The expression of α-, β-, and γ-synucleins in olfactory mucosa from patients with and without neurodegenerative diseases

Experimental Neurology

Volumn 160, Issue 2, 1999, Pages 515-522

  Duda, John E ^a   Shah, Usman ^a   Arnold, Steven E ^a   Lee, Virginia M Y ^a   Trojanowski, John Q ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Alzheimer's disease; Multiple system atrophy; Neuronal plasticity; Olfactory epithelium; Parkinson's disease; Regeneration; Synuclein proteins; Synucleinopathies

Indexed keywords

ALPHA SYNUCLEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CELL REGENERATION; CONTROLLED STUDY; DEGENERATIVE DISEASE; FEMALE; HUMAN; HUMAN TISSUE; LEWY BODY; MALE; NERVE CELL PLASTICITY; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHY DRAGER SYNDROME; SYNAPTOSOME;

EID: 0032763540     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1999.7228     Document Type: Article

References (39)

1. Clayton D. F., George J. M. The synucleins: A family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci. 21:1998;249-254.
2. Crino P. B., Martin J. A., Hill W. D., Greenberg B., Lee V. M. Y., Trojanowski J. Q. Beta-Amyloid peptide and amyloid precursor proteins in olfactory mucosa of patients with Alzheimer's disease, Parkinson's disease, and Down syndrome. Ann. Otol. Rhinol. Laryngol. 104:1995;655-661.
3. Doty R. L., Reyes P. F., Gregor T. Presence of both odor identification and detection deficits in Alzheimer's disease. Brain Res. Bull. 18:1987;597-600.
4. Doty R. L., Riklan M., Deems D. A., Reynolds C., Stellar S. The olfactory and cognitive deficits of Parkinson's disease: Evidence for independence. Ann. Neurol. 25:1989;166-171.
5. George J. M., Jin H., Woods W. S., Clayton D. F. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron. 15:1995;361-372.
6. Giasson B., Uryu K., Trojanowski J. Q., Lee V. M. Y. Mutant and wild type human alpha-synucleins assemble into elongated filaments with distinct morphologies in vitro. J. Biol. Chem. 274:1999;7619-7622.
7. Gilman S., Low P. A., Quinn N., Albanese A., Ben-Shlomo Y., Fowler C. J., Kaufmann H., Klockgether T., Lang A. E., Lantos P. L., Litvan I., Mathias C. J., Oliver E., Robertson D., Schatz I., Wenning G. K. Consensus statement on the diagnosis of multiple system atrophy. J. Neurolog. Sci. 163:1999;94-98.
8. Graziadei, P. P. C., and G. A. Monti-Graziadei. 1978. Continuous nerve cell renewal in the olfactory system. In Handbook of Sensory Physiology, Vol. IX: Development of Sensory SystemsM. Jacobson, Ed., pp. 55-83. Springer-Verlag, New York.
9. Hsu L. J., Mallory M., Xia Y., Veinbergs I., Hashimoto M., Yoshimoto M., Thal L. J., Saitoh T., Masliah E. Expression pattern of synucleins (non-Abeta component of Alzheimer's disease amyloid precursor protein/alpha-synuclein) during murine brain development. J. Neurochem. 71:1998;338-344.
10. Iseki E., Marvi W., Kosaka K., Akiyama H., Ueda K., Iwatsubo T. Degenerative terminals of the perforant pathway are human alpha-synuclein immunoreactive in the hippocampus of patients with diffuse Lewy body disease. Neurosci. Lett. 258:1998;81-84.
11. Jin H., Clayton D. F. Synelfin regulation during the critical period for song learning in normal and isolated juvenile zebra finches. Neurobiol. Learn. Mem. 68:1997;271-284.
12. Kruger R., Kuhn W., Muller T., Woitalla D., Graeber M., Kosel S., Przuntek H., Epplen J. T., Schols L., Riess O. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Gen. 18:1998;106-108.
13. Kulkarni-Narla A., Getchell T. V., Schmitt F. A., Getchell M. L. Manganese and copper-zinc superoxide dismutases in the human olfactory mucosa: Increased immunoreactivity in Alzheimer's disease. Exp. Neurol. 140:1996;115-125.
14. Lanza D. C., Moran D. T., Doty R. L., Trojanowski J. Q., Lee J. H., Rowley J. C. III, Kennedy D. W. Endoscopic human olfactory biopsy technique: A preliminary report. Laryngoscope. 103:1993;815-819.
15. Lavedan C. The synuclein family. Genome Res. 8:1998;871-880.
16. Lee J. H., Goedert M., Hill W. D., Lee V. M. Y., Trojanowski J. Q. Tau proteins are abnormally expressed in olfactory epithelium of Alzheimer patients and developmentally regulated in human fetal spinal cord. Exp. Neurol. 121:1993;93-105.
