Computational analysis of calcium signaling and membrane electrophysiology in cerebellar Purkinje neurons associated with ataxia

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Brown, Sherry Ann ^a   Loew, Leslie M ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Ataxia; BK channel; CAG repeat instability; Computational; Homer; IP3R; K Ca channels; Model; Spinocerebellar; Virtual cell

Indexed keywords

ANIMALIA; MUS;

CALCIUM ACTIVATED POTASSIUM CHANNEL; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PEPTIDE FRAGMENT;

ALGORITHM; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CALCIUM SIGNALING; CELL MEMBRANE; CHEMISTRY; ELECTROPHYSIOLOGY; HUMAN; METABOLISM; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PURKINJE CELL; SPINOCEREBELLAR DEGENERATION;

ALGORITHMS; ANIMALS; CALCIUM SIGNALING; CELL MEMBRANE; ELECTROPHYSIOLOGICAL PROCESSES; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MICE; MODELS, NEUROLOGICAL; PEPTIDE FRAGMENTS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; PURKINJE CELLS; SPINOCEREBELLAR ATAXIAS;

EID: 84862166730     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-70     Document Type: Article

References (103)

1. Goetz CG. Textbook of Clinical Neurology 2003, St. Louis, MO: WB Saunders.
2. Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K, Takano H, Minowa O, Kuno J, Sakakibara S, Yamada M, et al. Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 1996, 379:168-171. 10.1038/379168a0, 8538767.
3. van de Leemput J, Chandran J, Knight M, Holtzclaw L, Scholz S, Cookson M, Houlden H, Gwinn-Hardy K, Fung H, Lin X, et al. Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet 2007, 3:e108. 10.1371/journal.pgen.0030108, 1892049, 17590087.
4. Street V, Bosma M, Demas V, Regan M, Lin D, Robinson L, Agnew W, Tempel B. The type 1 inositol 1,4,5-trisphosphate receptor gene is altered in the opisthotonos mouse. J Neurosci 1997, 17:635-645.
5. Ogura H, Matsumoto M, Mikoshiba K. Motor discoordination in mutant mice heterozygous for the type 1 inositol 1,4,5-trisphosphate receptor. Behav Brain Res 2001, 122:215-219. 10.1016/S0166-4328(01)00187-5, 11334652.
6. Chen X, Tang T, Tu H, Nelson O, Pook M, Hammer R, Nukina N, Bezprozvanny I. Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 3. J Neurosci 2008, 28:12713-12724. 10.1523/JNEUROSCI.3909-08.2008, 2663415, 19036964.
7. Chou A, Yeh T, Ouyang P, Chen Y, Chen S, Wang H. Polyglutamine-expanded ataxin-3 causes cerebellar dysfunction of SCA3 transgenic mice by inducing transcriptional dysregulation. Neurobiol Dis 2008, 31:89-101. 10.1016/j.nbd.2008.03.011, 18502140.
8. Inoue T, Lin X, Kohlmeier K, Orr H, Zoghbi H, Ross W. Calcium dynamics and electrophysiological properties of cerebellar Purkinje cells in SCA1 transgenic mice. J Neurophysiol 2001, 85:1750-1760.
9. Lin X, Antalffy B, Kang D, Orr H, Zoghbi H. Polyglutamine expansion down-regulates specific neuronal genes before pathologic changes in SCA1. Nat Neurosci 2000, 3:157-163. 10.1038/72101, 10649571.
10. Liu J, Tang T, Tu H, Nelson O, Herndon E, Huynh D, Pulst S, Bezprozvanny I. Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2. J Neurosci 2009, 29:9148-9162. 10.1523/JNEUROSCI.0660-09.2009, 2749883, 19625506.
11. Serra H, Byam C, Lande J, Tousey S, Zoghbi H, Orr H. Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum Mol Genet 2004, 13:2535-2543. 10.1093/hmg/ddh268, 15317756.
12. Iwaki A, Kawano Y, Miura S, Shibata H, Matsuse D, Li W, Furuya H, Ohyagi Y, Taniwaki T, Kira J, Fukumaki Y. Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16. J Med Genet 2008, 45:32-35.
