; BIOACCUMULATION; BRAIN REGION; CELL TYPE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; HIPPOCAMPUS; MOLECULAR RECOGNITION; MOUSE; NERVE CELL; NERVE ENDING; NEUROCHEMISTRY; NONHUMAN; PHENOTYPE; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; ULTRASTRUCTURE;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PRESYNAPTIC TERMINALS; SYNUCLEINS;

EID: 1642350127     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2003.10.072     Document Type: Article

References (54)

1. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.E., Shinsky N., Verdugo J.M., Armanini M., Ryan A., Hynes M., Phillips H., Sulzer D., Rosenthal A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron. 25:2000;239-252.
2. Alheid G.F., de Olmos J.S., Beltramino C.A. Amygdala and Extended Amygdala. Paxinos G. The Rat Nervous System. 1995;495-578 Academic Press, London.
3. Amaral D.G., Witter M.P. Hippocampal formation. Paxinos G. The Rat Nervous System. 1995;443-493 Academic Press, London.
4. Arima K., Mizutani T., Alim M.A., Tonozuka-Uehara H., Izumiyama Y., Hirai S., Ueda K. NACP/alpha-synuclein and tau constitute two distinctive subsets of filaments in the same neuronal inclusions in brains from a family of parkinsonism and dementia with Lewy bodies: double-immunolabeling fluorescence and electron microscopic studies. Acta Neuropathol. (Berl). 100:2000;115-121.
5. Baba M., Nakajo S., Tu P.H., Tomita T., Nakaya K., Lee V.M., Trojanowski J.Q., Iwatsubo T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152:1998;879-884.
6. Bevan M.D., Bolam J.P., Crossman A.R. Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Eur. J. Neurosci. 6:1994;320-334.
7. Braak H., Sandmann-Keil D., Gai W., Braak E. Extensive axonal Lewy neurites in Parkinson's disease: a novel pathological feature revealed by alpha-synuclein immunocytochemistry. Neurosci. Lett. 265:1999;67-69.
8. Braak H., Del Tredici K., Gai W.P., Braak E. Alpha-synuclein is not a requisite component of synaptic boutons in the adult human central nervous system. J. Chem. Neuroanat. 20:2000;245-252.
9. Braak E., Sandmann-Keil D., Rub U., Gai W.P., de Vos R.A., Steur E.N., Arai K., Braak H. Alpha-synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol. (Berl). 101:2001;195-201.
10. Clayton D.F., George J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 58:1999;120-129.
11. Corvaja N., Doucet G., Bolam J.P. Ultrastructure and synaptic targets of the raphe-nigral projection in the rat. Neuroscience. 55:1993;417-427.
12. Duda J.E., Giasson B.I., Mabon M.E., Lee V.M., Trojanowski J.Q. Novel antibodies to synuclein show abundant striatal pathology in Lewy body diseases. Ann. Neurol. 52:2002;205-210.
13. Freund T.F., Powell J.F., Smith A.D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience. 13:1984;1189-1215.
14. Galvin J.E., Uryu K., Lee V.M., Trojanowski J.Q. Axon pathology in Parkinson's disease and Lewy body dementia hippocampus contains alpha-, beta-, and gamma-synuclein. Proc. Natl. Acad. Sci. USA. 96:1999;13450-13455.
15. Galvin J.E., Lee V.M., Trojanowski J.Q. Synucleinopathies: clinical and pathological implications. Arch. Neurol. 58:2001;186-190.
16. Goedert M. Alpha-synuclein and neurodegenerative diseases. Nat. Rev., Neurosci. 2:2001;492-501.
17. Ishimaru H., Ueda K., Takahashi A., Maruyama Y. Changes in presynaptic protein NACP/alpha-synuclein in an ischemic gerbil hippocampus. Brain Res. 788:1998;311-314.
18. Iwai A., Masliah E., Yoshimoto M., Ge N., Flanagan L., de Silva H.A., Kittel A., Saitoh T. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron. 14:1995;467-475.
19. Jakes R., Spillantini M.G., Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett. 345:1994;27-32.
20. Johnson L.R., Aylward R.L., Hussain Z., Totterdell S. Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience. 61:1994;851-865.
21. Johnson L.R., Aylward R.L., Totterdell S. Synaptic orgnization of the amygdalar input to the nucleus accumbens in the rat. Percheron G.E.A. The Basal Ganglia IV. 1994;109-114 Plenum Press, New York.
22. Kahle P.J., Neumann M., Ozmen L., Muller V., Odoy S., Okamoto N., Jacobsen H., Iwatsubo T., Trojanowski J.Q., Takahashi H., Wakabayashi K., Bogdanovic N., Riederer P., Kretzschmar H.A., Haass C. Selective insolubility of alpha-synuclein in human Lewy body diseases is recapitulated in a transgenic mouse model. Am. J. Pathol. 159:2001;2215-2225.
23. Kholodilov N.G., Neystat M., Oo T.F., Lo S.E., Larsen K.E., Sulzer D., Burke R.E. Increased expression of rat synuclein in the substantia nigra pars compacta identified by mRNA differential display in a model of developmental target injury. J. Neurochem. 73:1999;2586-2599.
24. Lavedan C. The synuclein family. Genome Res. 8:1998;871-880.
25. Maroteaux L., Scheller R.H. The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res. Mol. Brain Res. 11:1991;335-343.