17. Lippa C. F., Fujiwara H., Mann D. M. A., Giasson B., Baba M., Schmidt M. L., Nee L. E., O'Connell B., Pollen D. A., St P., Ghetti B., Nochlin D., Bird T. D., Cairns N. J., Lee V. M. Y., Iwatsubo T., Trojanowski J. Q. 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. Path. 153:1998;1365-1370.
18. Lippa C. F., Schmidt M. L., Lee V. M. Y., Trojanowski J. Q. Antibodies to alpha-synuclein detect Lewy bodies in many Down's syndrome brains with Alzheimer's disease. Ann. Neurol. 45:1999;353-357.
19. Lovell M. A., Jafek B. W., Moran D. T., Rowley J. C. Biopsy of human olfactory mucosa. An instrument and a technique. Arch. Otolaryngol. 108:1982;247-249.
20. Mezey E., Dehejia A., Harta G., Papp M. I., Polymeropoulos M. H., Brownstein M. J. Alpha-synuclein in neurodegenerative disorders: Murderer or accomplice. Nat. Med. 4:1998;755-757.
21. Nee L. E., Scott J., Polinsky R. J. Olfactory dysfunction in the Shy-Drager syndrome. Clin. Autonom. Res. 3:1993;281-282.
22. Papadimitriou A., Veletza V., Hadjigeorgiou G. M., Patrikiou A., Hirano M., Anastasopoulos I. Mutated alpha-synuclein gene in two Greek Kindreds with familial PD; Incomplete penetrance. Neurology. 52:1999;651-654.
23. Polymeropoulos M. H., Lavedan C., Leroy E., Ide S. E., Dehejia A., Dutra B., Pike H., Root J., Rubenstein R., Boyer E. S., Stenroos S., Chandrasekharappa A., Athanassiadou T., Papapetropoulos W. G., Johnson A. M., Lazzarini R. C., Duvoisin G., Di Iorio L. I., Golbe, Nussbaum R. L. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047.
24. Smutzer G., Lee V. M. Y., Trojanowski J. Q., Arnold S. E. Human olfactory mucosa in schizophrenia. Ann. Otol. Rhinol. Laryngol. 107:1998;349-355.
25. Spillantini M. G., Crowther R. A., Jakes R., Cairns N. J., Lantos P. L., Goedert M. Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci. Lett. 251:1998;205-208.
26. Spillantini M. G., Crowther R. A., Jakes R., Hasegawa M., Goedert M. Alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc. Nat. Acad. Sci. USA. 95:1998;6469-6473.
27. Spillantini M. G., Schmidt M. L., Lee V. M. Y., Trojanowski J. Q., Jakes R., Goedert M. Alpha-synuclein in Lewy bodies. Nature. 388:1997;839-840.
28. Talamo B. R., Rudel R., Kosik K. S., Lee V. M. Y., Neff S., Adelman, Kauer J. S. Pathological changes in olfactory neurons in patients with Alzheimer's disease. Nature. 337:1989;736-739.
29. Trojanowski J. Q., Newman P. D., Hill W. D., Lee V. M. Y. Human olfactory epithelium in normal aging, Alzheimer's disease, and other neurodegenerative disorders. J. Comp. Neurol. 310:1991;365-376.
30. Trojanowski J. Q., Schuck T., Schmidt M. L., Lee V. M. Y. The distribution of tau in the normal human nervous system. J. Histochem. Cytochem. 37:1989;209-215.
31. Tu P. H., Galvin J. E., Baba M., Giasson B., Tomita T., Leight S., Nakajo S., Iwatsubo T., Trojanowski J. Q., Lee V. M. Y. Glial cytoplasmic inclusions in white matter oligodendrocytes of multiple system atrophy brains contain insoluble alpha-synuclein. Ann. Neurol. 44:1998;415-422.
32. Wakabayashi K., Hayashi S., Kakita A., Yamada M., Toyoshima Y., Yoshimoto M., Takahashi H. Accumulation of alpha-synuclein/NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy. Acta Neuropathol. 96:1998;445-452.
33. 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.
34. 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.
35. Wenning G. K., Shephard B., Hawkes C., Petruckevitch A., Lees A., Quinn N. Olfactory function in atypical parkinsonian syndromes. Acta Neurol. Scan. 91:1995;247-250.
36. Withers G. S., George J. M., Banker G. A., Clayton D. F. Delayed localization of synelfin (synuclein, NACP) to presynaptic terminals in cultured rat hippocampal neurons. Dev. Brain Res. 99:1997;87-94.
37. Yachnis A. T., Trojanowski J. Q. Studies of childhood brain tumors using immunohistochemistry and microwave technology: Methodological considerations. J. Neurosci. Methods. 55:1994;191-200.
38. Yamagishi M., Getchell M. L., Takami S., Getchell T. V. Increased density of olfactory receptor neurons immunoreactive for apolipoprotein E in patients with Alzheimer's disease. Ann. Otol. Rhinol. Laryngol. 107:1998;421-426.
39. Yamagishi M., Takami S., Getchell T. V. Ontogenetic expression of spot 35 protein (calbindin-D28k) in human olfactory receptor neurons and its decrease in Alzheimer's disease patients. Ann. Otol. Rhinol. Laryngol. 105:1996;132-139.