Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein

European Journal of Neuroscience

Volumn 29, Issue 5, 2009, Pages 879-890

  Marxreiter, Franz ^b   Nuber, Silke ^c   Kandasamy, Mahesh ^b   Klucken, Jochen ^b,e   Aigner, Robert ^b,e   Burgmayer, Ralf ^b   Couillard Despres, Sebastien ^b   Riess, Olaf ^c   Winkler, Jürgen ^d,e   Winner, Beate ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Adult neurogenesis; Neural progenitor cells; Parkinson disease; Subventricular zone; Synucleinopathies

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; TETRACYCLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CENTRAL NERVOUS SYSTEM DISEASE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE; SYNUCLEINOPATHY;

ALANINE; ALPHA-SYNUCLEIN; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DEATH; CELL PROLIFERATION; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NEUROGENESIS; NEURONS; NEUROPEPTIDES; OLFACTORY BULB; PROLIFERATING CELL NUCLEAR ANTIGEN; PROLINE;

EID: 61449087466     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06641.x     Document Type: Article

References (42)

1. Berendse, H.W., Booij, J., Francot, C.M., Bergmans, P.L., Hijman, R., Stoof, J.C. Wolters, E.C. (2001) Subclinical dopaminergic dysfunction in asymptomatic Parkinson's disease patients' relatives with a decreased sense of smell. Ann. Neurol., 50, 34 41.
2. Biebl, M., Winner, B. Winkler, J. (2005) Caspase inhibition decreases cell death in regions of adult neurogenesis. Neuroreport, 16, 1147 1150.
3. Braak, H., Sandmann-Keil, D., Gai, W. Braak, E. (1999) Extensive axonal Lewy neurites in Parkinson's disease: a novel pathological feature revealed by alpha-synuclein immunocytochemistry. Neurosci. Lett., 265, 67 69.
4. Braak, H., Del Tredici, K., Rub, U., de Vos, R.A., Jansen Steur, E.N. Braak, E. (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging, 24, 197 211.
5. Carleton, A., Petreanu, L.T., Lansford, R., Alvarez-Buylla, A. Lledo, P.M. (2003) Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci., 6, 507 518.
6. Conway, K.A., Harper, J.D. Lansbury, P.T. (1998) Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med., 4, 1318 1320.
7. Conway, K.A., Lee, S.J., Rochet, J.C., Ding, T.T., Williamson, R.E. Lansbury, P.T. Jr. (2000) Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl Acad. Sci. USA, 97, 571 576.
8. Conway, K.A., Rochet, J.C., Bieganski, R.M. Lansbury, P.T. Jr. (2001) Kinetic stabilization of the alpha-synuclein protofibril by a dopamine-alpha-synuclein adduct. Science, 294, 1346 1349.
9. Curtis, M.A., Kam, M., Nannmark, U., Anderson, M.F., Axell, M.Z., Wikkelso, C., Holtas, S., van Roon-Mom, W.M., Bjork-Eriksson, T., Nordborg, C., Frisen, J., Dragunow, M., Faull, R.L. Eriksson, P.S. (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 315, 1243 1249.
10. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. Alvarez-Buylla, A. (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 97, 703 716.
11. 2+/calmodulin-dependent protein kinase in rat brain. J. Neurosci., 5, 3270 3277.
12. 2+/calmodulin-dependent protein kinase II in developing P19 neurons. Int. J. Dev. Neurosci., 20, 585 592.
13. Fleming, S.M., Tetreault, N.A., Mulligan, C.K., Hutson, C.B., Masliah, E. Chesselet, M.F. (2008) Olfactory deficits in mice overexpressing human wildtype alpha-synuclein. Eur. J. Neurosci., 28, 247 256.
14. Freichel, C., Neumann, M., Ballard, T., Muller, V., Woolley, M., Ozmen, L., Borroni, E., Kretzschmar, H.A., Haass, C., Spooren, W. Kahle, P.J. (2007) Age-dependent cognitive decline and amygdala pathology in alpha-synuclein transgenic mice. Neurobiol. Aging, 28, 1421 1435.
15. Gai, W.P., Blessing, W.W. Blumbergs, P.C. (1995) Ubiquitin-positive degenerating neurites in the brainstem in Parkinson's disease. Brain, 118 (Pt 6 1447 1459.
16. Gallyas, F. (1971) Silver staining of Alzheimer's neurofibrillary changes by means of physical development. Acta Morphol Acad Sci Hung, 19, 1 8.
17. Gavrieli, Y., Sherman, Y. Ben-Sasson, S.A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119, 493 501.
18. Giasson, B.I., Murray, I.V., Trojanowski, J.Q. Lee, V.M. (2001) A hydrophobic stretch of 12 amino acid residues in the middle of alpha-synuclein is essential for filament assembly. J. Biol. Chem., 276, 2380 2386.
19. Gibb, W.R. Lees, A.J. (1988) The relevance of the Lewy body to the pathogenesis of idiopathic Parkinson's disease. J. Neurol. Neurosurg. Psychiatry, 51, 745 752.
20. Gossen, M. Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA, 89, 5547 5551.
21. Gundersen, H.J., Bendtsen, T.F., Korbo, L., Marcussen, N., Moller, A., Nielsen, K., Nyengaard, J.R., Pakkenberg, B., Sorensen, F.B. Vesterby, A. (1988) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis, 96, 379 394.
