Pathological α-synuclein impairs adult-born granule cell development and functional integration in the olfactory bulb

Nature Communications

Volumn 5, Issue , 2014, Pages

  Neuner, Johanna ^a   Ovsepian, Saak V ^b   Dorostkar, Mario ^a   Filser, Severin ^b   Gupta, Aayush ^a   Michalakis, Stylianos ^a   Biel, Martin ^a   Herms, Jochen ^b,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^c Center for Integrated Protein Science Munich ^*  (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; 4 AMINOBUTYRIC ACID RECEPTOR; MUTANT PROTEIN; SNCA PROTEIN, MOUSE;

BRAIN; GRANULAR MEDIUM; NEUROLOGY; OLFACTION; PATHOLOGY; RODENT; SYMPTOM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DENDRITE; ELECTRIC CAPACITANCE; GRANULE CELL; IN VIVO STUDY; INTEGRATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY BULB; PARKINSON DISEASE; SYSTEMATIC REVIEW; AGING; ANIMAL; CYTOLOGY; DENDRITIC SPINE; EXCITATORY POSTSYNAPTIC POTENTIAL; MALE; METABOLISM; SURVIVAL; SYNAPSE; TRANSGENIC MOUSE;

AGING; ALPHA-SYNUCLEIN; ANIMALS; DENDRITIC SPINES; EXCITATORY POSTSYNAPTIC POTENTIALS; GABAERGIC NEURONS; MALE; MICE; MICE, TRANSGENIC; MUTANT PROTEINS; OLFACTORY BULB; SURVIVAL ANALYSIS; SYNAPSES;

EID: 84901715819     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4915     Document Type: Article

References (61)

