Integration of modeling with experimental and clinical findings synthesizes and refines the central role of inositol 1,4,5-trisphosphate receptor 1 in spinocerebellar ataxia

Frontiers in Neuroscience

Volumn 9, Issue JAN, 2015, Pages

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

^a MAYO CLINIC   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Carbonic anhydrase related proteins; Computational; Homer; Inositol 1,4,5 trisphosphate receptor 1; Model; Purkinje; Spinocerebellar ataxia; Translational

Indexed keywords

CALBINDIN; CALCIUM ACTIVATED POTASSIUM CHANNEL; GLUTAMATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR 1; ION CHANNEL; LARGE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; PARVALBUMIN; UNCLASSIFIED DRUG;

ARTERY MUSCLE; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CALCIUM TRANSPORT; HUMAN; MEMBRANE ELECTROPHYSIOLOGY; NEUROMODULATION; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PURKINJE CELL; SHORT SURVEY; SMOOTH ENDOPLASMIC RETICULUM; SPINOCEREBELLAR DEGENERATION; SYNTHESIS; UPREGULATION;

EID: 84921824666     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00453     Document Type: Short Survey

References (133)

1. Alonso, I., Costa, C., Gomes, A., Ferro, A., Seixas, A., Silva, S., et al. (2005). A novel H101Q mutation causes PKCgamma loss in spinocerebellar ataxia type 14. J. Hum. Genet. 50, 523-529. doi: 10.1007/s10038-005-0287-z
2. Alviña, K., and Khodakhah, K. (2010a). KCa channels as therapeutic targets in episodic ataxia type-2. J. Neurosci. 30, 7249-7257. doi: 10.1523/JNEUROSCI.6341-09.2010
3. Alviña, K., and Khodakhah, K. (2010b). The therapeutic mode of action of 4-aminopyridine in cerebellar ataxia. J. Neurosci. 30, 7258-7268. doi: 10.1523/JNEUROSCI.3582-09.2010
4. Berridge, M., Lipp, P., and Bootman, M. (2000). The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21. doi: 10.1038/35036035
5. Brown, S.-A., Holmes, R., and Loew, L. M. (2012). "Spatial organization and diffusion in neuronal signaling" in Computational Systems Neurobiology, ed N. L. Novere (Dordrecht: Springer), 133-161.
6. Brown, S.-A., and Loew, L. M. (2009). Toward a computational model of IP3R1-associated ataxia. Biophys. J. 96(Suppl. 1), 96a. doi: 10.1016/j.bpj.2008.12.405
7. Brown, S. A., and Loew, L. M. (2012). Computational analysis of calcium signaling and membrane electrophysiology in cerebellar Purkinje neurons associated with ataxia. BMC Syst. Biol. 6:70. doi: 10.1186/1752-0509-6-70
8. Brown, S.-A., McCullough, L. D., and Loew, L. M. (2015). Computational neurobiology is a useful tool in translational neurology: the example of ataxia. Front. Neurosci. 9:1. doi: 10.3389/fnins.2015.00001
9. Brown, S.-A., Moraru, I., Schaff, J., and Loew, L. M. (2011). Virtual NEURON: a strategy for merged biochemical and electrophysiological modeling. J. Comput. Neurosci. 31, 385-400. doi: 10.1007/s10827-011-0317-0
10. Brown, S-A., Morgan, F., Watras, J., and Loew, L. (2008). Analysis of phosphatidylinositol-4,5-bisphosphate signaling in cerebellar Purkinje spines. Biophys. J. 95, 1795-1812. doi: 10.1529/biophysj.108.130195
11. Bürk, K., Kaiser, F. J., Tennstedt, S., Schöls, L., Kreuz, F. R., Wieland, T. et al. (2014). A novel missense mutation in CACNA1A evaluated by in silico protein modeling is associated with non-episodic spinocerebellar ataxia with slow progression. Eur. J. Med. Genet. 57, 207-211. doi: 10.1016/j.ejmg.2014.01.005
12. Burright, E., Clark, H., Servadio, A., Matilla, T., Feddersen, R., Yunis, W., et al. (1995). SCA1 transgenic mice: a model for neurodegeneration caused by an expanded CAG trinucleotide repeat. Cell 82, 937-948. doi: 10.1016/0092-8674(95)90273-2