13. Desaiah D, Vig P, Subramony S, Currier R. Inositol 1,4,5-trisphosphate receptors and protein kinase C in olivopontocerebellar atrophy. Brain Res 1991, 552:36-40. 10.1016/0006-8993(91)90656-G, 1655168.
14. Zecevic N, Milosevic A, Ehrlich B. Calcium signaling molecules in human cerebellum at midgestation and in ataxia. Early Hum Dev 1999, 54:103-116. 10.1016/S0378-3782(98)00090-5, 10213289.
15. Di Gregorio E, Orsi L, Godani M, Vaula G, Jensen S, Salmon E, Ferrari G, Squadrone S, Abete M, Cagnoli C, et al. Two Italian Families with ITPR1 Gene Deletion Presenting a Broader Phenotype of SCA15. Cerebellum 2010, 9:115-123. 10.1007/s12311-009-0154-0, 20082166.
16. Hara K, Shiga A, Nozaki H, Mitsui J, Takahashi Y, Ishiguro H, Yomono H, Kurisaki H, Goto J, Ikeuchi T, et al. Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology 2008, 71:547-551. 10.1212/01.wnl.0000311277.71046.a0, 18579805.
17. Novak M, Davis M, Li A, Goold R, Tabrizi S, Sweeney M, Houlden H, Treacy C, Giunti P. PAW32 ITPR1 gene deletion causes spinocerebellar ataxia 15/16: a genetic, clinical and radiological description of a novel kindred. J Neurol Neurosurg Psychiatry 2010, 81:e32.
18. Bezprozvanny I. Role of Inositol 1,4,5-Trishosphate Receptors in Pathogenesis of Huntington's Disease and Spinocerebellar Ataxias. Neurochem Res 2011, 36:1186-1197. 10.1007/s11064-010-0393-y, 3094593, 21210219.
19. 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, 33:211-219. 10.1016/j.tins.2010.02.005, 20226542.
20. Kurnellas M, Lee A, Li H, Deng L, Ehrlich D, Elkabes S. Molecular alterations in the cerebellum of the plasma membrane calcium ATPase 2 (PMCA2)-null mouse indicate abnormalities in Purkinje neurons. Mol Cell Neurosci 2007, 34:178-188. 10.1016/j.mcn.2006.10.010, 2561181, 17150372.
21. Tu H, Tang T, Wang Z, Bezprozvanny I. Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J Biol Chem 2004, 279:19375-19382. 10.1074/jbc.M313476200, 14982933.
22. Bezprozvanny I. The inositol 1,4,5-trisphosphate receptors. Cell Calcium 2005, 38:261-272. 10.1016/j.ceca.2005.06.030, 16102823.
23. Burright E, Clark H, Servadio A, Matilla T, Feddersen R, Yunis W, Duvick L, Zoghbi H, Orr H. SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 1995, 82:937-948. 10.1016/0092-8674(95)90273-2, 7553854.
24. Orr H, Chung M, Banfi S, Kwiatkowski TJ, Servadio A, Beaudet A, McCall A, Duvick L, Ranum L, Zoghbi H. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat Genet 1993, 4:221-226. 10.1038/ng0793-221, 8358429.
25. Pulst S, Nechiporuk A, Nechiporuk T, Gispert S, Chen X, Lopes-Cendes I, Pearlman S, Starkman S, Orozco-Diaz G, Lunkes A, et al. Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat Genet 1996, 14:269-276.
26. Boy J, Schmidt T, Schumann U, Grasshoff U, Unser S, Holzmann C, Schmitt I, Karl T, Laccone F, Wolburg H, et al. A transgenic mouse model of spinocerebellar ataxia type 3 resembling late disease onset and gender-specific instability of CAG repeats. Neurobiol Dis 2010, 37:284-293. 10.1016/j.nbd.2009.08.002, 19699305.