1. Petreanu, L. & Alvarez-Buylla, A. Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106-6113 (2002). (Pubitemid 35387653)
2. Ming, G. L. & Song, H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70, 687-702 (2011).
3. Alonso, M. et al. Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb. J. Neurosci. 26, 10508-105013 (2006).
4. Mandairon, N., Stack, C., Kiselycznyk, C. & Linster, C. Enrichment to odors improves olfactory discrimination in adult rats. Behav. Neurosci. 120, 173-179 (2006). (Pubitemid 43345114)
5. Marxreiter, F., Regensburger, M. & Winkler, J. Adult neurogenesis in Parkinson's disease. Cell. Mol. Life Sci. 70, 459-473 (2013).
6. Shepherd, G. M., Chen, W. R., Willhite, D., Migliore, M. & Greer, C. A. The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res. Rev. 55, 373-382 (2007). (Pubitemid 47538754)
7. Lazarini, F. & Lledo, P. M. Is adult neurogenesis essential for olfaction? Trends Neurosci. 34, 20-30 (2011).
8. Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A. & Lledo, P. M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6, 507-518 (2003). (Pubitemid 36514699)
9. Lledo, P. M. & Saghatelyan, A. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci. 28, 248-254 (2005). (Pubitemid 41556909)
10. Kosaka, K. & Kosaka, T. Chemical properties of type 1 and type 2 periglomerular cells in the mouse olfactory bulb are different from those in the rat olfactory bulb. Brain Res. 1167, 42-55 (2007). (Pubitemid 47302430)
11. Rall, W., Shepherd, G. M., Reese, T. S. & Brightman, M. W. Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44-56 (1966).
12. Price, J. L. & Powell, T. P. The synaptology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 125-155 (1970).
13. Isaacson, J. S. & Strowbridge, B. W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20, 749-761 (1998). (Pubitemid 28199053)
14. Breton-Provencher, V., Lemasson, M., Peralta, M. R. & Saghatelyan, A. Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. J. Neurosci. 29, 15245-15257 (2009).
15. Nissant, A. & Pallotto, M. Integration and maturation of newborn neurons in the adult olfactory bulb-from synapses to function. Eur. J. Neurosci. 33, 1069-1077 (2011).
16. Braithwaite, S. P., Stock, J. B. & Mouradian, M. M. a-Synuclein phosphorylation as a therapeutic target in Parkinson's disease. Rev. Neurosci. 23, 191-198 (2012).
17. 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. 2, 166-171 (1989). (Pubitemid 19051250)
18. Braak, H. et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211 (2003). (Pubitemid 36007810)
19. Ubeda-Bañon, I. et al. alpha-Synucleinopathy in the human olfactory system in Parkinson's disease: involvement of calcium-binding protein-and substance P-positive cells. Acta Neuropathol. 119, 723-735 (2010).
20. Sanai, N., Nguyen, T. & Ihrie, R. A. Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478, 382-386 (2011).
21. Huart, C., Rombaux, P. & Hummel, T. Plasticity of the human olfactory system: the olfactory bulb. Molecules 18, 11586-11600 (2013).
22. Lötsch, J. et al. Functional genomics suggest neurogenesis in the adult human olfactory bulb. Brain Struct. Funct. (doi:10, 1007/s00429-013-0618- 3).
23. Kahle, P. J. et al. Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha synuclein in human and transgenic mouse brain. J. Neurosci. 20, 6365-6373 (2000).
24. Kollias, G. et al. Differential regulation of a Thy-1 gene in transgenic mice. Proc. Natl Acad. Sci. USA 84, 1492-1496 (1987).
25. Neuner, J., Filser, S., Michalakis, S., Biel, M. & Herms, J. A30P a-synuclein interferes with the stable integration of adult-born neurons into the olfactory bulb. Sci. Rep. 4, 1-9 (2014).
26. Mizrahi, A. Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat. Neurosci. 10, 444-452 (2007). (Pubitemid 46494595)
27. Livneh, Y., Feinstein, N., Klein, M. & Mizrahi, A. Sensory input enhances synaptogenesis of adult-born neurons. J. Neurosci. 29, 86-97 (2009).
28. Lepousez, G., Valley, M. T. & Lledo, P. M. The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu. Rev. Physiol. 75, 339-363 (2013).
29. Leuba, G. Aging of dendrites in the cerebral cortex of the mouse. Neuropathol. Appl. Neurobiol. 9, 467-475 (1983). (Pubitemid 14178206)
30. Yamaguchi, M. & Mori, K. Critical period for sensory experience-dependent survival of newly generated granule cells in the adult mouse olfactory bulb. Proc. Natl Acad. Sci. USA 102, 9697-9702 (2005). (Pubitemid 40981743)
31. Kelsch, W., Lin, C. W., Mosley, C. P. & Lois, C. A critical period for activity-dependent synaptic development during olfactory bulb adult neurogenesis. J. Neurosci. 29, 11852-11858 (2009).