13. Cárdenas, C., Juretic, N., Bevilacqua, J., García, I., Figueroa, R., Hartley, R., et al. (2010). Abnormal distribution of inositol 1,4,5-trisphosphate receptors in human muscle can be related to altered calcium signals and gene expression in Duchenne dystrophy-derived cells. FASEB J. 24, 3210-3221. doi: 10.1096/fj.09-152017
14. Castrioto, A., Prontera, P., Di Gregorio, E., Rossi, V., Parnetti, L., Rossi, A., et al. (2011). A novel spinocerebellar ataxia type 15 family with involuntary movements and cognitive decline. Eur. J. Neurol. 18, 1263-1265. doi: 10.1111/j.1468-1331.2011.03366.x
15. Chen, J., Tao, R., Sun, H., Tse, H., Lau, C., and Li, G. (2010). Multiple Ca2+ signaling pathways regulate intracellular Ca2+ activity in human cardiac fibroblasts. J. Cell. Physiol. 223, 68-75. doi: 10.1002/jcp.22010
16. Chen, X., Tang, T., Tu, H., Nelson, O., Pook, M., Hammer, R., et al. (2008). Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 3. J. Neurosci. 28, 12713-12724. doi: 10.1523/JNEUROSCI.3909-08.2008
17. Chou, A., Yeh, T., Ouyang, P., Chen, Y., Chen, S., and Wang, H. (2008). Polyglutamine-expanded ataxin-3 causes cerebellar dysfunction of SCA3 transgenic mice by inducing transcriptional dysregulation. Neurobiol. Dis. 31, 89-101. doi: 10.1016/j.nbd.2008.03.011
18. Chung, H., Steinberg, J., Huganir, R., and Linden, D. (2003). Requirement of AMPA receptor GluR2 phosphorylation for cerebellar long-term depression. Science 300, 1751-1755. doi: 10.1126/science.1082915
19. Chung, H., Xia, J., Scannevin, R., Zhang, X., and Huganir, R. (2000). Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci. 20, 7258-7267. Available online at: http://www.jneurosci.org/content/20/19/7258.long
20. Cohen, D. (2003). Of rafts and moving water. Sci. STKE 2003:pe36. doi: 10.1126/stke.2003.199.pe36
21. Colomer Gould, V. F. (2012). Mouse models of spinocerebellar ataxia type 3 (Machado-Joseph disease). Neurotherapeutics 9, 285-296. doi: 10.1007/s13311-012-0117-x
22. Conroy, J., McGettigan, P., Murphy, R., Webb, D., Murphy, S. M., McCoy, B., et al. (2014). A novel locus for episodic ataxia:UBR4 the likely candidate. Eur. J. Hum. Genet. 22, 505-510. doi: 10.1038/ejhg.2013.173
23. Dai, S., Hall, D., and Hell, J. (2009). Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol. Rev. 89, 411-452. doi: 10.1152/physrev.00029.2007
24. Datta, M., Choudhury, A., Lahiri, A., and Bhattacharyya, N. P. (2011). Genome wide gene expression regulation by HIP1 Protein Interactor, HIPPI: prediction and validation. BMC Genomics 12:463. doi: 10.1186/1471-2164-12-463
25. David, G., Abbas, N., Stevanin, G., Dürr, A., Yvert, G., Cancel, G., et al. (1997). Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nat. Genet. 17, 65-70. doi: 10.1038/ng0997-65
26. De Smedt, H., Missiaen, L., Parys, J., Henning, R., Sienaert, I., Vanlingen, S., et al. (1997). Isoform diversity of the inositol trisphosphate receptor in cell types of mouse origin. Biochem. J. 322(Pt 2), 575-583.
27. de Vries, B., Mamsa, H., Stam, A. H., Wan, J., Bakker, S. L., Vanmolkot, K. R. et al. (2009). Episodic ataxia associated with EAAT1 mutation C186S affecting glutamate reuptake. Arch. Neurol. 66, 97-101. doi: 10.1001/archneurol.2008.53
28. deSouza, N., Cui, J., Dura, M., McDonald, T., and Marks, A. (2007). A function for tyrosine phosphorylation of type 1 inositol 1,4,5-trisphosphate receptor in lymphocyte activation. J. Cell Biol. 179, 923-934. doi: 10.1083/jcb.200708200
29. Di Gregorio, E., Orsi, L., Godani, M., Vaula, G., Jensen, S., Salmon, E., et al. (2010). Two Italian families with ITPR1 gene deletion presenting a broader phenotype of SCA15. Cerebellum 9, 115-123. doi: 10.1007/s12311-009-0154-0
