Deranged Calcium Signaling in Purkinje Cells and Pathogenesis in Spinocerebellar Ataxia 2 (SCA2) and Other Ataxias
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- 作者：Adebimpe Kasumu (1)
Ilya Bezprozvanny (1) - 关键词：Purkinje cell ; Calcium ; Ataxia ; Polyglutamine ; Excitotoxicity ; Neurodegeneration ; SCA2
- 刊名：The Cerebellum
- 出版年：2012
- 出版时间：September 2012
- 年：2012
- 卷：11
- 期：3
- 页码：630-639
- 全文大小：429KB
- 参考文献：1. Filla A, De Michele G, Santoro L, Calabrese O, Castaldo I, Giuffrida S, et al. Spinocerebellar ataxia type 2 in southern Italy: a clinical and molecular study of 30 families. J Neurol. 1999;246(6):467鈥?1. CrossRef
2. Schols L, Bauer P, Schmidt T, Schulte T, Riess O. Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis. Lancet Neurol. 2004;3(5):291鈥?04. CrossRef
3. Lastres-Becker I, Rub U, Auburger G. Spinocerebellar ataxia 2 (SCA2). Cerebellum. 2008;7(2):115鈥?4. CrossRef
4. Matilla-Duenas A, Sanchez I, Corral-Juan M, Davalos A, Alvarez R, Latorre P. Cellular and Molecular Pathways Triggering Neurodegeneration in the Spinocerebellar Ataxias. Cerebellum. 2010;9(2):148鈥?6.
5. Paulson HL. The spinocerebellar ataxias. J Neuroophthalmol. 2009;29(3):227鈥?7. CrossRef
6. Carlson KM, Andresen JM, Orr HT. Emerging pathogenic pathways in the spinocerebellar ataxias. Curr Opin Genet Dev. 2009;19(3):247鈥?3. CrossRef
7. Bezprozvanny I, Klockgether T. Therapeutic prospects for spinocerebellar ataxia type 2 and 3. Drugs of the Future. 2010;34(12):991鈥?.
8. Pirker W, Back C, Gerschlager W, Laccone F, Alesch F. Chronic thalamic stimulation in a patient with spinocerebellar ataxia type 2. Mov Disord. 2003;18(2):222鈥?. CrossRef
9. Lin X, Antalffy B, Kang D, Orr HT, Zoghbi HY. Polyglutamine expansion down-regulates specific neuronal genes before pathologic changes in SCA1. Nat Neurosci. 2000;3(2):157鈥?3. CrossRef
10. Vig PJ, Subramony SH, Qin Z, McDaniel DO, Fratkin JD. Relationship between ataxin-1 nuclear inclusions and Purkinje cell specific proteins in SCA-1 transgenic mice. J Neurol Sci. 2000;174(2):100鈥?0. CrossRef
11. Serra HG, Duvick L, Zu T, Carlson K, Stevens S, Jorgensen N, et al. RORalpha-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell. 2006;127(4):697鈥?08. CrossRef
12. Adachi N, Kobayashi T, Takahashi H, Kawasaki T, Shirai Y, Ueyama T, et al. Enzymological analysis of mutant protein kinase C gamma causing spinocerebellar ataxia type 14 and dysfunction in Ca2+ homeostasis. J Biol Chem. 2008;283(28):19854鈥?3. CrossRef
13. Chen X, Tang T-S, Tu H, Nelson O, Pook MA, Hammer RE, et al. Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 3. J Neurosci. 2008;28:12713鈥?4. CrossRef
14. Hara K, Shiga A, Nozaki H, Mitsui J, Takahashi Y, Ishiguro H, et al. Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology. 2008;71(8):547鈥?1. CrossRef
15. Iwaki A, Kawano Y, Miura S, Shibata H, Matsuse D, Li W, et al. Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16. J Med Genet. 2008;45(1):32鈥?. CrossRef
16. Watase K, Barrett CF, Miyazaki T, Ishiguro T, Ishikawa K, Hu Y, et al. Spinocerebellar ataxia type 6 knockin mice develop a progressive neuronal dysfunction with age-dependent accumulation of mutant CaV2.1 channels. Proc Natl Acad Sci USA. 2008;105(33):11987鈥?2. CrossRef
17. Liu J, Tang TS, Tu H, Nelson O, Herndon E, Huynh DP, et al. Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2. J Neurosci. 2009;29(29):9148鈥?2. CrossRef
18. Schorge S, van de Leemput J, Singleton A, Houlden H, Hardy J. Human ataxias: a genetic dissection of inositol triphosphate receptor (ITPR1)-dependent signaling. Trends Neurosci. 2010 Mar 10. PMID: 20226542.