26. Maroteaux L., Campanelli J.T., Scheller R.H. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8:1988;2804-2815.
27. Martinez-Murillo R., Villalba R., Montero-Caballero M.I., Rodrigo J. Cholinergic somata and terminals in the rat substantia nigra: an immunocytochemical study with optical and electron microscopic techniques. J. Comp. Neurol. 281:1989;397-415.
28. Matsuoka Y., Vila M., Lincoln S., McCormack A., Picciano M., LaFrancois J., Yu X., Dickson D., Langston W.J., McGowan E., Farrer M., Hardy J., Duff K., Przedborski S., Di Monte D.A. Lack of nigral pathology in transgenic mice expressing human alpha-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol. Dis. 8:2001;535-539.
29. Meredith G.E., Agolia R., Arts M.P., Groenewegen H.J., Zahm D.S. Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience. 50:1992;149-162.
30. Murphy D.D., Rueter S.M., Trojanowski J.Q., Lee V.M. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 20:2000;3214-3220.
31. Ohama E., Ikuta F. Parkinson's disease: distribution of Lewy bodies and monoamine neuron system. Acta Neuropathol. (Berl). 34:1976;311-319.
32. Petersen K., Olesen O.F., Mikkelsen J.D. Developmental expression of alpha-synuclein in rat hippocampus and cerebral cortex. Neuroscience. 91:1999;651-659.
33. Petroske E., Meredith G.E., Callen S., Totterdell S., Lau Y.S. Mouse model of Parkinsonism: a comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience. 106:2001;589-601.
34. Piao Y.S., Wakabayashi K., Hayashi S., Yoshimoto M., Takahashi H. Aggregation of alpha-synuclein/NACP in the neuronal and glial cells in diffuse Lewy body disease: a survey of six patients. Clin. Neuropathol. 19:2000;163-169.
35. Pitkanen A. Connectivity of the rat amygdaloid complex. Aggleton J.P. The Amygdala: a Functional Analysis. 2000;OUP, Oxford.
36. Polymeropoulos M.H., Lavedan 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., Nussbaum R.L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047.
37. Reynolds E.S. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17:1963;208-212.
38. Shastry B.S. Parkinson disease: etiology, pathogenesis and future of gene therapy. Neurosci. Res. 41:2001;5-12.
39. Solano S.M., Miller D.W., Augood S.J., Young A.B., Penney J.B. Jr. Expression of alpha-synuclein, parkin, and ubiquitin carboxy-terminal hydrolase L1 mRNA in human brain: genes associated with familial Parkinson's disease. Ann. Neurol. 47:2000;201-210.
40. Soriano E., Frotscher M. Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus. 4:1994;65-69.
41. Specht C.G., Schoepfer R. Deletion of the alpha-synuclein locus in a subpopulation of C57Bl/6J inbred mice. BMC Neurosci. 2:2001;11.
42. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature. 388:1997;839-840.
43. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Research Bulletin. 9:1982;321-353.
44. Tabrizi S.J., Orth M., Wilkinson J.M., Taanman J.W., Warner T.T., Cooper J.M., Schapira A.H. Expression of mutant alpha-synuclein causes increased susceptibility to dopamine toxicity. Hum. Mol. Genet. 9:2000;2683-2689.
45. Totterdell S., Ingham C.A., Bolam J.P. Immunocytochemistry I: pre-embedding staining. Bolam J.P. Experimental Neuroanatomy, a Practical Approach. 1992;103-128 IRL press, Oxford, UK.
46. Trojanowski J.Q., Lee V.M. Aggregation of neurofilament and alpha-synuclein proteins in Lewy bodies: implications for the pathogenesis of Parkinson disease and Lewy body dementia. Arch. Neurol. 55:1998;151-152.
47. Ueda K., Fukushima H., Masliah E., Xia Y., Iwai A., Yoshimoto M., Otero D.A., Kondo J., Ihara Y., Saitoh T. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 90:1993;11282-11286.
48. Uversky V.N., Li J., Fink A.L. Evidence for a partially folded intermediate in alpha-synuclein fibril formation. J. Biol. Chem. 276:2001;10737-10744.
49. Van Bockstaele E.J., Chan J., Pickel V.M. Pre- and postsynaptic sites for serotonin modulation of GABA-containing neurons in the shell region of the rat nucleus accumbens. J. Comp. Neurol. 371:1996;116-128.
50. Vila M., Vukosavic S., Jackson-Lewis V., Neystat M., Jakowec M., Przedborski S. Alpha-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J. Neurochem. 74:2000;721-729.
51. Wakabayashi K., Matsumoto K., Takayama K., Yoshimoto M., Takahashi H. NACP, a presynaptic protein, immunoreactivity in Lewy bodies in Parkinson's disease. Neurosci. Lett. 239:1997;45-48.
52. Wakabayashi K., Yoshimoto M., Tsuji S., Takahashi H. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci. Lett. 249:1998;180-182.
53. West M.J. New stereological methods for counting neurons. Neurobiology of Aging. 14:1993;275-285.
54. Zahm D.S. An electron microscopic morphometric comparison of tyrosine hydroxylase immunoreactive innervation in the neostriatum and the nucleus accumbens core and shell. Brain Res. 575:1992;341-346.