Mapping of rat brain using the Synuclein-1 monoclonal antibody reveals somatodendritic expression of α-synuclein in populations of neurons homologous to those vulnerable to Lewy body formation in human synucleopathies

Journal of Neuropathology and Experimental Neurology

Volumn 62, Issue 10, 2003, Pages 1060-1075

  Andringa, Gerda ^a   Du, Fu ^b   Chase, Thomas N ^a   Bennett, M Catherine ^a,c  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b FD Neuro Technologies Inc   (United States)

^c Blanchette Rockefeller Neurosciences Institute   (United States)

Author keywords

Immunohistochemistry; Neuron; Parkinson disease; Rodent; Subcellular distribution; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY SYNUCLEIN 1; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; BRAIN STEM; CELL POPULATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; DISEASE PREDISPOSITION; ENTORHINAL CORTEX; FOREBRAIN; GENE LOCUS; HIPPOCAMPUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; LEWY BODY; MALE; MESENCEPHALON; NEOCORTEX; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PYRIFORM CORTEX; RAT; THALAMUS;

EID: 0141891162     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/62.10.1060     Document Type: Article

References (62)

1. Polymeropoulos MH, Lavedan C, Leroy E, et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997;276:2045-47
2. Kruger R, Kuhn W, Muller T, et al. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet 1998;18:106-8
3. Feany MB, Bender WW. A Drosophila model of Parkinson's disease. Nature 2000;23:394-98
4. Masliah E, Rockenstein E, Veinbergs I, et al. Dopaminergic loss and inclusion body formation in alpha-synuclein mice: Implications for neurodegenerative disorders. Science 2000;287:1265-69
5. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M. Alpha-synuclein in Lewy bodies. Nature 1997;28:839-40
6. Baba M, Nakajo S, Tu PH, et al. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am J Pathol 1998;152:879-84
7. Mezey E, Dehejia AM, Harta G, et al. Alpha synuclein is present in Lewy bodies in sporadic Parkinson's disease. Mol Psychiat 1998;3:493-99
8. Mattila PM, Rinne JO, Helenius H, Dickson DW, Roytta M. Alpha-synuclein-immunoreactive cortical Lewy bodies are associated with cognitive impairment in Parkinson's disease. Acta Neuropathol 2000;100:285-90
9. Iwai A, Masliah E, Yoshimoto M, et al. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 1995;14:467-75
10. Irizarry MC, Kim TW, McNamara M, Tanzi RE, et al. Characterization of the precursor protein of the non-Abeta component of senile plaques (NACP) in the human central nervous system. J Neuropathol Exp Neurol 1996;55:889-95
11. Mezey E, Dehejia A, Harta G, Papp MI, Polymeropoulos MH, Brownstein MJ. Alpha synuclein in neurodegenerative disorders: Murderer or accomplice? Nat Med 1998;4:755-57
12. Lippa CF, Fujiwara H, Mann DM, et al. Lewy bodies contain altered alpha-synuclein in brains of many familial Alzheimer's disease patients with mutations in presenilin and amyloid precursor protein genes. Am J Pathol 1998;153:1365-70
13. Lippa CF, Schmidt ML, Lee VM, Trojanowski JQ. Antibodies to alpha-synuclein detect Lewy bodies in many Down's syndrome brains with Alzheimer's disease. Ann Neurol 1999;45:353-57
14. Tu PH, Galvin JE, Baba M, et al. Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann Neurol 1998;44:415-22
15. Wakabayashi K, Hayashi S, Kakita A, et al. Accumulation of alpha-synuclein/NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy. Acta Neuropathol 1998;96:445-52
