Purkinje cell ataxin-1 Modulates climbing fiber synaptic input in developing and adult mouse cerebellum

Journal of Neuroscience

Volumn 33, Issue 13, 2013, Pages 5806-5820

  Ebner, Blake A ^a   Ingram, Melissa A ^a,b   Barnes, Justin A ^a,b   Duvick, Lisa A ^a   Frisch, Jill L ^a   Clark, H Brent ^a   Zoghbi, Huda Y ^c   Ebner, Timothy J ^b   Orr, Harry T ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAXIN 1; POLYGLUTAMINE; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CEREBELLUM; CEREBELLUM ATROPHY; CLIMBING FIBER; CONTROLLED STUDY; DISEASE SEVERITY; EVOKED RESPONSE; FLUORESCENCE IMAGING; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INNERVATION; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE; WESTERN BLOTTING;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBELLUM; DISABILITY EVALUATION; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; FLUORESCENT DYES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MUTAGENESIS, SITE-DIRECTED; MUTATION; NERVE FIBERS; NERVE TISSUE PROTEINS; NEUROPEPTIDES; NUCLEAR PROTEINS; OPTICAL IMAGING; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; RNA, MESSENGER; SPINOCEREBELLAR ATAXIAS; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84875457898     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6311-11.2013     Document Type: Article

References (46)

1. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. II. Phases in the maturation of Purkinje cells and of the molecular layer. J Comp Neurol 145:399-463. CrossRef Medline
2. Barnes JA, Ebner BA, Duvick LA, Gao W, Chen G, Orr HT, Ebner TJ (2011) Abnormalities in the climbing fiber-purkinje cell circuitry contribute to neuronal dysfunction in ATXN1[82Q] Mice. J Neurosci 31:12778-12789. CrossRef Medline
3. Bosman LW, Konnerth A (2009) Activity-dependent plasticity of developing climbing fiber-Purkinje cell synapses. Neuroscience 162:612-623. CrossRef Medline
4. Bravin M, Morando L, Vercelli A, Rossi F, Strata P (1999) Control of spine formation by electrical activity in the adult cerebellum. Proc Natl Acad Sci USA 96:1704-1709. CrossRef Medline
5. Burright EN, Clark HB, Servadio A, Matilla T, Feddersen RM, Yunis WS, Duvick LA, Zoghbi HY, Orr HT (1995) SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 82:937-948. CrossRef Medline
6. Cesa R, Strata P (2009) Axonal competition in the synaptic wiring of the cerebellar cortex during development and in the mature cerebellum. Neuroscience 162:624-632. CrossRef Medline
7. Clark HB, Burright EN, Yunis WS, Larson S, Wilcox C, Hartman B, Matilla A, Zoghbi HY, Orr HT (1997) Purkinje cell expression of a mutant allele of SCA1 in transgenic mice leads to disparate effects on motor behaviors, followed by a progressive cerebellar dysfunction and histological alterations. J Neurosci 17:7385-7395. Medline
8. Crepel F (1982) Regression of functional synapses in the immature mammalian cerebellum. Trends Neurosci 5:266-269. CrossRef
9. de Chiara C, Menon RP, Strom M, Gibson TJ, Pastore A (2009) Phosphorylation of S776 and 14-3-3 binding modulate ataxin-1 interaction with splicing factors. PLoS One 4:e8372. CrossRef Medline
10. De Zeeuw CI, Hansel C, Bian F, Koekkoek SK, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-508. CrossRef Medline
11. Duvick L, Barnes J, Ebner B, Agrawal S, Andresen M, Lim J, Giesler GJ, Zoghbi HY, Orr HT (2010) SCA1-like disease in mice expressing wild-type ataxin-1 with a serine to aspartic acid replacement at residue 776. Neuron 67:929-935. CrossRef Medline
12. Eccles JC, Llinís R., Sasaki K (1966) The excitatory synaptic action of climbing fibres on the purkinje cells of cells of the cerebellum. J Physiol 182: 268-296. Medline
13. Emamian ES, Kaytor MD, Duvick LA, Zu T, Tousey SK, Zoghbi HY, Clark HB, Orr HT (2003) Serine 776 of ataxin-1 is critical for polyglutamineinduced disease in SCA1 transgenic mice. Neuron 38:375-387. CrossRef Medline
14. Fernandez-Funez P, Nino-Rosales ML, de Gouyon B, She WC, Luchak JM, Martinez P, Turiegano E, Benito J, Capovilla M, Skinner PJ, McCall A, Canal I, Orr HT, Zoghbi HY, Botas J (2000) Identification of genes that modify ataxin-1-induced neurodegeneration. Nature 408:101-106. CrossRef Medline
15. Freemeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260. CrossRef Medline
16. Gao W, Chen G, Reinert KC, Ebner TJ (2006) Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J Neurosci 26:8377-8387. CrossRef Medline
17. Goldowitz D, Hamre K (1998) The cells and molecules that make a cerebellum. Trend Neurosci 21:375-382. CrossRef Medline
18. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925. CrossRef Medline
19. Gossen M, Bujard H (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A 89: 5547-5551. CrossRef Medline
20. Granit R, Philips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of cerebellum in cats. J Physiol 133:520-547. Medline
21. Hashimoto K, Kano M (2003) Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron 38:785-796. CrossRef Medline
22. Hashimoto K, Ichikawa R, Kitamura K, Watanabe M, Kano M (2009) Translocation of a "winner" climbing fiber to the Purkinje cell dendrite and subsequent elimination of "losers" from the soma in developing cerebellum. Neuron 63:106-118. CrossRef Medline
23. Irwin S, Vandelft M, Howell JL, Graczyk J, Orr HT, Truant R (2005) RNA association and nucleocytoplasmic shuttling by ataxin-1. J Cell Sci 118: 233-242. CrossRef Medline
24. Kakizawa S, Yamada K, Iino M, Kano M (2003) Effects of insulin-like growth factor 1 on climbing fibre synapse elimination during cerebellar development. Eur J Neurosci 17:545-554. CrossRef Medline
25. Kakizawa S, Miyazaki T, Yanagihara D, Iino M, Watanabe M, Kano M (2005) Maintenance of presynaptic function by AMPA receptor-mediated excitatory postsynaptic activity in adult brain. Proc Natl Acad Sci U S A 102: 19180-19185. CrossRef Medline
26. Kano M, Hashimoto K (2009) Synapse elimination in the central nervous system. Curr Opin Neurobiol 19:154-161. CrossRef Medline
27. Kano M, Hashimoto K, Chen C, Abeliovich A, Aiba A, Kurihara H, Watanabe M, Inoue Y, Tonegawa S (1995) Impaired synapse elimination during cerebellar development in PKCg mutant mice. Cell 83:1223-1231. CrossRef Medline
28. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, Zoghbi HY, Orr HT (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95:41-53. CrossRef Medline
29. Landis DMD, Rosenberg RN, Landis DM, Schut L, Nyhan WL (1974) Olivopontocerbellar degeneration clinical and ultrastructural abnormalities. Arch Neurol 31:295-307. CrossRef Medline
30. Mason CA, Christakos S, Catalano SM (1990) Early climbing fiber interactions with Purkinje cell in the postnatal mouse cerebellum. J Comp Neurol 297:77-90. CrossRef Medline
31. Matilla A, Roberson ED, Banfi S, Morales J, Armstrong DL, Burright EN, Orr HT, Sweatt JD, Zoghbi HY, Matzuk MM (1998) Mice lacking ataxin-1 display learning deficits and decreased hippocampal paired-pulse facilitation. J Neurosci 18:5508-5516. Medline
32. Matilla-Dueñas A, Goold R, Giunti P (2008) Clinical, genetic, molecular, and pathophysiological insights into spinocerebellar ataxia type 1. Cerebellum 7:106-114. CrossRef Medline
33. 2+ channel a1A regulates synaptic competition on developing cerebellar Purkinje cells. J Neurosci 24:1734-1743. CrossRef Medline
34. O'Leary JL, Inukai J, Smith JM (1971) Histogenesis of the cerebellar climbing fiber in the rat. J Comp Neurol 142:377-391. CrossRef Medline
35. Orr HT, Chung MY, Banfi S, Kwiatkowski TJ Jr, Servadio A, Beaudet AL, McCall AE, Duvick LA, Ranum LP, Zoghbi HY (1993) Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat Genet 4:221-226. CrossRef Medline
36. Oz G, Nelson CD, Koski DM, Henry PG, Marjanska M, Deelchand DK, Shanley R, Eberly LE, Orr HT, Clark HB (2010) Noninvasive detection of presymptomatic and progressive neurodegeneration in a mouse model of spinocerebellar ataxia type 1. J Neurosci 30:3831-3838. CrossRef Medline
37. Ramoný Cajal S (1911) Histolgie du systéme nerveux de l'homme et des vertébrés. Paris: A. Malone.
38. Reinert KC, Dunbar RL, Gao W, Chen G, Ebner TJ (2004) Flavoprotein autofluorescence imaging of neuronal activation in the cerebellar cortex in vivo. J Neurophysiol 92:199-211. CrossRef Medline
39. Reinert KC, Gao W, Chen G, Ebner TJ (2007) Flavoprotein autofluorescence imaging in the cerebellar cortex in vivo. J Neurosci Res 85:3221-3232. CrossRef Medline
40. Rossi F, van der Want JJ, Wiklund L, Strata P (1991) Reinnervation of cerebellar Purkinje cells by climbing fibres surviving to a subtotal lesion of the inferior olive in the adult rat. Synaptic organization on reinnervated Purkinje cells. J Comp Neurol 308:536-554. CrossRef Medline
41. Serra HG, Duvick L, Zu T, Carlson K, Stevens S, Jorgensen N, Lysholm A, Burright E, Zoghbi HY, Clark HB, Andresen JM, Orr HT (2006) ROR - mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127:697-708. CrossRef Medline
42. Sotelo C (1978) Purkinje cell ontogeny: formation and maintenance of spines. Progr Brain Res 48:149-170.
43. Sotelo C, Hillman DE, Zamora AJ, Llinás R (1975) Climbing fiber deafferentation: its action on Purkinje cell dendritic spines. Brain Res 98:574-581. CrossRef Medline
44. Strata P (2002) Dendritic spines in Purkinje cells. Cerebellum 1:230-232. CrossRef Medline
45. Takagishi Y, Hashimoto K, Kayahara T, Watanabe M, Otsuka H, Mizoguchi A, Kano M, Murata Y (2007) Diminished climbing fiber innervation of Purkinje cells in the cerebellum of myosin Va mutant mice and rats. Dev Neurobiol 67:909-923. CrossRef Medline
46. Zu T, Duvick LA, Kaytor MD, Berlinger MS, Zoghbi HY, Clark HB, Orr HT (2004) Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice. J Neurosci 24:8853-8861. CrossRef Medline