Cellular and circuit mechanisms underlying spinocerebellar ataxias

Journal of Physiology

Volumn 594, Issue 16, 2016, Pages 4653-4660

  Meera, Pratap ^a   Pulst, Stefan M ^b   Otis, Thomas S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; METABOTROPIC RECEPTOR;

ACTION POTENTIAL; ANTIDROMIC STIMULATION; CALCIUM HOMEOSTASIS; CALCIUM METABOLISM; CELL FUNCTION; CONNECTOME; DISEASE ACTIVITY; DISEASE ASSOCIATION; HUMAN; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PURKINJE CELL; REVIEW; SIGNAL TRANSDUCTION; SPINOCEREBELLAR DEGENERATION;

EID: 84982231285     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP271897     Document Type: Review

References (67)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA & Tonegawa S (1994). Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79, 377–388.
2. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A & Meyer M (1997). Ataxia and altered dendritic calcium signalling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA 94, 1488–1493.
3. Armbrust KR, Wang X, Hathorn TJ, Cramer SW, Chen G, Zu T, Kangas T, Zink AN, Oz G, Ebner TJ & Ranum LP (2014). Mutant β-III spectrin causes mGluR1α mislocalization and functional deficits in a mouse model of spinocerebellar ataxia type 5. J Neurosci 34, 9891–9904.
4. Batchelor AM & Garthwaite J (1997). Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature 385, 74–77.
5. Becker EB, Oliver PL, Glitsch MD, Banks GT, Achilli F, Hardy A, Nolan PM, Fisher EM & Davies KE (2009). A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci USA 106, 6706–6711.
6. Bezprozvanny I, Watras J & Ehrlich BE (1991). Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351, 751–754.
7. Brasnjo G & Otis TS (2001). Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron 31, 607–616.
8. 2+ homeostasis in a patient with cerebellar ataxia and laminin subunit 1α mutations. J Biol Chem 290, 16132–16141.
9. Carlson KM, Andresen JM & Orr HT (2009). Emerging pathogenic pathways in the spinocerebellar ataxias. Curr Opin Genes Dev 19, 247–253.
10. Conquet F, Bashir ZI, Davies CH, Daniel H, Ferraguti F, Bordi F, Franz-Bacon K, Reggiani A, Matarese V, Conde F, et al. (1994). Motor deficit and impairment of synaptic plasticity in mice lacking mGluR1. Nature 372, 237–243.
11. Dell'Orco JM, Wasserman AH, Chopra R, Ingram MA, Hu YS, Singh V, Wulff H, Opal P, Orr HT & Shakkottai VG (2015). Neuronal atrophy early in degenerative ataxia is a compensatory mechanism to regulate membrane excitability. J Neurosci 35, 11292–11307.
12. Dzubay JA & Otis TS (2002). Climbing fibre activation of metabotropic glutamate receptors on cerebellar purkinje neurons. Neuron 36, 1159–1167.
13. 2+ dynamics in mouse cerebellar Purkinje neurones and alters the precision of motor coordination. J Physiol 588, 907–922.
14. Finch EA & Augustine GJ (1998). Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396, 753–756.
15. Finch EA, Turner TJ & Goldin SM (1991). Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252, 443–446.
16. Fogel BL, Hanson SM & Becker EB (2015). Do mutations in the murine ataxia gene TRPC3 cause cerebellar ataxia in humans? Mov Disord 30, 284–286.
17. Gehman LT, Meera P, Stoilov P, Shiue L, O'Brien JE, Meisler MH, Ares M Jr, Otis TS & Black DL (2012). The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev 26, 445–460.
18. Guergueltcheva V, Azmanov DN, Angelicheva D, Smith KR, Chamova T, Florez L, Bynevelt M, Nguyen T, Cherninkova S, Bojinova V, Kaprelyan A, Angelova L, Morar B, Chandler D, Kaneva R, Bahlo M, Tournev I & Kalaydjieva L (2012). Autosomal-recessive congenital cerebellar ataxia is caused by mutations in metabotropic glutamate receptor 1. Am J Hum Genet 91, 553–564.
19. Hansen ST, Meera P, Otis TS & Pulst SM (2013). Changes in Purkinje cell firing and gene expression precede behavioral pathology in a mouse model of SCA2. Hum Mol Genet 22, 271–283.
20. Hartmann J, Henning HA & Konnerth A (2011). mGluR1/TRPC3-mediated synaptic transmission and calcium signaling in mammalian central neurons. Cold Spring Harb Perspect Biol 3, a006726.
21. 11 for Purkinje cell signaling and motor behavior. J Neurosci 24, 5119–5130.
22. Hartmann J, Dragicevic E, Adelsberger H, Henning HA, Sumser M, Abramowitz J, Blum R, Dietrich A, Freichel M, Flockerzi V, Birnbaumer L & Konnerth A (2008). TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 59, 392–398.