16. Wakabayashi K, Yoshimoto M, Tsuji S, Takahashi H. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci Lett 1998;249:180-82
17. Charles V, Mezey E, Reddy PH, et al. Alpha-synuclein immunoreactivity of huntingtin polyglutamine aggregates in striatum and cortex of Huntington's disease patients and transgenic mouse models. Neurosci Lett 2000;289:29-32
18. Ohama E, Ikuta F. Parkinson's disease distribution of Lewy bodies and monoamine neuron system. Acta Neuropathol 1976;26:311-19
19. Gibb WR, Esiri MM, Lees AJ. Clinical and pathological features of diffuse cortical Lewy body disease (Lewy body dementia). Brain 1987;110:1131-53
20. Gibb WR, Lees AJ. The significance of the Lewy body in the diagnosis of idiopathic Parkinson's disease. Neuropathol Appl Neurobiol 1989;15:27-44
21. Hurtig HI, Trojanowski JQ, Galvin, et al. Alpha-synuclein cortical Lewy bodies correlate with dementia in Parkinson's disease. Neurology 2000;23:1916-21
22. Halliday GM, Li YW, Blumbergs PC, et al. Neuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease. Ann Neurol 1990;27:373-85
23. Jakes R, Spillantini MG, Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett 1994;23:27-32
24. Masliah E, Iwai A, Mallory M, Ueda K, Saitoh T Altered presynaptic protein NACP is associated with plaque formation and neurodegeneration in Alzheimer's disease. Am J Pathol 1996;148:201-10
25. Petersen K, Olesen OF. Mikkelsen JD. Developmental expression of alpha-synuclein in rat hippocampus and cerebral cortex. Neurosci 1999;91:651-59
26. Tobe T, Nakajo S, Tanaka A, et al. Cloning and characterization of the cDNA encoding a novel brain-specific 14-kDa protein. J Neurochem 1992;59:1624-29
27. Alvord EC, Jr, Forno LS, Kusske JA, Kauffman RJ, Rhodes JS, Goetowski CR. The pathology of Parkinsonism: A comparison of degenerations in cerebral cortex and brainstem. Adv Neurol 1974;5:175-93
28. Jensen PH, Nielsen MS, Jakes R, Dotti CG, Goedert M. Binding of alpha-synuclein to brain vesicles is abolished by familial Parkinson's disease mutation. J Biol Chem 1998;273:26292-94
29. Leng Y, Chase TN, Bennett MC. Muscarinic receptor stimulation induces translocation of an alpha-synuclein oligomer from plasma membrane to a light vesicle fraction in cytoplasm. J Biol Chem 2001;276:28212-18
30. Andringa G, Du F, Chase TN, Bennett MC. Mapping of α-Synuclein in Rat Brain: Presence in Neuronal Cell Bodies Defines Subset of Neurons Vulnerable to Lewy Body Formation [Abstract]. Society for Neuroscience, San Diego, CA, 2001;545:4
31. Galvin JE, Schuck TM, Lee VM, Trojanowski JQ. Differential expression and distribution of alpha-, beta-, and gamma-synuclein in the developing human substantia nigra. Exp Neurol 2001;168:347-55
32. Giasson BI, Duda JE, Forman MS, Lee VM, Trojanowski JQ. Prominent perikaryal expression of alpha- and beta-synuclein in neurons of dorsal root ganglion and in medullary neurons. Exp Neurol 2001;172:354-62
33. Fallon JH, Laughin SE. Substantia nigra. In: Paxinos G, ed. The rat nervous system, Vol. 1. Australia: Academic Press 1985:353-74
34. Beckstead RM, Domesick VB, Nauta WJ. Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res 1979;19:191-217
35. McGeorge AJ, Faull RL. The organization of the projection from the cerebral cortex to the striatum in the rat. Neurosci 1989;29:503-5
36. Ottersen OP. Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J Comp Neurol 1982;10:30-48
37. Russchen FT. Cortical and subcortical afferents of the amygdaloid complex. Adv Exp Med Biol 1986;203:35-52
38. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. New York: Academic Press, 1982