30. Duarri, A., Jezierska, J., Fokkens, M., Meijer, M., Schelhaas, H. J., den Dunnen, W. F., et al. (2012). Mutations in potassium channel kcnd3 cause spinocerebellar ataxia type 19. Ann. Neurol. 72, 870-880. doi: 10.1002/ana.23700
31. Dürr, A., Stevanin, G., Cancel, G., Duyckaerts, C., Abbas, N., Didierjean, O., et al. (1996). Spinocerebellar ataxia 3 and Machado-Joseph disease: clinical, molecular, and neuropathological features. Ann. Neurol. 39, 490-499. doi: 10.1002/ana.410390411
32. Ehrlich, L., Medina, G., Khan, M., Powell, M., Mikoshiba, K., and Carter, C. (2010). Activation of the inositol (1,4,5)-triphosphate calcium gate receptor is required for HIV-1 Gag Release. J. Virol. 84, 6438-6451. doi: 10.1128/JVI.01588-09
33. Escayg, A., De Waard, M., Lee, D. D., Bichet, D., Wolf, P., Mayer, T., et al. (2000). Coding and noncoding variation of the human calcium-channel beta4-subunit gene CACNB4 in patients with idiopathic generalized epilepsy and episodic ataxia. Am. J. Hum. Genet. 66, 1531-1539. doi: 10.1086/302909
34. Euler, P., Friedrich, B., Ziegler, R., Kuhn, A., Lindenberg, K. S., Weiller, C., et al. (2012). Gene expression analysis on a single cell level in Purkinje cells of Huntington's disease transgenic mice. Neurosci. Lett. 517, 7-12. doi: 10.1016/j.neulet.2012.03.080
35. Falkenburger, B., Jensen, J., and Hille, B. (2010). Kinetics of PIP2 metabolism and KCNQ2/3 channel regulation studied with a voltage-sensitive phosphatase in living cells. J. Gen. Physiol. 135, 99-114. doi: 10.1085/jgp.200910345
36. Fiala, J., Grossberg, S., and Bullock, D. (1996). Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response. J. Neurosci. 16, 3760-3774.
37. Finch, E., and Augustine, G. (1998). Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites. Nature 396, 753-756. doi: 10.1038/25541
38. Friedrich, B., Euler, P., Ziegler, R., Kuhn, A., Landwehrmeyer, B. G., Luthi-Carter, R., et al. (2012). Comparative analyses of Purkinje cell gene expression profiles reveal shared molecular abnormalities in models of different polyglutamine diseases. Brain Res. 1481, 37-48. doi: 10.1016/j.brainres.2012.08.005
39. Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N., and Mikoshiba, K. (1989). Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 342, 32-38. doi: 10.1038/342032a0
40. Gehrking, K. M., Andresen, J. M., Duvick, L., Lough, J., Zoghbi, H. Y., and Orr, H. T. (2011). Partial loss of Tip60 slows mid-stage neurodegeneration in a spinocerebellar ataxia type 1 (SCA1) mouse model. Hum. Mol. Genet. 20, 2204-2212. doi: 10.1093/hmg/ddr108
41. Guergueltcheva, V., Azmanov, D. N., Angelicheva, D., Smith, K. R., Chamova, T., Florez, L., et al. (2012). Autosomal-recessive congenital cerebellar ataxia is caused by mutations in metabotropic glutamate receptor 1. Am. J. Hum. Genet. 91, 553-564. doi: 10.1016/j.ajhg.2012.07.019
42. Guida, S., Trettel, F., Pagnutti, S., Mantuano, E., Tottene, A., Veneziano, L., et al. (2001). 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. 68, 759-764. doi: 10.1086/318804
43. Hall, S., and Armstrong, D. (2000). Conditional and unconditional inhibition of calcium-activated potassium channels by reversible protein phosphorylation. J. Biol. Chem. 275, 3749-3754. doi: 10.1074/jbc.275.6.3749
44. Hansen, S. T., Meera, P., Otis, T. S., and Pulst, S. M. (2013). Changes in Purkinje cell firing and gene expression precede behavioral pathology in a mouse model of SCA2. Hum. Mol. Genet. 22, 271-283. doi: 10.1093/hmg/dds427
45. Hara, K., Shiga, A., Nozaki, H., Mitsui, J., Takahashi, Y., Ishiguro, H., et al. (2008). Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology 71, 547-551. doi: 10.1212/01.wnl.0000311277.71046.a0
46. Harris, K., and Stevens, J. (1988). Dendritic spines of rat cerebellar Purkinje cells: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 8, 4455-4469.