19. Greer PL, Greenberg ME. From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron. 2008;59(6):846鈥?0. CrossRef
20. Neher E, Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 2008;59(6):861鈥?2. CrossRef
21. Bezprozvanny I. Calcium signaling and neurodegenerative diseases. Trends Mol Med. 2009;15(3):89鈥?00. CrossRef
22. Shakkottai VG, Chou CH, Oddo S, Sailer CA, Knaus HG, Gutman GA, et al. Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. J Clin Invest. 2004;113(4):582鈥?0.
23. Potts MB, Adwanikar H, Noble-Haeusslein LJ. Models of traumatic cerebellar injury. Cerebellum. 2009;8(3):211鈥?1. CrossRef
24. Pulst SM, Nechiporuk A, Nechiporuk T, Gispert S, Chen XN, Lopes-Cendes I, et al. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet. 1996;14(3):269鈥?6. CrossRef
25. Imbert G, Saudou F, Yvert G, Devys D, Trottier Y, Garnier JM, et al. Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats. Nat Genet. 1996;14(3):285鈥?1. CrossRef
26. Sanpei K, Takano H, Igarashi S, Sato T, Oyake M, Sasaki H, et al. Identification of the spinocerebellar ataxia type 2 gene using a direct identification of repeat expansion and cloning technique, DIRECT. Nat Genet. 1996;14(3):277鈥?4. CrossRef
27. Huynh DP, Figueroa K, Hoang N, Pulst SM. Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat Genet. 2000;26(1):44鈥?0. CrossRef
28. Kiehl TR, Shibata H, Pulst SM. The ortholog of human ataxin-2 is essential for early embryonic patterning in C. elegans. J Mol Neurosci. 2000;15(3):231鈥?1. CrossRef
29. Satterfield TF, Jackson SM, Pallanck LJ. A Drosophila homolog of the polyglutamine disease gene SCA2 is a dosage-sensitive regulator of actin filament formation. Genetics. 2002;162(4):1687鈥?02.
30. Kiehl TR, Nechiporuk A, Figueroa KP, Keating MT, Huynh DP, Pulst SM. Generation and characterization of Sca2 (ataxin-2) knockout mice. Biochem Biophys Res Commun. 2006;339(1):17鈥?4. CrossRef
31. Pulst SM, Santos N, Wang D, Yang H, Huynh D, Velazquez L, et al. Spinocerebellar ataxia type 2: polyQ repeat variation in the CACNA1A calcium channel modifies age of onset. Brain. 2005;128(Pt 10):2297鈥?03. CrossRef
32. Furuichi T, Simon-Chazottes D, Fujino I, Yamada N, Hasegawa M, Miyawaki A, et al. Widespread expression of inositol 1, 4, 5-trisphosphate receptor type 1 gene (Insp3r1) in the mouse central nervous system. Recept Channels. 1993;1(1):11鈥?4.