39. Woolf NJ, Butcher LL. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 1986;16:603-37
40. Lowe J. Lewy bodies. In: Calne DB, ed. Neurodegenerative diseases. Philadelphia: WB Saunders Co, 1994:51-69
41. Dymecki J, Lechowicz W, Bertrand E, Szpak GM. Changes in dopaminergic neurons of the mesocorticolimbic system in Parkinson's disease. Folia Neuropathol 1996;34:102-6
42. McRitchie DA, Cartwright HR, Halliday GM. Specific A 10 dopaminergic nuclei in the midbrain degenerate in Parkinson's disease. Exp Neurol 1997;144:202-13
43. Jellinger KA. Pathology of Parkinson's disease: Changes other than the nigrostriatal pathway. Mol Chem Neuropathol 1991;14:153-97
44. Gomez-Tortosa E, Newell K, Irizarry MC, Sanders JL, Hyman BT. Alpha-synuclein immunoreactivity in dementia with Lewy bodies: Morphological staging and comparison with ubiquitin immunostaining. Acta Neuropathol 2000;99:352-57
45. Irizarry MC, Growden W, Gomez-Isla T Nigral and cortical neurites in Parkinson's disease and cortical Lewy body disease contain α-synuclein immunoreactivity. J Neuropathol Exp Neurol 1998;57:334-37
46. 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 1999;9:67-69
47. Maroteaux L, Scheller RH. The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res Mol Brain Res 1991;11:335-43
48. Masliah E, Rockenstein E, Veinbergs I, et al. Beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci USA 2001;9:12245-50
49. Mori F, Tanji K, Yoshimoto M, Takashashi H, Wakabayashi K. Demonstration of alpha-synuclein immunoreactivity in neuronal and glial cytoplasm in normal human brain tissue using proteinase K and formic acid pretreatment. Exp Neurol 2002;176:98-104
50. Davidson WS, Jonas A, Clayton DF, George JM. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 1998;273:9443-49
51. Perrin RJ, Woods WS, Clayton DF. George JM. Interaction of human alpha-synuclein and Parkinson's disease variants with phospholipids: Structural analysis using site-directed mutagenesis. J Biol Chem 2000;44:34393-98
52. Braak H, Braak E, Yilmazer D, et al. Amygdala pathology in Parkinson's disease. Acta Neuropathol 1994;88:493-500
53. Braak E, Sandmann-Keil D, Rub U, et al. alpha-Synuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol 2001;101:195-201
54. Forno LS, Alvord EC. Depigmentation in the nerve cells of the substantia nigra and locus coeruleus in Parkinsonism. Adv Neurol 1974;5:195-202
55. Henderson JM, Carpenter K, Cartwright H, Halliday GM. Loss of thalamic intralaminar nuclei in progressive supranuclear palsy and Parkinson's disease: Clinical and therapeutic implications. Brain 2000;123:1410-21
56. Iwanaga K, Wakabayashi K, Yoshimoto M, et al. Lewy body-type degeneration in cardiac plexus in Parkinson's and incidental Lewy body diseases. Neurol 1999;52:1269-71
57. Kakita A, Takahashi H, Homma Y, Ikuta F. Lewy bodies in the cerebellar dentate nucleus of a patient with Parkinson's disease. Pathol Int 1994;44:878-80
58. Kremer HP, Bots GT. Lewy bodies in the lateral hypothalamus: Do they imply neuronal loss? Mov Disord 1993;8:315-20
59. Langston JW, Forno LS. The hypothalamus in Parkinson disease. Ann Neurol 1978;3:129-33
60. Mattila PM, Roytta M, Torikka H, Dickson DW, Rinne JO. Cortical Lewy bodies and Alzheimer-type changes in patients with Parkinson's disease. Acta Neuropathol 1998;95:576-82
61. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, Goedert M. Alpha-synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc Natl Acad Sci USA 1998;95:6469-73
62. Ulfig N, Braak E, Braak H. Changes within the basal nucleus in Parkinson's disease. Prog Clin Biol Res 1989;317:493-500