47. Harris, K., and Stevens, J. (1989). Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997.
48. Healy, J., Nilsson, K., Hohmeier, H., Berglund, J., Davis, J., Hoffman, J., et al. (2010). Cholinergic augmentation of insulin release requires ankyrin-B. Sci. Signal. 3, ra19. doi: 10.1126/scisignal.2000771
49. Hearst, S. M., Shao, Q., Lopez, M., Raucher, D., and Vig, P. J. (2014). Focused cerebellar laser light induced hyperthermia improves symptoms and pathology of polyglutamine disease sca1 in a mouse model. Cerebellum 13, 596-606. doi: 10.1007/s12311-014-0576-1
50. Hernjak, N., Slepchenko, B., Fernald, K., Fink, C., Fortin, D., Moraru, I., et al. (2005). Modeling and analysis of calcium signaling events leading to long-term depression in cerebellar Purkinje cells. Biophys. J. 89, 3790-3806. doi: 10.1529/biophysj.105.065771
51. Hilgemann, D., Feng, S., and Nasuhoglu, C. (2001). The complex and intriguing lives of PIP2 with ion channels and transporters. Sci. STKE 2001:re19. doi: 10.1126/stke.2001.111.re19
52. Hirota, J., Ando, H., Hamada, K., and Mikoshiba, K. (2003). Carbonic anhydrase-related protein is a novel binding protein for inositol 1,4,5-trisphosphate receptor type 1. Biochem. J. 372(Pt 2), 435-441. doi: 10.1042/BJ20030110
53. Hisatsune, C., Miyamoto, H., Hirono, M., Yamaguchi, N., Sugawara, T., Ogawa, N., et al. (2013). IP3R1 deficiency in the cerebellum/brainstem causes basal ganglia-independent dystonia by triggering tonic Purkinje cell firings in mice. Front. Neural Circuits 7:156. doi: 10.3389/fncir.2013.00156
54. Huang, L., Chardon, J. W., Carter, M. T., Friend, K. L., Dudding, T. E., Schwartzentruber, J., et al. (2012). Missense mutations in ITPR1 cause autosomal dominant congenital nonprogressive spinocerebellar ataxia. Orphanet J. Rare Dis. 7:67. doi: 10.1186/1750-1172-7-67
55. Ikeda, Y., Dick, K. A., Weatherspoon, M. R., Gincel, D., Armbrust, K. R., Dalton, J. C., et al. (2006). Spectrin mutations cause spinocerebellar ataxia type 5. Nat. Genet. 38, 184-190. doi: 10.1038/ng1728
56. Imbrici, P., Cusimano, A., D'Adamo, M., De Curtis, A., and Pessia, M. (2003). Functional characterization of an episodic ataxia type-1 mutation occurring in the S1 segment of hKv1.1 channels. Pflugers Arch. 446, 373-379. doi: 10.1007/s00424-002-0962-2
57. Imbrici, P., D'Adamo, M., Kullmann, D., and Pessia, M. (2006). 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. 24, 3073-3083. doi: 10.1111/j.1460-9568.2006.05186.x
58. Inoue, T., Lin, X., Kohlmeier, K., Orr, H., Zoghbi, H., and Ross, W. (2001). Calcium dynamics and electrophysiological properties of cerebellar Purkinje cells in SCA1 transgenic mice. J. Neurophysiol. 85, 1750-1760. Available online at: http://jn.physiology.org/content/85/4/1750.long
59. Ishikawa, K., Tanaka, H., Saito, M., Ohkoshi, N., Fujita, T., Yoshizawa, K., et al. (1997). Japanese families with autosomal dominant pure cerebellar ataxia map to chromosome 19p13.1-p13.2 and are strongly associated with mild CAG expansions in the spinocerebellar ataxia type 6 gene in chromosome 19p13.1. Am. J. Hum. Genet. 61, 336-346. doi: 10.1086/514867
60. Ito, M., Sakurai, M., and Tongroach, P. (1982). Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. 324, 113-134. doi: 10.1113/jphysiol.1982.sp014103
61. Iwaki, A., Kawano, Y., Miura, S., Shibata, H., Matsuse, D., Li, W., et al. (2008). Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16. J. Med. Genet. 45, 32-35. doi: 10.1136/jmg.2007.053942
62. Ji, J., Hassler, M. L., Shimobayashi, E., Paka, N., Streit, R., and Kapfhammer, J. P. (2014). Increased protein kinase C gamma activity induces Purkinje cell pathology in a mouse model of spinocerebellar ataxia 14. Neurobiol. Dis. 70C, 1-11. doi: 10.1016/j.nbd.2014.06.002
63. Jiao, Y., Yan, J., Zhao, Y., Donahue, L. R., Beamer, W. G., Li, X., et al. (2005). Carbonic anhydrase-related protein VIII deficiency is associated with a distinctive lifelong gait disorder in waddles mice. Genetics 171, 1239-1246. doi: 10.1534/genetics.105.044487
64. Kasumu, A., and Bezprozvanny, I. (2012). Deranged calcium signaling in Purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias. Cerebellum 11, 630-639. doi: 10.1007/s12311-010-0182-9
65. Kasumu, A. W., Hougaard, C., Rode, F., Jacobsen, T. A., Sabatier, J. M., Eriksen, B. L., et al. (2012). 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. doi: 10.1016/j.chembiol.2012.07.013