33. Sharp AH, Nucifora Jr FC, Blondel O, Sheppard CA, Zhang C, Snyder SH, et al. Differential cellular expression of isoforms of inositol 1, 4, 5-triphosphate receptors in neurons and glia in brain. J Comp Neurol. 1999;406(2):207鈥?0. CrossRef
34. van de Loo S, Eich F, Nonis D, Auburger G, Nowock J. Ataxin-2 associates with rough endoplasmic reticulum. Exp Neurol. 2009;215(1):110鈥?. CrossRef
35. Hof PR, Glezer II, Conde F, Flagg RA, Rubin MB, Nimchinsky EA, et al. Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat. 1999;16(2):77鈥?16. CrossRef
36. Airaksinen MS, Eilers J, Garaschuk O, Thoenen H, Konnerth A, Meyer M. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc Natl Acad Sci USA. 1997;94(4):1488鈥?3. CrossRef
37. Farre-Castany MA, Schwaller B, Gregory P, Barski J, Mariethoz C, Eriksson JL, et al. Differences in locomotor behavior revealed in mice deficient for the calcium-binding proteins parvalbumin, calbindin D-28k or both. Behav Brain Res. 2007;178(2):250鈥?1. CrossRef
38. Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio MR. Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neurosci. 2000;12(3):945鈥?4. CrossRef
39. Spat A, Szanda G, Csordas G, Hajnoczky G. High- and low-calcium-dependent mechanisms of mitochondrial calcium signalling. Cell Calcium. 2008;44(1):51鈥?3. CrossRef
40. Hajnoczky G, Davies E, Madesh M. Calcium signaling and apoptosis. Biochem Biophys Res Commun. 2003;304(3):445鈥?4. CrossRef
41. Campisi A, Caccamo D, Li Volti G, Curro M, Parisi G, Avola R, et al. Glutamate-evoked redox state alterations are involved in tissue transglutaminase upregulation in primary astrocyte cultures. FEBS Lett. 2004;578(1-2):80鈥?. CrossRef
42. Vosler PS, Brennan CS, Chen J. Calpain-mediated signaling mechanisms in neuronal injury and neurodegeneration. Mol Neurobiol. 2008;38(1):78鈥?00. CrossRef
43. Bolanos JP, Moro MA, Lizasoain I, Almeida A. Mitochondria and reactive oxygen and nitrogen species in neurological disorders and stroke: therapeutic implications. Adv Drug Deliv Rev. 2009;61(14):1299鈥?15. CrossRef
44. Wang SS, Denk W, Hausser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci. 2000;3(12):1266鈥?3. CrossRef
45. Miyata M, Finch EA, Khiroug L, Hashimoto K, Hayasaka S, Oda SI, et al. Local calcium release in dendritic spines required for long-term synaptic depression. Neuron. 2000;28(1):233鈥?4. CrossRef
46. Finch EA, Augustine GJ. Local calcium signalling by inositol-1, 4, 5-trisphosphate in Purkinje cell dendrites. Nature. 1998;396(6713):753鈥?. CrossRef
47. Coesmans M, Weber JT, De Zeeuw CI, Hansel C. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron. 2004;44(4):691鈥?00. CrossRef
48. Jorntell H, Hansel C. Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron. 2006;52(2):227鈥?8. CrossRef
49. Kano M, Hashimoto K, Tabata T. Type-1 metabotropic glutamate receptor in cerebellar Purkinje cells: a key molecule responsible for long-term depression, endocannabinoid signalling and synapse elimination. Philos Trans R Soc Lond B Biol Sci. 2008;363(1500):2173鈥?6. CrossRef
50. Brasnjo G, Otis TS. Neuronal glutamate transporters control activation of postsynaptic metabotropic glutamate receptors and influence cerebellar long-term depression. Neuron. 2001;31(4):607鈥?6. CrossRef
51. Kimura T, Sugimori M, Llinas RR. Purkinje cell long-term depression is prevented by T-588, a neuroprotective compound that reduces cytosolic calcium release from intracellular stores. Proc Natl Acad Sci USA. 2005;102(47):17160鈥?. CrossRef
52. Welsh JP, Yamaguchi H, Zeng XH, Kojo M, Nakada Y, Takagi A, et al. Normal motor learning during pharmacological prevention of Purkinje cell long-term depression. Proc Natl Acad Sci USA. 2005;102(47):17166鈥?1. CrossRef
53. Inoue T, Kato K, Kohda K, Mikoshiba K. Type 1 inositol 1, 4, 5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J Neurosci. 1998;18(14):5366鈥?3.
