Torsin A Localization in the Mouse Cerebellar Synaptic Circuitry

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Puglisi, Francesca ^a   Vanni, Valentina ^a   Ponterio, Giulia ^a   Tassone, Annalisa ^a   Sciamanna, Giuseppe ^a   Bonsi, Paola ^a   Pisani, Antonio ^a   Mandolesi, Georgia ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PROTEIN; TORSIN A; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; CHAPERONE; DYT1 PROTEIN, MOUSE; GLUTAMIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN SYNAPTOSOME; CEREBELLUM NUCLEUS; CONTROLLED STUDY; GABAERGIC TRANSMISSION; GLIA CELL; JUVENILE ANIMAL; MOUSE; NERVE ENDING; NONHUMAN; PERINATAL PERIOD; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PURKINJE CELL; SPINAL NERVE; SYNAPTOGENESIS; ANIMAL; C57BL MOUSE; CEREBELLUM; GENETICS; METABOLISM; SYNAPSE;

MUS;

ANIMALS; CEREBELLUM; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MICE; MICE, INBRED C57BL; MOLECULAR CHAPERONES; SYNAPSES;

EID: 84879236801     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068063     Document Type: Article

References (71)

1. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, et al. (1997) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat Genet 17: 40-48. doi:10.1038/ng0997-40. PubMed: 9288096.
2. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, et al. (1998) The gene (DYT1) for early-onset torsion dystonia encodes a novel protein related to the Clp protease/heat shock family. Adv Neurol 78: 93-105. PubMed: 9750906.
3. Vale RD, (2000) AAA proteins. Lords of the ring. J Cell Biol 150: F13-F19. doi:10.1083/jcb.150.1.13. PubMed: 10893253.
4. Neychev VK, Fan X, Mitev VI, Hess EJ, Jinnah HA, (2008) The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain 131: 2499-2509. doi:10.1093/brain/awn168. PubMed: 18669484.
5. Argyelan M, Carbon M, Niethammer M, Ulug AM, Voss HU, et al. (2009) Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci 29: 9740-9747. doi:10.1523/JNEUROSCI.2300-09.2009. PubMed: 19657027.
6. Uluǧ AM, Vo A, Argyelan M, Tanabe L, Schiffer WK, et al. (2011) Cerebellothalamocortical pathway abnormalities in torsinA DYT1 knock-in mice. Proc Natl Acad Sci U S A 108: 6638-6643. doi:10.1073/pnas.1016445108. PubMed: 21464304.
7. Neychev VK, Gross RE, Lehéricy S, Hess EJ, Jinnah HA, (2011) The functional neuroanatomy of dystonia. Neurobiol Dis 42: 185-201. doi:10.1016/j.nbd.2011.01.026. PubMed: 21303695.
8. Goodchild RE, Kim CE, Dauer WT, (2005) Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48: 923-932. doi:10.1016/j.neuron.2005.11.010. PubMed: 16364897.
9. Hewett JW, Zeng J, Niland BP, Bragg DC, Breakefield XO, (2006) Dystonia-causing mutant torsinA inhibits cell adhesion and neurite extension through interference with cytoskeletal dynamics. Neurobiol Dis 22: 98-111. doi:10.1016/j.nbd.2005.10.012. PubMed: 16361107.
10. Naismith TV, Heuser JE, Breakefield XO, Hanson PI, (2004) TorsinA in the nuclear envelope. Proc Natl Acad Sci U S A 101: 7612-7617. doi:10.1073/pnas.0308760101. PubMed: 15136718.
11. Ferrari-Toninelli G, Paccioretti S, Francisconi S, Uberti D, Memo M, (2004) TorsinA negatively controls neurite outgrowth of SH-SY5Y human neuronal cell line; Res B, eds.
12. Hewett J, Gonzalez-Agosti C, Slater D, Ziefer P, Li S, et al. (2000) Mutant torsinA, responsible for early-onset torsion dystonia, forms membrane inclusions in cultured neural cells. Hum Mol Genet 9: 1403-1413. doi:10.1093/hmg/9.9.1403. PubMed: 10814722.
13. Kamm C, Boston H, Hewett J, Wilbur J, Corey DP, et al. (2004) The early onset dystonia protein torsinA interacts with kinesin light chain 1. J Biol Chem 279: 19882-19892. doi:10.1074/jbc.M401332200. PubMed: 14970196.
14. Nery FC, Zeng J, Niland BP, Hewett J, Farley J, et al. (2008) TorsinA binds the KASH domain of nesprins and participates in linkage between nuclear envelope and cytoskeleton. J Cell Sci 121: 3476-3486. doi:10.1242/jcs.029454. PubMed: 18827015.