66. Kawaguchi, Y., Okamoto, T., Taniwaki, M., Aizawa, M., Inoue, M., Katayama, S., et al. (1994). CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nat. Genet. 8, 221-228. doi: 10.1038/ng1194-221
67. Koide, R., Ikeuchi, T., Onodera, O., Tanaka, H., Igarashi, S., Endo, K., et al. (1994). Unstable expansion of CAG repeat in hereditary dentatorubral-pallidoluysian atrophy (DRPLA). Nat. Genet. 6, 9-13. doi: 10.1038/ng0194-9
68. Koide, R., Kobayashi, S., Shimohata, T., Ikeuchi, T., Maruyama, M., Saito, M., et al. (1999). A neurological disease caused by an expanded CAG trinucleotide repeat in the TATA-binding protein gene: a new polyglutamine disease? Hum. Mol. Genet. 8, 2047-2053. doi: 10.1093/hmg/8.11.2047
69. Krysa, W., Rajkiewicz, M., and Sulek, A. (2012). Rapid detection of large expansions in progressive myoclonus epilepsy type 1, myotonic dystrophy type 2 and spinocerebellar ataxia type 8. Neurol. Neurochir. Pol. 46, 113-120. doi: 10.5114/ninp.2012.28253
70. Kurnellas, M., Lee, A., Li, H., Deng, L., Ehrlich, D., and Elkabes, S. (2007). Molecular alterations in the cerebellum of the plasma membrane calcium ATPase 2 (PMCA2)-null mouse indicate abnormalities in Purkinje neurons. Mol. Cell. Neurosci. 34, 178-188. doi: 10.1016/j.mcn.2006.10.010
71. Lee, Y. C., Durr, A., Majczenko, K., Huang, Y. H., Liu, Y. C., Lien, C. C., et al. (2012). Mutations in KCND3 cause spinocerebellar ataxia type 22. Ann. Neurol. 72, 859-869. doi: 10.1002/ana.23701
72. Lin, X., Antalffy, B., Kang, D., Orr, H., and Zoghbi, H. (2000). Polyglutamine expansion down-regulates specific neuronal genes before pathologic changes in SCA1. Nat. Neurosci. 3, 157-163. doi: 10.1038/72101
73. Liu, J., Tang, T., Tu, H., Nelson, O., Herndon, E., Huynh, D., et al. (2009). Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2. J. Neurosci. 29, 9148-9162. doi: 10.1523/JNEUROSCI.0660-09.2009
74. Lucchese, G., and Kanduc, D. (2014). Single amino acid repeats connect viruses to neurodegeneration. Curr. Drug Discov. Technol. 11, 214-219. doi: 10.2174/1570163811666140212112300
75. Mandal, A., Shahidullah, M., and Delamere, N. (2010). Hydrostatic pressure-induced release of stored calcium in cultured rat optic nerve head astrocytes. Invest. Ophthalmol. Vis. Sci. 51, 3129-3138. doi: 10.1167/iovs.09-4614
76. Mantuano, E., Veneziano, L., Spadaro, M., Giunti, P., Guida, S., Leggio, M., et al. (2004). Clusters of non-truncating mutations of P/Q type Ca2+ channel subunit Ca(v)2.1 causing episodic ataxia 2. J. Med. Genet. 41, e82. doi: 10.1136/jmg.2003.015396
77. Marelli, C., van de Leemput, J., Johnson, J. O., Tison, F., Thauvin-Robinet, C., Picard, F., et al. (2011). SCA15 due to large ITPR1 deletions in a cohort of 333 white families with dominant ataxia. Arch. Neurol. 68, 637-643. doi: 10.1001/archneurol.2011.81
78. Matsumoto, M., Nakagawa, T., Inoue, T., Nagata, E., Tanaka, K., Takano, H., et al. (1996). Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379, 168-171. doi: 10.1038/379168a0
79. Mikoshiba, K. (2007). IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J. Neurochem. 102, 1426-1446. doi: 10.1111/j.1471-4159.2007.04825.x
80. Miyasho, T., Takagi, H., Suzuki, H., Watanabe, S., Inoue, M., Kudo, Y., et al. (2001). 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. 891, 106-115. doi: 10.1016/S0006-8993(00)03206-6
81. Mondin, L., Balghi, H., Constantin, B., Cognard, C., and Sebille, S. (2009). Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death. Am. J. Physiol. Cell Physiol. 297, C1133-C1145. doi: 10.1152/ajpcell.00048.2009
82. Moseley, M. L., Zu, T., Ikeda, Y., Gao, W., Mosemiller, A. K., Daughters, R. S., et al. (2006). Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat. Genet. 38, 758-769. doi: 10.1038/ng1827
83. Murchison, D., Dove, L., Abbott, L., and Griffith, W. (2002). Homeostatic compensation maintains Ca2+ signaling functions in Purkinje neurons in the leaner mutant mouse. Cerebellum 1, 119-127. doi: 10.1080/147342202753671259
84. Nakamura, K., Jeong, S., Uchihara, T., Anno, M., Nagashima, K., Nagashima, T., et al. (2001). SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum. Mol. Genet. 10, 1441-1448. doi: 10.1093/hmg/10.14.1441
85. Nishizuka, Y. (1984). The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 308, 693-698. doi: 10.1038/308693a0