54. Barenberg P, Strahlendorf H, Strahlendorf J. Hypoxia induces an excitotoxic-type of dark cell degeneration in cerebellar Purkinje neurons. Neurosci Res. 2001;40(3):245鈥?4. CrossRef
55. Strahlendorf J, Box C, Attridge J, Diertien J, Finckbone V, Henne WM, et al. AMPA-induced dark cell degeneration of cerebellar Purkinje neurons involves activation of caspases and apparent mitochondrial dysfunction. Brain Res. 2003;994(2):146鈥?9. CrossRef
56. Maltecca F, Magnoni R, Cerri F, Cox GA, Quattrini A, Casari G. Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration. J Neurosci. 2009;29(29):9244鈥?4. CrossRef
57. Custer SK, Garden GA, Gill N, Rueb U, Libby RT, Schultz C, et al. Bergmann glia expression of polyglutamine-expanded ataxin-7 produces neurodegeneration by impairing glutamate transport. Nat Neurosci. 2006;9(10):1302鈥?1. CrossRef
58. Zoghbi HY, Orr HT. Pathogenic mechanisms of a polyglutamine-mediated neurodegenerative disease, spinocerebellar ataxia type 1. J Biol Chem. 2009;284(12):7425鈥?. CrossRef
59. Klement IA, Skinner PJ, Kaytor MD, Yi H, Hersch SM, Clark HB, et al. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell. 1998;95(1):41鈥?3. CrossRef
60. Goold R, Hubank M, Hunt A, Holton J, Menon RP, Revesz T, et al. Down-regulation of the dopamine receptor D2 in mice lacking ataxin 1. Hum Mol Genet. 2007;16(17):2122鈥?4. CrossRef
61. Serra HG, Byam CE, Lande JD, Tousey SK, Zoghbi HY, Orr HT. Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum Mol Genet. 2004;13(20):2535鈥?3. CrossRef
62. Inoue T, Lin X, Kohlmeier KA, Orr HT, Zoghbi HY, Ross WN. Calcium dynamics and electrophysiological properties of cerebellar Purkinje cells in SCA1 transgenic mice. J Neurophysiol. 2001;85(4):1750鈥?0.
63. Piedras-Renteria ES, Watase K, Harata N, Zhuchenko O, Zoghbi HY, Lee CC, et al. Increased expression of alpha 1A Ca2+ channel currents arising from expanded trinucleotide repeats in spinocerebellar ataxia type 6. J Neurosci. 2001;21(23):9185鈥?3.
64. Ikeda Y, Dick KA, Weatherspoon MR, Gincel D, Armbrust KR, Dalton JC, et al. Spectrin mutations cause spinocerebellar ataxia type 5. Nat Genet. 2006;38(2):184鈥?0. CrossRef
65. Kose A, Saito N, Ito H, Kikkawa U, Nishizuka Y, Tanaka C. Electron microscopic localization of type I protein kinase C in rat Purkinje cells. J Neurosci. 1988;8(11):4262鈥?.