27. Dürr A, Stevanin G, Cancel G, Duyckaerts C, Abbas N, Didierjean O, Chneiweiss H, Benomar A, Lyon-Caen O, Julien J, et al. Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular, and neuropathological features. Ann Neurol 1996, 39:490-499. 10.1002/ana.410390411, 8619527.
28. Paulson H, Perez M, Trottier Y, Trojanowski J, Subramony S, Das S, Vig P, Mandel J, Fischbeck K, Pittman R. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 1997, 19:333-344. 10.1016/S0896-6273(00)80943-5, 9292723.
29. Mantuano E, Veneziano L, Spadaro M, Giunti P, Guida S, Leggio M, Verriello L, Wood N, Jodice C, Frontali M. Clusters of non-truncating mutations of P/Q type Ca2+ channel subunit Ca(v)2.1 causing episodic ataxia 2. J Med Genet 2004, 41:e82. 10.1136/jmg.2003.015396, 1735819, 15173248.
30. Inoue T. Dynamics of calcium and its roles in the dendrite of the cerebellar Purkinje cell. Keio J Med 2003, 52:244-249. 10.2302/kjm.52.244, 14748477.
31. Gardner R. "SCA16" is really SCA15. J Med Genet 2008, 45:192.
32. Brown S-A, Loew LM. Toward A Computational Model Of IP3R1-associated Ataxia. Biophysical Journal 2009, 96(3:S1):96a.
33. Khodakhah K, Ogden D. Functional heterogeneity of calcium release by inositol trisphosphate in single Purkinje neurones, cultured cerebellar astrocytes, and peripheral tissues. Proc Natl Acad Sci U S A 1993, 90:4976-4980. 10.1073/pnas.90.11.4976, 46636, 8506344.
34. Fujiwara A, Hirose K, Yamazawa T, Iino M. Reduced IP3 sensitivity of IP3 receptor in Purkinje neurons. Neuroreport 2001, 12:2647-2651. 10.1097/00001756-200108280-00012, 11522941.
35. Hernjak N, Slepchenko B, Fernald K, Fink C, Fortin D, Moraru I, Watras J, Loew L. Modeling and analysis of calcium signaling events leading to long-term depression in cerebellar Purkinje cells. Biophys J 2005, 89:3790-3806. 10.1529/biophysj.105.065771, 1366947, 16169982.
36. Brown SA, Moraru II, Schaff JC, Loew LM. Virtual NEURON: a strategy for merged biochemical and electrophysiological modeling. J Comput Neurosci 2011, 31:385-400. 10.1007/s10827-011-0317-0, 3221887, 21340454.
37. Loew L, Schaff J. The Virtual Cell: a software environment for computational cell biology. Trends Biotechnol 2001, 19:401-406. 10.1016/S0167-7799(01)01740-1, 11587765.
38. Schaff J, Fink C, Slepchenko B, Carson J, Loew L. A general computational framework for modeling cellular structure and function. Biophys J 1997, 73:1135-1146. 10.1016/S0006-3495(97)78146-3, 1181013, 9284281.
39. Schaff J, Slepchenko B, Loew L. Physiological modeling with virtual cell framework. Methods Enzymol 2000, 321:1-23.
40. Cowan AE, Moraru II, Schaff JC, Slepchenko BM, Loew LM. Spatial modeling of cell signaling networks. Methods Cell Biol 2012, 110:195-221.
41. Moraru I, Schaff J, Slepchenko B, Loew L. The virtual cell: an integrated modeling environment for experimental and computational cell biology. Ann N Y Acad Sci 2002, 971:595-596. 10.1111/j.1749-6632.2002.tb04535.x, 12438191.
42. Brown S, Morgan F, Watras J, Loew L. Analysis of phosphatidylinositol-4,5-bisphosphate signaling in cerebellar Purkinje spines. Biophys J 2008, 95:1795-1812. 10.1529/biophysj.108.130195, 2483750, 18487300.
43. Tang T, Tu H, Wang Z, Bezprozvanny I. Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase a and protein phosphatase 1alpha. J Neurosci 2003, 23:403-415.