86. Novak, M., Davis, M., Li, A., Goold, R., Tabrizi, S., Sweeney, M., et al. (2010a). PAW32 ITPR1 gene deletion causes spinocerebellar ataxia 15/16: a genetic, clinical and radiological description of a novel kindred. J. Neurol. Neurosurg. Psychiatr. 81, e32. doi: 10.1136/jnnp.2010.226340.60
87. Novak, M. J., Sweeney, M. G., Li, A., Treacy, C., Chandrashekar, H. S., Giunti, P., et al. (2010b). An ITPR1 gene deletion causes spinocerebellar ataxia 15/16: a genetic, clinical and radiological description. Mov. Disord. 25, 2176-2182. doi: 10.1002/mds.23223
88. Obayashi, M., Ishikawa, K., Izumi, Y., Takahashi, M., Niimi, Y., Sato, N., et al. (2012). Prevalence of inositol 1, 4, 5-triphosphate receptor type 1 gene deletion, the mutation for spinocerebellar ataxia type 15, in Japan screened by gene dosage. J. Hum. Genet. 57, 202-206. doi: 10.1038/jhg.2012.5
89. Ogasawara, H., Doi, T., Doya, K., and Kawato, M. (2007). Nitric oxide regulates input specificity of long-term depression and context dependence of cerebellar learning. PLoS Comput. Biol. 3:e179. doi: 10.1371/journal.pcbi.0020179
90. Ogasawara, H., Doi, T., and Kawato, M. (2008). Systems biology perspectives on cerebellar long-term depression. Neurosignals 16, 300-317. doi: 10.1159/000123040
91. Ogura, H., Matsumoto, M., and Mikoshiba, K. (2001). Motor discoordination in mutant mice heterozygous for the type 1 inositol 1,4,5-trisphosphate receptor. Behav. Brain Res. 122, 215-219. doi: 10.1016/S0166-4328(01)00187-5
92. Orr, H., Chung, M., Banfi, S., Kwiatkowski, T. J., Servadio, A., Beaudet, A., et al. (1993). Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nat. Genet. 4, 221-226. doi: 10.1038/ng0793-221
93. Park, K., Yule, D., and Bowers, W. (2010). Impaired TNF-alpha control of IP3R-mediated Ca2+ release in Alzheimer's disease mouse neurons. Cell. Signal. 22, 519-526. doi: 10.1016/j.cellsig.2009.11.006
94. Paulson, H., Perez, M., Trottier, Y., Trojanowski, J., Subramony, S., Das, S., et al. (1997). Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron 19, 333-344. doi: 10.1016/S0896-6273(00)80943-5
95. Pulst, S., Nechiporuk, A., Nechiporuk, T., Gispert, S., Chen, X., Lopes-Cendes, I., et al. (1996). Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2. Nat. Genet. 14, 269-276. doi: 10.1038/ng1196-269
96. Santamaria, F., Wils, S., De Schutter, E., and Augustine, G. (2006). Anomalous diffusion in Purkinje cell dendrites caused by spines. Neuron 52, 635-648. doi: 10.1016/j.neuron.2006.10.025
97. Sarkisov, D., and Wang, S. (2008). Order-dependent coincidence detection in cerebellar Purkinje neurons at the inositol trisphosphate receptor. J. Neurosci. 28, 133-142. doi: 10.1523/JNEUROSCI.1729-07.2008
98. Sausbier, M., Hu, H., Arntz, C., Feil, S., Kamm, S., Adelsberger, H., et al. (2004). Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2+-activated K+ channel deficiency. Proc. Natl. Acad. Sci. U.S.A. 101, 9474-9478. doi: 10.1073/pnas.0401702101
99. Schorge, S., van de Leemput, J., Singleton, A., Houlden, H., and Hardy, J. (2010). Human ataxias: a genetic dissection of inositol triphosphate receptor (ITPR1)-dependent signaling. Trends Neurosci. 33, 211-219. doi: 10.1016/j.tins.2010.02.005
100. Serra, H., Byam, C., Lande, J., Tousey, S., Zoghbi, H., and Orr, H. (2004). Gene profiling links SCA1 pathophysiology to glutamate signaling in Purkinje cells of transgenic mice. Hum. Mol. Genet. 13, 2535-2543. doi: 10.1093/hmg/ddh268
101. Serra, H., Duvick, L., Zu, T., Carlson, K., Stevens, S., Jorgensen, N., et al. (2006). RORalpha-mediated Purkinje cell development determines disease severity in adult SCA1 mice. Cell 127, 697-708. doi: 10.1016/j.cell.2006.09.036
102. Shipston, M., and Armstrong, D. (1996). Activation of protein kinase C inhibits calcium-activated potassium channels in rat pituitary tumour cells. J Physiol 493(Pt 3), 665-672. doi: 10.1113/jphysiol.1996.sp021413
103. Shuvaev, A. N., Horiuchi, H., Seki, T., Goenawan, H., Irie, T., Iizuka, A., et al. (2011). Mutant PKCgamma in spinocerebellar ataxia type 14 disrupts synapse elimination and long-term depression in Purkinje cells in vivo. J. Neurosci. 31, 14324-14334. doi: 10.1523/JNEUROSCI.5530-10.2011
104. Street, V., Bosma, M., Demas, V., Regan, M., Lin, D., Robinson, L., et al. (1997). The type 1 inositol 1,4,5-trisphosphate receptor gene is altered in the opisthotonos mouse. J. Neurosci. 17, 635-645.