15. Nery FC, Armata IA, Farley JE, Cho JA, Yaqub U, et al. (2011) TorsinA participates in endoplasmic reticulum-associated degradation. Nat Commun 2: 393. doi:10.1038/ncomms1383. PubMed: 21750546.
16. Hewett JW, Nery FC, Niland B, Ge P, Tan P, et al. (2008) siRNA knock-down of mutant torsinA restores processing through secretory pathway in DYT1 dystonia cells. Hum Mol Genet 17: 1436-1445. doi:10.1093/hmg/ddn032. PubMed: 18258738.
17. Misbahuddin A, Placzek MR, Taanman JW, Gschmeissner S, Schiavo G, et al. (2005) Mutant torsinA, which causes early-onset primary torsion dystonia, is redistributed to membranous structures enriched in vesicular monoamine transporter in cultured human SH-SY5Y cells. Mov Disord 20: 432-440. doi:10.1002/mds.20351. PubMed: 15593317.
18. Torres GE, Sweeney AL, Beaulieu JM, Shashidharan P, Caron MG, (2004) Effect of torsinA on membrane proteins reveals a loss of function and a dominant-negative phenotype of the dystonia-associated DeltaE-torsinA mutant. Proc Natl Acad Sci U S A 101: 15650-15655. doi:10.1073/pnas.0308088101. PubMed: 15505207.
19. Granata A, Watson R, Collinson LM, Schiavo G, Warner TT, (2008) The dystonia-associated protein torsinA modulates synaptic vesicle recycling. J Biol Chem 283: 7568-7579. doi:10.1074/jbc.M704097200. PubMed: 18167355.
20. Granata A, Koo SJ, Haucke V, Schiavo G, Warner TT, (2011) CSN complex controls the stability of selected synaptic proteins via a torsinA-dependent process. EMBO J 30: 181-193. doi:10.1038/emboj.2010.285. PubMed: 21102408.
21. Kakazu Y, Koh JY, Ho KW, Gonzalez-Alegre P, Harata NC, (2012) Synaptic vesicle recycling is enhanced by torsinA that harbors the DYT1 dystonia mutation. Synapse 66: 453-464. doi:10.1002/syn.21534. PubMed: 22213465.
22. Kakazu Y, Koh JY, Iwabuchi S, Gonzalez-Alegre P, Harata NC, (2012) Miniature release events of glutamate from hippocampal neurons are influenced by the dystonia-associated protein torsinA. Synapse 66: 807-822. doi:10.1002/syn.21571. PubMed: 22588999.
23. Warner TT, Granata A, Schiavo G, (2010) TorsinA and DYT1 dystonia: a synaptopathy? Biochem Soc Trans 38: 452-456. doi:10.1042/BST0380452. PubMed: 20298201.
24. Augood SJ, Keller-McGandy CE, Siriani A, Hewett J, Ramesh V, et al. (2003) Distribution and ultrastructural localization of torsinA immunoreactivity in the human brain. Brain Res 986: 12-21. doi:10.1016/S0006-8993(03)03164-0. PubMed: 12965225.
25. Konakova M, Huynh DP, Yong W, Pulst SM, (2001) Cellular distribution of torsin A and torsin B in normal human brain. Arch Neurol 58: 921-927. doi:10.1001/archneur.58.6.921. PubMed: 11405807.
26. Konakova M, Pulst SM, (2001) Immunocytochemical characterization of torsin proteins in mouse brain. Brain Res 922: 1-8. doi:10.1016/S0006-8993(01)03014-1. PubMed: 11730696.
27. Rostasy K, Augood SJ, Hewett JW, Leung JC, Sasaki H, et al. (2003) TorsinA protein and neuropathology in early onset generalized dystonia with GAG deletion. Neurobiol Dis 12: 11-24. doi:10.1016/S0969-9961(02)00010-4. PubMed: 12609485.
28. Shashidharan P, Kramer BC, Walker RH, Olanow CW, Brin MF, (2000) Immunohistochemical localization and distribution of torsinA in normal human and rat brain. Brain Res 853: 197-206. doi:10.1016/S0006-8993(99)02232-5. PubMed: 10640617.
29. Walker RH, Brin MF, Sandu D, Gujjari P, Hof PR, et al. (2001) Distribution and immunohistochemical characterization of torsinA immunoreactivity in rat brain. Brain Res 900: 348-354. doi:10.1016/S0006-8993(01)02302-2. PubMed: 11334819.
30. Xiao J, Gong S, Zhao Y, LeDoux MS, (2004) Developmental expression of rat torsinA transcript and protein. Brain Res Dev Brain Res 152: 47-60. doi:10.1016/j.devbrainres.2004.05.012. PubMed: 15283994.