23. Hausser M & Clark BA (1997). Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19, 665–678.
24. Heiney SA, Kim J, Augustine GJ & Medina JF (2014). Precise control of movement kinematics by optogenetic inhibition of Purkinje cell activity. J Neurosci 34, 2321–2330.
25. Hourez R, Servais L, Orduz D, Gall D, Millard I, de Kerchove d'Exaerde A, Cheron G, Orr HT, Pandolfo M & Schiffmann SN (2011). Aminopyridines correct early dysfunction and delay neurodegeneration in a mouse model of spinocerebellar ataxia type 1. J Neurosci 31, 11795–11807.
26. Huber KM (2006). The fragile X-cerebellum connection. Trends Neurosci 29, 183–185.
27. Ichise T, Kano M, Hashimoto K, Yanagihara D, Nakao K, Shigemoto R, Katsuki M & Aiba A (2000). mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science 288, 1832–1835.
28. Kano M, Hashimoto K, Watanabe M, Kurihara H, Offermanns S, Jiang H, Wu Y, Jun K, Shin HS, Inoue Y, Simon MI & Wu D (1998). Phospholipase cβ4 is specifically involved in climbing fiber synapse elimination in the developing cerebellum. Proc Natl Acad Sci USA 95, 15724–15729.
29. Kasumu AW, Hougaard C, Rode F, Jacobsen TA, Sabatier JM, Eriksen BL, Strobaek D, Liang X, Egorova P, Vorontsova D, Christophersen P, Ronn LC & Bezprozvanny I (2012b). Selective positive modulator of calcium-activated potassium channels exerts beneficial effects in a mouse model of spinocerebellar ataxia type 2. Chem Biol 19, 1340–1353.
30. Kasumu AW, Liang X, Egorova P, Vorontsova D & Bezprozvanny I (2012a). Chronic suppression of inositol 1,4,5-triphosphate receptor-mediated calcium signaling in cerebellar purkinje cells alleviates pathological phenotype in spinocerebellar ataxia 2 mice. J Neurosci 32, 12786–12796.
31. Khaliq ZM, Gouwens NW & Raman IM (2003). The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23, 4899–4912.
32. Konno A, Shuvaev AN, Miyake N, Miyake K, Iizuka A, Matsuura S, Huda F, Nakamura K, Yanagi S, Shimada T & Hirai H (2014). Mutant ataxin-3 with an abnormally expanded polyglutamine chain disrupts dendritic development and metabotropic glutamate receptor signaling in mouse cerebellar Purkinje cells. Cerebellum 13, 29–41.
33. Lee KH, Mathews PJ, Reeves AM, Choe KY, Jami SA, Serrano RE & Otis TS (2015). Circuit mechanisms underlying motor memory formation in the cerebellum. Neuron 86, 529–540.
34. Lin X, Antalffy B, Kang D, Orr HT & Zoghbi HY (2000). Polyglutamine expansion down-regulates specific neuronal genes before pathologic changes in SCA1. Nat Neurosci 3, 157–163.
35. Liu J, Tang TS, Tu H, Nelson O, Herndon E, Huynh DP, Pulst SM & Bezprozvanny I (2009). Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2. J Neurosci 29, 9148–9162.
36. Mark MD, Krause M, Boele HJ, Kruse W, Pollok S, Kuner T, Dalkara D, Koekkoek S, De Zeeuw CI & Herlitze S (2015). Spinocerebellar ataxia type 6 protein aggregates cause deficits in motor learning and cerebellar plasticity. J Neurosci 35, 8882–8895.
37. Mathews PJ, Lee KH, Peng Z, Houser CR & Otis TS (2012). Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J Neurosci 32, 17988–17997.
38. Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno J, Sakakibara S, Yamada M, Yoneshima H, Miyawaki A, Fukuuchi Y, Furuichi T, Okano H, Mikoshiba K & Noda T (1996). Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379, 168–171.
39. Miyata M, Kim HT, Hashimoto K, Lee TK, Cho SY, Jiang H, Wu Y, Jun K, Wu D, Kano M & Shin HS (2001). Deficient long-term synaptic depression in the rostral cerebellum correlated with impaired motor learning in phospholipase C β4 mutant mice. Eur J Neurosci 13, 1945–1954.
40. Nakao H, Nakao K, Kano M & Aiba A (2007). Metabotropic glutamate receptor subtype-1 is essential for motor coordination in the adult cerebellum. Neurosci Res 57, 538–543.
41. Notartomaso S, Zappulla C, Biagioni F, Cannella M, Bucci D, Mascio G, Scarselli P, Fazio F, Weisz F, Lionetto L, Simmaco M, Gradini R, Battaglia G, Signore M, Puliti A & Nicoletti F (2013). Pharmacological enhancement of mGlu1 metabotropic glutamate receptors causes a prolonged symptomatic benefit in a mouse model of spinocerebellar ataxia type 1. Mol Brain 6, 48.
42. Offermanns S, Hashimoto K, Watanabe M, Sun W, Kurihara H, Thompson RF, Inoue Y, Kano M & Simon MI (1997). Impaired motor coordination and persistent multiple climbing fibre innervation of cerebellar Purkinje cells in mice lacking Gαq. Proc Natl Acad Sci USA 94, 14089–14094.