105. Sugawara, T., Hisatsune, C., Le, T. D., Hashikawa, T., Hirono, M., Hattori, M., et al. (2013). Type 1 inositol trisphosphate receptor regulates cerebellar circuits by maintaining the spine morphology of purkinje cells in adult mice. J. Neurosci. 33, 12186-12196. doi: 10.1523/JNEUROSCI.0545-13.2013
106. Suzuki, K., Zhou, J., Sato, T., Takao, K., Miyagawa, T., Oyake, M., et al. (2012). DRPLA transgenic mouse substrains carrying single copy of full-length mutant human DRPLA gene with variable sizes of expanded CAG repeats exhibit CAG repeat length- and age-dependent changes in behavioral abnormalities and gene expression profiles. Neurobiol. Dis. 46, 336-350. doi: 10.1016/j.nbd.2012.01.014
107. Switonski, P. M., Szlachcic, W. J., Krzyzosiak, W. J., and Figiel, M. (2014). A new humanized ataxin-3 knock-in mouse model combines the genetic features, pathogenesis of neurons and glia and late disease onset of SCA3/MJD. Neurobiol. Dis. 73, 174-188. doi: 10.1016/j.nbd.2014.09.020
108. Takechi, H., Eilers, J., and Konnerth, A. (1998). A new class of synaptic response involving calcium release in dendritic spines. Nature 396, 757-760. doi: 10.1038/25547
109. Tang, T., Guo, C., Wang, H., Chen, X., and Bezprozvanny, I. (2009). Neuroprotective effects of inositol 1,4,5-trisphosphate receptor C-terminal fragment in a Huntington's disease mouse model. J. Neurosci. 29, 1257-1266. doi: 10.1523/JNEUROSCI.4411-08.2009
110. Tang, T., Tu, H., Wang, Z., and Bezprozvanny, I. (2003). Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase a and protein phosphatase 1alpha. J. Neurosci. 23, 403-415. Available online at: http://www.jneurosci.org/content/23/2/403.long
111. Tonelli, A., D'Angelo, M., Salati, R., Villa, L., Germinasi, C., Frattini, T., et al. (2006). Early onset, non fluctuating spinocerebellar ataxia and a novel missense mutation in CACNA1A gene. J. Neurol. Sci. 241, 13-17. doi: 10.1016/j.jns.2005.10.007
112. Trottier, Y., Biancalana, V., and Mandel, J. (1994). Instability of CAG repeats in Huntington's disease: relation to parental transmission and age of onset. J. Med. Genet. 31, 377-382. doi: 10.1136/jmg.31.5.377
113. Tu, H., Miyakawa, T., Wang, Z., Glouchankova, L., Iino, M., and Bezprozvanny, I. (2002). Functional characterization of the type 1 inositol 1,4,5-trisphosphate receptor coupling domain SII(+/-) splice variants and the Opisthotonos mutant form. Biophys. J. 82, 1995-2004. doi: 10.1016/S0006-3495(02)75548-3
114. Tu, H., Tang, T., Wang, Z., and Bezprozvanny, I. (2004). Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J. Biol. Chem. 279, 19375-19382. doi: 10.1074/jbc. M313476200
115. Tu, H., Wang, Z., Nosyreva, E., De Smedt, H., and Bezprozvanny, I. (2005). Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms. Biophys. J. 88, 1046-1055. doi: 10.1529/biophysj.104.049593
116. Türkmen, S., Guo, G., Garshasbi, M., Hoffmann, K., Alshalah, A. J., Mischung, C., et al. (2009). CA8 mutations cause a novel syndrome characterized by ataxia and mild mental retardation with predisposition to quadrupedal gait. PLoS Genet. 5:e1000487. doi: 10.1371/journal.pgen.1000487
117. Van De Leemput, J., Chandran, J., Knight, M., Holtzclaw, L., Scholz, S., Cookson, M., et al. (2007). Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans. PLoS Genet. 3:e108. doi: 10.1371/journal.pgen.0030108