44. Wang S, Denk W, Häusser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 2000, 3:1266-1273. 10.1038/81792, 11100147.
45. Finch E, Augustine G. Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 1998, 396:753-756. 10.1038/25541, 9874372.
46. Takechi H, Eilers J, Konnerth A. A new class of synaptic response involving calcium release in dendritic spines. Nature 1998, 396:757-760. 10.1038/25547, 9874373.
47. Destexhe A, Babloyantz A, Sejnowski T. Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. Biophys J 1993, 65:1538-1552. 10.1016/S0006-3495(93)81190-1, 1225880, 8274647.
48. De Schutter E, Bower J. An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. J Neurophysiol 1994, 71:375-400.
49. Miyasho T, Takagi H, Suzuki H, Watanabe S, Inoue M, Kudo Y, Miyakawa H. Low-threshold potassium channels and a low-threshold calcium channel regulate Ca2+ spike firing in the dendrites of cerebellar Purkinje neurons: a modeling study. Brain Res 2001, 891:106-115. 10.1016/S0006-8993(00)03206-6, 11164813.
50. Gabbiani F, Midtgaard J, Knöpfel T. Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 1994, 72:999-1009.
51. Cui J, Yang H, Lee U. Molecular mechanisms of BK channel activation. Cell Mol Life Sci 2009, 66:852-875. 10.1007/s00018-008-8609-x, 2694844, 19099186.
52. Tang T, Tu H, Chan E, Maximov A, Wang Z, Wellington C, Hayden M, Bezprozvanny I. Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Neuron 2003, 39:227-239. 10.1016/S0896-6273(03)00366-0, 3220623, 12873381.
53. Tang T, Guo C, Wang H, Chen X, Bezprozvanny I. Neuroprotective effects of inositol 1,4,5-trisphosphate receptor C-terminal fragment in a Huntington's disease mouse model. J Neurosci 2009, 29:1257-1266. 10.1523/JNEUROSCI.4411-08.2009, 2768402, 19193873.
54. Brown SA, Holmes RM, Loew LM. Spatial Organization and Diffusion in Neuronal Signaling. Computational Systems Neurobiology 2012, Dordrecht: Springer, Novère N, Chapter 5, in press.
55. Tu H, Wang Z, Bezprozvanny I. Modulation of mammalian inositol 1,4,5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region. Biophys J 2005, 88:1056-1069. 10.1529/biophysj.104.049601, 1305112, 15531634.
56. Sarkisov D, Wang S. Order-dependent coincidence detection in cerebellar Purkinje neurons at the inositol trisphosphate receptor. J Neurosci 2008, 28:133-142. 10.1523/JNEUROSCI.1729-07.2008, 18171931.
57. Kasumu A, Bezprozvanny I. Deranged Calcium Signaling in Purkinje Cells and Pathogenesis in Spinocerebellar Ataxia 2 (SCA2) and Other Ataxias. Cerebellum 2010,
58. Miyata M, Finch E, Khiroug L, Hashimoto K, Hayasaka S, Oda S, Inouye M, Takagishi Y, Augustine G, Kano M. Local calcium release in dendritic spines required for long-term synaptic depression. Neuron 2000, 28:233-244. 10.1016/S0896-6273(00)00099-4, 11086997.
59. Wagner W, Hammer J. Myosin V and the endoplasmic reticulum: the connection grows. J Cell Biol 2003, 163:1193-1196. 10.1083/jcb.200311077, 2173711, 14691131.
60. Vecellio M, Schwaller B, Meyer M, Hunziker W, Celio M. Alterations in Purkinje cell spines of calbindin D-28 k and parvalbumin knock-out mice. Eur J Neurosci 2000, 12:945-954. 10.1046/j.1460-9568.2000.00986.x, 10762324.
61. Vig PJ, Wei J, Shao Q, Lopez ME, Halperin R, Gerber J. Suppression of Calbindin-D28k Expression Exacerbates SCA1 Phenotype in a Disease Mouse Model. Cerebellum 2011,
62. Schmidt H, Stiefel K, Racay P, Schwaller B, Eilers J. Mutational analysis of dendritic Ca2+ kinetics in rodent Purkinje cells: role of parvalbumin and calbindin D28k. J Physiol 2003, 551:13-32. 10.1113/jphysiol.2002.035824, 2343131, 12813159.