66. Zhu LP, Yu XD, Ling S, Brown RA, Kuo TH. Mitochondrial Ca(2+)homeostasis in the regulation of apoptotic and necrotic cell deaths. Cell Calcium. 2000;28(2):107鈥?7. CrossRef
67. van de Leemput J, Chandran J, Knight MA, Holtzclaw LA, Scholz S, Cookson MR, et al. Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet. 2007;3(6):e108. CrossRef
68. Miyoshi Y, Yamada T, Tanimura M, Taniwaki T, Arakawa K, Ohyagi Y, et al. A novel autosomal dominant spinocerebellar ataxia (SCA16) linked to chromosome 8q22.1鈥?4.1. Neurology. 2001;57(1):96鈥?00. CrossRef
69. Miura S, Shibata H, Furuya H, Ohyagi Y, Osoegawa M, Miyoshi Y, et al. The contactin 4 gene locus at 3p26 is a candidate gene of SCA16. Neurology. 2006;67(7):1236鈥?1. CrossRef
70. Tanaka E, Maruyama H, Morino H, Nakajima E, Kawakami H. The CNTN4 c.4256C>T mutation is rare in Japanese with inherited spinocerebellar ataxia. J Neurol Sci. 2008;266(1鈥?):180鈥?. CrossRef
71. Hisatsune C, Kuroda Y, Akagi T, Torashima T, Hirai H, Hashikawa T, et al. Inositol 1, 4, 5-trisphosphate receptor type 1 in granule cells, not in Purkinje cells, regulates the dendritic morphology of Purkinje cells through brain-derived neurotrophic factor production. J Neurosci. 2006;26(42):10916鈥?4. CrossRef
72. Fujii S, Matsumoto M, Igarashi K, Kato H, Mikoshiba K. Synaptic plasticity in hippocampal CA1 neurons of mice lacking type 1 inositol-1, 4, 5-trisphosphate receptors. Learn Mem. 2000;7(5):312鈥?0. CrossRef
73. Nagase T, Ito KI, Kato K, Kaneko K, Kohda K, Matsumoto M, et al. Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP(3) type 1 receptor. Neuroscience. 2003;117(4):821鈥?0. CrossRef
74. Hartmann J, Dragicevic E, Adelsberger H, Henning HA, Sumser M, Abramowitz J, et al. TRPC3 channels are required for synaptic transmission and motor coordination. Neuron. 2008;59(3):392鈥?. CrossRef
75. Becker EB, Oliver PL, Glitsch MD, Banks GT, Achilli F, Hardy A, et al. A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci USA. 2009;106(16):6706鈥?1. CrossRef
76. Walter JT, Alvina K, Womack MD, Chevez C, Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci. 2006;9(3):389鈥?7. CrossRef - 作者单位：Adebimpe Kasumu (1)
Ilya Bezprozvanny (1)
1. Department of Physiology, UT Southwestern Medical Center at Dallas, Dallas, Texas, USA - ISSN：1473-4230
文摘
Spinocerebellar ataxias (SCAs) constitute a heterogeneous group of more than 30 autosomal-dominant genetic and neurodegenerative disorders. SCAs are generally characterized by progressive ataxia and cerebellar atrophy. Although all SCA patients present with the phenotypic overlap of cerebellar atrophy and ataxia, 17 different gene loci have so far been implicated as culprits in these SCAs. It is not currently understood how mutations in these 17 proteins lead to the cerebellar atrophy and ataxia. Several pathogenic mechanisms have been studied in SCAs but there is yet to be a promising target for successful treatment of SCAs. Emerging research suggests that a fundamental cellular signaling pathway is disrupted by a majority of these mutated genes, which could explain the characteristic death of Purkinje cells, cerebellar atrophy, and ataxia that occur in many SCAs. We propose that mutations in SCA genes cause disruptions in multiple cellular pathways but the characteristic SCA pathogenesis does not begin until calcium signaling pathways are disrupted in cerebellar Purkinje cells either as a result of an excitotoxic increase or a compensatory suppression of calcium signaling. We argue that disruptions in Purkinje cell calcium signaling lead to initial cerebellar dysfunction and ataxic sympoms and eventually proceed to Purkinje cell death. Here, we discuss a calcium hypothesis of Purkinje cell neurodegeneration in SCAs by primarily focusing on an example of spinocerebellar ataxia 2 (SCA2). We will also present evidence linking deranged calcium signaling to the pathogenesis of other SCAs (SCA1, 3, 5, 6, 14, 15/16) that lead to significant Purkinje cell dysfunction and loss in patients.