32. Katagiri, H. et al. Dynamic development of the first synapse impinging on adult-born neurons in the olfactory bulb circuit. Neural Syst. Circuits 1, 6 (2011).
33. Espinosa, F. & Kavalali, E. T. NMDA receptor activation by spontaneous glutamatergic neurotransmission. J. Neurophysiol. 101, 2290-2296 (2009).
34. Schoppa, N. E. AMPA/kainite receptors drive rapid output and precise synchrony in olfactory bulb granule cells. J. Neurosci. 26, 12996-13006 (2006). (Pubitemid 44954618)
35. Winner, B. et al. Human wild-type alpha-synuclein impairs neurogenesis. J. Neuropathol. Exp. Neurol. 63, 1155-1166 (2004). (Pubitemid 39492021)
36. Marxreiter, F. et al. Changes in adult olfactory bulb neurogenesis in mice expressing the A30P mutant form of alpha-synuclein. Eur. J. Neurosci. 29, 879-890 (2009).
37. Burré, J. et al. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329, 1663-1667 (2010)
38. Nemani, V. M. et al. Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65, 66-79 (2010).
39. Spillantini, M. G. et al. Alpha synuclein in Lewy bodies. Nature 388, 839-840 (1997).
40. McNeill, T. H., Brown, S. A., Rafols, J. A. & Shoulson, I. Atrophy of medium spiny I striatal dendrites in advanced Parkinson's disease. Brain Res. 455, 148-152 (1988).
41. Zaja-Milatovic, S. et al. Dendritic degeneration in neostriatal medium spiny neurons in Parkinson disease. Neurology 64, 545-547 (2005). (Pubitemid 40189880)
42. Jellinger, K. A. Interaction between pathogenic proteins in neurodegenerative disorders. J. Cell. Mol. Med. 16, 1166-1183 (2012).
43. Südhof, T. C. & Rizo, J. Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol. 1, a005637 (2011).
44. Ovsepian, S. V. & Dolly, J. O. Dendritic SNAREs add a new twist to the old neuron theory. Proc. Natl Acad. Sci. USA 108, 19113-19120 (2011)
45. Sousa, V. L. et al. {alpha}-synuclein and its A30P mutant affect actin cytoskeletal structure and dynamics. Mol. Biol. Cell 20, 3725-3739 (2009).
46. Tsaneva-Atanasova, K., Burgo, A., Galli, T. & Holcman, D. Quantifying neurite growth mediated by interactions among secretory vesicles, microtubules, and actin networks. Biophys. J. 96, 840-857 (2009).
47. Winner, B. et al. Role of a-synuclein in adult neurogenesis and neuronal maturation in the dentate gyrus. J. Neurosci. 32, 16906-16916 (2012).
48. Lim, Y. et al. alpha-Syn suppression reverses synaptic and memory defects in a mouse model of dementia with Lewy bodies. J. Neurosci. 31, 10076-10087 (2011).
49. Saghatelyan, A. et al. Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46, 103-116 (2005). (Pubitemid 40488315)
50. Ovsepian, S. V. & Friel, D. D. The leaner P/Q-type calcium channel mutation renders cerebellar Purkinje neurons hyper-excitable and eliminates Ca2 +-Na + spike bursts. Eur. J. Neurosci. 27, 93-103 (2008).
51. Häusser, M. & Clark, B. A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665-678 (1997). (Pubitemid 27430752)
52. Wall, M. J., Robert, A., Howe, J. R. & Usowicz, M. M. The speeding of EPSC kinetics during maturation of a central synapse. Eur. J. Neurosci. 15, 785-797 (2002). (Pubitemid 35463643)
53. Wall, M. J. & Usowicz, M. M. Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur. J. Neurosci. 9, 533-548 (1997).
54. Armstrong, C. M. & Gilly, W. F. Access resistance and space clamp problems associated with whole-cell patch clamping. Methods Enzymol. 207, 100-122 (1992).
55. Hüls, S. et al. AMPA-receptor-mediated excitatory synaptic transmission is enhanced by iron-induced a-synuclein oligomers. J. Neurochem. 117, 868-878 (2011).
56. Nusser, Z. et al. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559 (1998). (Pubitemid 28475506)
57. Abeliovich, A. et al. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239-352 (2000).
58. Mistŕik, P. et al. The murine HCN3 gene encodes a hyperpolarization-activated cation channel with slow kinetics and unique response to cyclic nucleotides. J. Biol. Chem. 280, 27056-27061 (2005). (Pubitemid 41040742)
59. Adam, Y. & Mizrahi, A. Long-term imaging reveals dynamic changes in the neuronal composition of the glomerular layer. J. Neurosci. 31, 7967-7973 (2011).
60. Dorostkar, M. M., Dreosti, E., Odermatt, B. & Lagnado, L. Computational processing of optical measurements of neuronal and synaptic activity in networks. J. Neurosci. Methods 188, 141-150 (2010).
61. Jung, C. K., Fuhrmann, M., Honarnejad, K., Van Leuven, F. & Herms, J. Role of presenilin 1 in structural plasticity of cortical dendritic spines in vivo. J. Neurochem. 119, 1064-1073 (2011).