63. Vig P, Subramony S, Burright E, Fratkin J, McDaniel D, Desaiah D, Qin Z. Reduced immunoreactivity to calcium-binding proteins in Purkinje cells precedes onset of ataxia in spinocerebellar ataxia-1 transgenic mice. Neurology 1998, 50:106-113. 10.1212/WNL.50.1.106, 9443466.
64. Vig P, Subramony S, McDaniel D. Calcium homeostasis and spinocerebellar ataxia-1 (SCA-1). Brain Res Bull 2001, 56:221-225. 10.1016/S0361-9230(01)00595-0, 11719254.
65. Sausbier M, Hu H, Arntz C, Feil S, Kamm S, Adelsberger H, Sausbier U, Sailer C, Feil R, Hofmann F, et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2 + -activated K + channel deficiency. Proc Natl Acad Sci U S A 2004, 101:9474-9478. 10.1073/pnas.0401702101, 439001, 15194823.
66. Cheron G, Sausbier M, Sausbier U, Neuhuber W, Ruth P, Dan B, Servais L. BK channels control cerebellar Purkinje and Golgi cell rhythmicity in vivo. PLoS One 2009, 4:e7991. 10.1371/journal.pone.0007991, 2776494, 19956720.
67. Kent J, Meredith A. BK channels regulate spontaneous action potential rhythmicity in the suprachiasmatic nucleus. PLoS One 2008, 3:e3884. 10.1371/journal.pone.0003884, 2586654, 19060951.
68. Womack M, Khodakhah K. Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J Neurosci 2004, 24:3511-3521. 10.1523/JNEUROSCI.0290-04.2004, 15071098.
69. Walter J, Alviña K, Womack M, Chevez C, Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat Neurosci 2006, 9:389-397. 10.1038/nn1648, 16474392.
70. Oliver D, Taberner A, Thurm H, Sausbier M, Arntz C, Ruth P, Fakler B, Liberman M. The role of BKCa channels in electrical signal encoding in the mammalian auditory periphery. J Neurosci 2006, 26:6181-6189. 10.1523/JNEUROSCI.1047-06.2006, 1806704, 16763026.
71. Weaver A, Olsen M, McFerrin M, Sontheimer H. BK channels are linked to inositol 1,4,5-triphosphate receptors via lipid rafts: a novel mechanism for coupling [Ca(2+)](i) to ion channel activation. J Biol Chem 2007, 282:31558-31568. 10.1074/jbc.M702866200, 2227909, 17711864.
72. Dai S, Hall D, Hell J. Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol Rev 2009, 89:411-452. 10.1152/physrev.00029.2007, 2733249, 19342611.
73. Sakagami Y, Yamamoto K, Sugiura S, Inokuchi K, Hayashi T, Kato N. Essential roles of Homer-1a in homeostatic regulation of pyramidal cell excitability: a possible link to clinical benefits of electroconvulsive shock. Eur J Neurosci 2005, 21:3229-3239. 10.1111/j.1460-9568.2005.04165.x, 16026461.
74. Vaithianathan T, Bukiya A, Liu J, Liu P, Asuncion-Chin M, Fan Z, Dopico A. Direct regulation of BK channels by phosphatidylinositol 4,5-bisphosphate as a novel signaling pathway. J Gen Physiol 2008, 132:13-28. 10.1085/jgp.200709913, 2442183, 18562499.
75. Bezprozvanny I, Watras J, Ehrlich B. Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 1991, 351:751-754. 10.1038/351751a0, 1648178.
76. Guida S, Trettel F, Pagnutti S, Mantuano E, Tottene A, Veneziano L, Fellin T, Spadaro M, Stauderman K, Williams M, et al. Complete loss of P/Q calcium channel activity caused by a CACNA1A missense mutation carried by patients with episodic ataxia type 2. Am J Hum Genet 2001, 68:759-764. 10.1086/318804, 1274487, 11179022.