43. Orr HT (2013). Toxic RNA as a driver of disease in a common form of ALS and dementia. Proc Natl Acad Sci USA 110, 7533–7534.
44. Paulson HL (2009). The spinocerebellar ataxias. J Neuroophthalmol 29, 227–237.
45. Perkins EM, Clarkson YL, Sabatier N, Longhurst DM, Millward CP, Jack J, Toraiwa J, Watanabe M, Rothstein JD, Lyndon AR, Wyllie DJ, Dutia MB & Jackson M (2010). Loss of β-III spectrin leads to Purkinje cell dysfunction recapitulating the behavior and neuropathology of spinocerebellar ataxia type 5 in humans. J Neurosci 30, 4857–4867.
46. Pulst SM, Nechiporuk A, Nechiporuk T, Gispert S, Chen XN, Lopes-Cendes I, Pearlman S, Starkman S, Orozco-Diaz G, Lunkes A, DeJong P, Rouleau GA, Auburger G, Korenberg JR, Figueroa C & Sahba S (1996). Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet 14, 269–276.
47. Raman IM & Bean BP (1999). Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19, 1663–1674.
48. Sarkisov DV & Wang SS (2008). Order-dependent coincidence detection in cerebellar Purkinje neurons at the inositol trisphosphate receptor. J Neurosci 28, 133–142.
49. Sekerkova G, Kim JA, Nigro MJ, Becker EB, Hartmann J, Birnbaumer L, Mugnaini E & Martina M (2013). Early onset of ataxia in moonwalker mice is accompanied by complete ablation of type II unipolar brush cells and Purkinje cell dysfunction. J Neurosci 33, 19689–19694.
50. Serra HG, Byam CE, Lande JD, Tousey SK, Zoghbi HY & Orr HT (2004). Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum Mol Genet 13, 2535–2543.
51. 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). RORα-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127, 697–708.
52. Shakkottai VG, do Carmo Costa M, Dell'Orco JM, Sankaranarayanan A, Wulff H & Paulson HL (2011). Early changes in cerebellar physiology accompany motor dysfunction in the polyglutamine disease spinocerebellar ataxia type 3. J Neurosci 31, 13002–13014.
53. Skinner PJ, Vierra-Green CA, Clark HB, Zoghbi HY & Orr HT (2001). Altered trafficking of membrane proteins in purkinje cells of SCA1 transgenic mice. Am J Pathol 159, 905–913.
54. Smith SL & Otis TS (2003). Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J Neurosci 23, 367–372.
55. Szapiro G & Barbour B (2007). Multiple climbing fibers signal to molecular layer interneurons exclusively via glutamate spillover. Nat Neurosci 10, 735–742.
56. Takechi H, Eilers J & Konnerth A (1998). A new class of synaptic response involving calcium release in dendritic spines. Nature 396, 757–760.
57. Tanaka J, Nakagawa S, Kushiya E, Yamasaki M, Fukaya M, Iwanaga T, Simon MI, Kano M & Watanabe M (2000). Gq protein alpha subunits Galphaq and Galpha11 are localized at postsynaptic extra-junctional membrane of cerebellar Purkinje cells and hippocampal pyramidal cells. Eur J Neurosci 12, 781–792.
58. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG & Sahin M (2012). Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature 488, 647–651.
59. van de Leemput J, Chandran J, Knight MA, Holtzclaw LA, Scholz S, Cookson MR, Houlden H, Gwinn-Hardy K, Fung HC, Lin X, Hernandez D, Simon-Sanchez J, Wood NW, Giunti P, Rafferty I, Hardy J, Storey E, Gardner RJ, Forrest SM, Fisher EM, Russell JT, Cai H & Singleton AB (2007). Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet 3, e108.
60. Vecellio M, Schwaller B, Meyer M, Hunziker W & Celio MR (2000). Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neurosci 12, 945–954.
61. Vig PJ, Wei J, Shao Q, Lopez ME, Halperin R & Gerber J (2012). Suppression of calbindin-D28k expression exacerbates SCA1 phenotype in a disease mouse model. Cerebellum 11, 718–732.
62. Walter JT, Alvina K, Womack MD, Chevez C & Khodakhah K (2006). Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 9, 389–397.
63. Wang SS, Denk W & Hausser M (2000). Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3, 1266–1273.
64. Yabe I, Sasaki H, Chen DH, Raskind WH, Bird TD, Yamashita I, Tsuji S, Kikuchi S & Tashiro K (2003). Spinocerebellar ataxia type 14 caused by a mutation in protein kinase C γ. Arch Neurol 60, 1749–1751.
65. 2+ homeostasis. Proc Natl Acad Sci USA 109, 14514–14519.
66. Zhou H, Lin Z, Voges K, Ju C, Gao Z, Bosman LW, Ruigrok TJ, Hoebeek FE, De Zeeuw CI & Schonewille M (2014). Cerebellar modules operate at different frequencies. eLife 3, e02536.
67. 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.