22. Kahle, P.J., Neumann, M., Ozmen, L., Muller, V., Jacobsen, H., Schindzielorz, A., Okochi, M., Leimer, U., van Der Putten, H., Probst, A., Kremmer, E., Kretzschmar, H.A. Haas, C. (2000) Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha synuclein in human and transgenic mouse brain. J. Neurosci., 20, 6365 6373.
23. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J.T., Schols, L. Riess, O. (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet., 18, 106 108.
24. Lois, C., Garcia-Verdugo, J.M. Alvarez-Buylla, A. (1996) Chain migration of neuronal precursors. Science, 271, 978 981.
25. Mansuy, I.M., Winder, D.G., Moallem, T.M., Osman, M., Mayford, M., Hawkins, R.D. Kandel, E.R. (1998) Inducible and reversible gene expression with the rtTA system for the study of memory. Neuron, 21, 257 265.
26. Maskri, L., Zhu, X., Fritzen, S., Kuhn, K., Ullmer, C., Engels, P., Andriske, M., Stichel, C.C. Lubbert, H. (2004) Influence of different promoters on the expression pattern of mutated human alpha-synuclein in transgenic mice. Neurodegener. Dis., 1, 255 265.
27. Mayford, M., Bach, M.E., Huang, Y.Y., Wang, L., Hawkins, R.D. Kandel, E.R. (1996) Control of memory formation through regulated expression of a CaMKII transgene. Science, 274, 1678 1683.
28. Montgomery, E.B. Jr., Koller, W.C., LaMantia, T.J., Newman, M.C., Swanson-Hyland, E., Kaszniak, A.W. Lyons, K. (2000) Early detection of probable idiopathic Parkinson's disease: I. Development of a diagnostic test battery. Mov. Disord., 15, 467 473.
29. Neumann, M., Kahle, P.J., Giasson, B.I., Ozmen, L., Borroni, E., Spooren, W., Muller, V., Odoy, S., Fuuiwara, H., Hasegawa, M., Iwatsubo, T., Trojanowski, J.Q., Kretzschmar, H.A. Haas, C. (2002) Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleinopathies. J. Clin. Invest., 110, 1429 1439.
30. Nuber, S., Petrasch-Parwez, E., Winner, B., Winkler, J., von Horsten, S., Schmidt, T., Boy, J., Kuhn, M., Nguyen, H.P., Teismann, P., Schulz, J.B., Neumann, M., Pichler, B.J., Reischl, G., Holzmann, C., Schmitt, I., Bornemann, A., Kuhn, W., Zimmermann, F., Servadio, A. Riess, O. (2008) Neurodegeneration and motor dysfunction in a conditional model of Parkinson's disease. J. Neurosci., 28, 2471 2484.
31. Ouimet, C.C., McGuinness, T.L. Greengard, P. (1984) Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc. Natl Acad. Sci. USA, 81, 5604 5608.
32. Paxinos, G. Franklin, K.B. (2001) The Mouse Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, San Diego, CA.
33. Sanai, N., Tramontin, A.D., Quinones-Hinojosa, A., Barbaro, N.M., Gupta, N., Kunwar, S., Lawton, M.T., McDermott, M.W., Parsa, A.T., Manuel-Garcia Verdugo, J., Berger, M.S. Alvarez-Buylla, A. (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature, 427, 740 744.
34. Schneider, B.L., Seehus, C.R., Capowski, E.E., Aebischer, P., Zhang, S.C. Svendsen, C.N. (2007) Over-expression of alpha-synuclein in human neural progenitors leads to specific changes in fate and differentiation. Hum. Mol. Genet., 16, 651 666.
35. Shults, C.W., Rockenstein, E., Crews, L., Adame, A., Mante, M., Larrea, G., Hashimoto, M., Song, D., Iwatsubo, T., Tsuboi, K. Masliah, E. (2005) Neurological and neurodegenerative alterations in a transgenic mouse model expressing human alpha-synuclein under oligodendrocyte promoter: implications for multiple system atrophy. J. Neurosci., 25, 10689 10699.
36. Siderowf, A., Newberg, A., Chou, K.L., Lloyd, M., Colcher, A., Hurtig, H.I., Stern, M.B., Doty, R.L., Mozley, P.D., Wintering, N., Duda, J.E., Weintraub, D. Moberg, P.J. (2005) [99mTc]TRODAT-1 SPECT imaging correlates with odor identification in early Parkinson disease. Neurology, 64, 1716 1720.
37. Spillantini, M.G., Schmidt, M.L., Lee, V.M., Trojanowski, J.Q., Jakes, R. Goedert, M. (1997) Alpha-synuclein in Lewy bodies. Nature, 388, 839 840.
38. Valente, E.M., Salvi, S., Ialongo, T., Marongiu, R., Elia, A.E., Caputo, V., Romito, L., Albanese, A., Dallapiccola, B. Bentivoglio, A.R. (2004) PINK1 mutations are associated with sporadic early-onset parkinsonism. Ann. Neurol., 56, 336 341.
39. Winner, B., Cooper-Kuhn, C.M., Aigner, R., Winkler, J. Kuhn, H.G. (2002) Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb. Eur. J. Neurosci., 16, 1681 1689.
40. Winner, B., Lie, D.C., Rockenstein, E., Aigner, R., Aigner, L., Masliah, E., Kuhn, H.G. Winkler, J. (2004) Human wild-type alpha-synuclein impairs neurogenesis. J. Neuropathol. Exp. Neurol., 63, 1155 1166.
41. Winner, B., Rockenstein, E., Lie, D.C., Aigner, R., Mante, M., Bogdahn, U., Couillard-Depres, S., Masliah, E. Winkler, J. (2007) Mutant alpha-synuclein exacerbates age-related decrease of neurogenesis. Neurobiol. Aging, 29, 913 925.
42. Xu, J., Kao, S.Y., Lee, F.J., Song, W., Jin, L.W. Yankner, B.A. (2002) Dopamine-dependent neurotoxicity of alpha-synuclein: a mechanism for selective neurodegeneration in Parkinson disease. Nat. Med., 8, 600 606.