77. Zhuchenko O, Bailey J, Bonnen P, Ashizawa T, Stockton D, Amos C, Dobyns W, Subramony S, Zoghbi H, Lee C. Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat Genet 1997, 15:62-69. 10.1038/ng0197-62, 8988170.
78. Yue Q, Jen J, Nelson S, Baloh R. Progressive ataxia due to a missense mutation in a calcium-channel gene. Am J Hum Genet 1997, 61:1078-1087. 10.1086/301613, 1716037, 9345107.
79. Imbrici P, Cusimano A, D'Adamo M, De Curtis A, Pessia M. Functional characterization of an episodic ataxia type-1 mutation occurring in the S1 segment of hKv1.1 channels. Pflugers Arch 2003, 446:373-379.
80. Adachi N, Arima K, Asada T, Kato M, Minami N, Goto Y, Onuma T, Ikeuchi T, Tsuji S, Hayashi M, Fukutani Y. Dentatorubral-pallidoluysian atrophy (DRPLA) presenting with psychosis. J Neuropsychiatry Clin Neurosci 2001, 13:258-260. 10.1176/appi.neuropsych.13.2.258, 11449034.
81. Martins S, Matamá T, Guimarães L, Vale J, Guimarães J, Ramos L, Coutinho P, Sequeiros J, Silveira I. Portuguese families with dentatorubropallidoluysian atrophy (DRPLA) share a common haplotype of Asian origin. Eur J Hum Genet 2003, 11:808-811. 10.1038/sj.ejhg.5201054, 14512972.
82. Yabe I, Sasaki H, Kikuchi S, Nonaka M, Moriwaka F, Tashiro K. Late onset ataxia phenotype in dentatorubro-pallidoluysian atrophy (DRPLA). J Neurol 2002, 249:432-436. 10.1007/s004150200034, 11967648.
83. Naito H, Oyanagi S. Familial myoclonus epilepsy and choreoathetosis: hereditary dentatorubral-pallidoluysian atrophy. Neurology 1982, 32:798-807. 10.1212/WNL.32.8.798, 6808417.
84. Bezprozvanny I. Calcium signaling and neurodegenerative diseases. Trends Mol Med 2009, 15:89-100. 10.1016/j.molmed.2009.01.001, 3226745, 19230774.
85. Bezprozvanny I, Hayden M. Deranged neuronal calcium signaling and Huntington disease. Biochem Biophys Res Commun 2004, 322:1310-1317. 10.1016/j.bbrc.2004.08.035, 15336977.
86. Zhang H, Li Q, Graham R, Slow E, Hayden M, Bezprozvanny I. Full length mutant huntingtin is required for altered Ca2+ signaling and apoptosis of striatal neurons in the YAC mouse model of Huntington's disease. Neurobiol Dis 2008, 31:80-88. 10.1016/j.nbd.2008.03.010, 2528878, 18502655.
87. Bezprozvanny I. Inositol 1,4,5-tripshosphate receptor, calcium signalling and Huntington's disease. Subcell Biochem 2007, 45:323-335. 10.1007/978-1-4020-6191-2_11, 18193642.
88. Stevanin G, Dürr A, Brice A. Clinical and molecular advances in autosomal dominant cerebellar ataxias: from genotype to phenotype and physiopathology. Eur J Hum Genet 2000, 8:4-18. 10.1038/sj.ejhg.5200403, 10713882.
89. Schmidt T, Lindenberg K, Krebs A, Schöls L, Laccone F, Herms J, Rechsteiner M, Riess O, Landwehrmeyer G. Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26 S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann Neurol 2002, 51:302-310. 10.1002/ana.10101, 11891825.
90. Klement I, Skinner P, Kaytor M, Yi H, Hersch S, Clark H, Zoghbi H, Orr H. Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 1998, 95:41-53. 10.1016/S0092-8674(00)81781-X, 9778246.