118. Van Gaalen, J., Vermeer, S., van Veluw, M., van de Warrenburg, B. P., and Dooijes, D. (2013). A de novo SCA14 mutation in an isolated case of late-onset cerebellar ataxia. Mov. Disord. 28, 1902-1903. doi: 10.1002/mds.25572
119. Vig, P., Subramony, S., Burright, E., Fratkin, J., McDaniel, D., Desaiah, D., et al. (1998). Reduced immunoreactivity to calcium-binding proteins in Purkinje cells precedes onset of ataxia in spinocerebellar ataxia-1 transgenic mice. Neurology 50, 106-113. doi: 10.1212/WNL.50.1.106
120. Vig, P., Subramony, S., and McDaniel, D. (2001). Calcium homeostasis and spinocerebellar ataxia-1 (SCA-1). Brain Res. Bull. 56, 221-225. doi: 10.1016/S0361-9230(01)00595-0
121. Wagner, L. N., Li, W., and Yule, D. (2003). 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. 278, 45811-45817. doi: 10.1074/jbc. M306270200
122. Walter, J., Alviña, K., Womack, M., Chevez, C., and Khodakhah, K. (2006). Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat. Neurosci. 9, 389-397. doi: 10.1038/nn1648
123. Wang, S., Denk, W., and Häusser, M. (2000). Coincidence detection in single dendritic spines mediated by calcium release. Nat. Neurosci. 3, 1266-1273. doi: 10.1038/81792
124. Waters, M. F., Minassian, N. A., Stevanin, G., Figueroa, K. P., Bannister, J. P., Nolte, D., et al. (2006). Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat. Genet. 38, 447-451. doi: 10.1038/ng1758
125. Weaver, A., Olsen, M., McFerrin, M., and Sontheimer, H. (2007). 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. 282, 31558-31568. doi: 10.1074/jbc. M702866200
126. Widmer, H., Rowe, I., and Shipston, M. (2003). Conditional protein phosphorylation regulates BK channel activity in rat cerebellar Purkinje neurons. J. Physiol. 552(Pt 2), 379-391. doi: 10.1113/jphysiol.2003.046441
127. Womack, M., Chevez, C., and Khodakhah, K. (2004). Calcium-activated potassium channels are selectively coupled to P/Q-type calcium channels in cerebellar Purkinje neurons. J. Neurosci. 24, 8818-8822. doi: 10.1523/JNEUROSCI.2915-04.2004
128. Womack, M., and Khodakhah, K. (2003). Somatic and dendritic small-conductance calcium-activated potassium channels regulate the output of cerebellar Purkinje neurons. J. Neurosci. 23, 2600-2607. doi: 10.1523/JNEUROSCI.2915-04.2004
129. Xu, C., Watras, J., and Loew, L. (2003). Kinetic analysis of receptor-activated phosphoinositide turnover. J. Cell Biol. 161, 779-791. doi: 10.1083/jcb.200301070
130. Yan, J., Jiao, Y., Jiao, F., Stuart, J., Donahue, L. R., Beamer, W. G., et al. (2007). Effects of carbonic anhydrase VIII deficiency on cerebellar gene expression profiles in the wdl mouse. Neurosci. Lett. 413, 196-201. doi: 10.1016/j.neulet.2006.11.046
131. Zecevic, N., Milosevic, A., and Ehrlich, B. (1999). Calcium signaling molecules in human cerebellum at midgestation and in ataxia. Early Hum. Dev. 54, 103-116. doi: 10.1016/S0378-3782(98)00090-5
132. Zhang, X., Chen, X., Jia, C., Geng, X., Du, X., and Zhang, H. (2010). Depolarization increases phosphatidylinositol (PI) 4,5-bisphosphate level and KCNQ currents through PI 4-kinase mechanisms. J. Biol. Chem. 285, 9402-9409. doi: 10.1074/jbc. M109.068205
133. Zhao, G., Neeb, Z. P., Leo, M. D., Pachuau, J., Adebiyi, A., Ouyang, K. et al. (2010). Type 1 IP3 receptors activate BKCa channels via local molecular coupling in arterial smooth muscle cells. J. Gen. Physiol. 136, 283-291. doi: 10.1085/jgp.201010453