91. Makarewicz D, Ziemińska E, Łazarewicz J. Dantrolene inhibits NMDA-induced 45Ca uptake in cultured cerebellar granule neurons. Neurochem Int 2003, 43:273-278. 10.1016/S0197-0186(03)00012-3, 12742069.
92. Zhao F, Li P, Chen S, Louis C, Fruen B. Dantrolene inhibition of ryanodine receptor Ca2+ release channels. Molecular mechanism and isoform selectivity. J Biol Chem 2001, 276:13810-13816.
93. Fruen B, Mickelson J, Louis C. Dantrolene inhibition of sarcoplasmic reticulum Ca2+ release by direct and specific action at skeletal muscle ryanodine receptors. J Biol Chem 1997, 272:26965-26971. 10.1074/jbc.272.43.26965, 9341133.
94. Krause T, Gerbershagen M, Fiege M, Weisshorn R, Wappler F. Dantrolene-a review of its pharmacology, therapeutic use and new developments. Anaesthesia 2004, 59:364-373. 10.1111/j.1365-2044.2004.03658.x, 15023108.
95. Gerbershagen M, Fiege M, Krause T, Agarwal K, Wappler F. Dantrolene. Pharmacological and therapeutic aspects. Anaesthesist 2003, 52:238-245. 10.1007/s00101-003-0461-7, 12666006.
96. Kobayashi S, Yano M, Suetomi T, Ono M, Tateishi H, Mochizuki M, Xu X, Uchinoumi H, Okuda S, Yamamoto T, et al. Dantrolene, a therapeutic agent for malignant hyperthermia, markedly improves the function of failing cardiomyocytes by stabilizing interdomain interactions within the ryanodine receptor. J Am Coll Cardiol 2009, 53:1993-2005. 10.1016/j.jacc.2009.01.065, 2764410, 19460614.
97. Sharp AH, McPherson PS, Dawson TM, Aoki C, Campbell KP, Snyder SH. Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain. J Neurosci 1993, 13:3051-3063.
98. Walton PD, Airey JA, Sutko JL, Beck CF, Mignery GA, Südhof TC, Deerinck TJ, Ellisman MH. Ryanodine and inositol trisphosphate receptors coexist in avian cerebellar Purkinje neurons. J Cell Biol 1991, 113:1145-1157. 10.1083/jcb.113.5.1145, 2289007, 1645737.
99. Khodakhah K, Armstrong CM. Inositol trisphosphate and ryanodine receptors share a common functional Ca2+ pool in cerebellar Purkinje neurons. Biophys J 1997, 73:3349-3357. 10.1016/S0006-3495(97)78359-0, 1181236, 9414245.
100. Ln W, Li W, Yule D. Phosphorylation of type-1 inositol 1,4,5-trisphosphate receptors by cyclic nucleotide-dependent protein kinases: a mutational analysis of the functionally important sites in the S2+ and S2- splice variants. J Biol Chem 2003, 278:45811-45817. 10.1074/jbc.M306270200, 12939273.
101. Imbrici P, D'Adamo M, Cusimano A, Pessia M. Episodic ataxia type 1 mutation F184C alters Zn2 + -induced modulation of the human K + channel Kv1.4-Kv1.1/Kvbeta1.1. Am J Physiol Cell Physiol 2007, 292:C778-787.
102. Imbrici P, D'Adamo M, Kullmann D, Pessia M. Episodic ataxia type 1 mutations in the KCNA1 gene impair the fast inactivation properties of the human potassium channels Kv1.4-1.1/Kvbeta1.1 and Kv1.4-1.1/Kvbeta1.2. Eur J Neurosci 2006, 24:3073-3083. 10.1111/j.1460-9568.2006.05186.x, 17156368.
103. Tonelli A, D'Angelo M, Salati R, Villa L, Germinasi C, Frattini T, Meola G, Turconi A, Bresolin N, Bassi M. Early onset, non fluctuating spinocerebellar ataxia and a novel missense mutation in CACNA1A gene. J Neurol Sci 2006, 241:13-17. 10.1016/j.jns.2005.10.007, 16325861.