31. Vasudevan A, Breakefield XO, Bhide PG, (2006) Developmental patterns of torsinA and torsinB expression. Brain Res 1073-1074: 139-145. doi:10.1016/j.brainres.2005.12.087. PubMed: 16458269.
32. Kano M, Watanabe M, (2013) Handbook of the Cerebellum and Cerebellar Disorders; ed S, editor.
33. Sassoè-Pognetto M, Patrizi A, (2013) Handbook of the Cerebellum and Cerebellar Disorders; Science S, editor.
34. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics Int 11: 36-42.
35. Sciamanna G, Tassone A, Mandolesi G, Puglisi F, Ponterio G, et al. (2012) Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J Neurosci 32: 11991-12004. doi:10.1523/JNEUROSCI.0041-12.2012. PubMed: 22933784.
36. Buchwalow IB, Bocker W, (2010) Immunohistochemistry: Basics and Methods Springer, editor.
37. Mandolesi G, Vanni V, Cesa R, Grasselli G, Puglisi F, et al. (2009) Distribution of the SNAP25 and SNAP23 synaptosomal-associated protein isoforms in rat cerebellar cortex. Neuroscience 164: 1084-1096. doi:10.1016/j.neuroscience.2009.08.067. PubMed: 19735702.
38. Li Q, Lau A, Morris TJ, Guo L, Fordyce CB, et al. (2004) A syntaxin 1, Galpha(o), and N-type calcium channel complex at a presynaptic nerve terminal: analysis by quantitative immunocolocalization. J Neurosci 24: 4070-4081. doi:10.1523/JNEUROSCI.0346-04.2004. PubMed: 15102922.
39. Bolte S, Cordelières FP, (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224: 213-232. doi:10.1111/j.1365-2818.2006.01706.x. PubMed: 17210054.
40. Diño MR, Willard FH, Mugnaini E, (1999) Distribution of unipolar brush cells and other calretinin immunoreactive components in the mammalian cerebellar cortex. J Neurocytol 28: 99-123. doi:10.1023/A:1007072105919. PubMed: 10590511.
41. De Zeeuw CI, Berrebi AS, (1995) Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat. Eur J Neurosci 7: 2322-2333. doi:10.1111/j.1460-9568.1995.tb00653.x. PubMed: 8563981.
42. Crepel F, Mariani J, Delhaye-Bouchaud N, (1976) Evidence for a multiple innervation of Purkinje cells by climbing fibers in the immature rat cerebellum. J Neurobiol 7: 567-578. doi:10.1002/neu.480070609. PubMed: 1003202.
43. 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. doi:10.1016/j.neuron.2009.06.008. PubMed: 19607796.
44. Ito M, (1984) The modifiable neuronal network of the cerebellum. Jpn J Physiol 34: 781-792. doi:10.2170/jjphysiol.34.781. PubMed: 6099855.
45. Fremeau RT Jr., Troyer MD, Pahner I, Nygaard GO, Tran CH, et al. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260. doi:10.1016/S0896-6273(01)00344-0. PubMed: 11502256.
46. Sotelo C, (2008) Development of "Pinceaux" formations and dendritic translocation of climbing fibers during the acquisition of the balance between glutamatergic and gamma-aminobutyric acidergic inputs in developing Purkinje cells. J Comp Neurol 506: 240-262. doi:10.1002/cne.21501. PubMed: 18022955.
47. Ango F, di Cristo G, Higashiyama H, Bennett V, Wu P, et al. (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119: 257-272. doi:10.1016/j.cell.2004.10.004. PubMed: 15479642.
48. Garin N, Escher G, (2001) The development of inhibitory synaptic specializations in the mouse deep cerebellar nuclei. Neuroscience 105: 431-441. doi:10.1016/S0306-4522(01)00127-0. PubMed: 11672609.
49. Bostan AC, Strick PL, (2010) The cerebellum and basal ganglia are interconnected. Neuropsychol Rev 20: 261-270. doi:10.1007/s11065-010-9143-9. PubMed: 20811947.
50. Palay SL, Chan-Palay V, (1974) Cerebellar cortex: cytology and organization; Springer-Verlag, editor.
51. Eccles JC, Sasaki K, Strata P, (1967) A comparison of the inhibitory actions of Golgi cells and of basket cells. Exp Brain Res 3: 81-94. PubMed: 6031001.
52. Larramendi LM, (1969) Electron microscopic studies of cerebellar interneurons; Sci UFM, editor.
53. Cathala L, Holderith NB, Nusser Z, DiGregorio DA, Cull-Candy SG, (2005) Changes in synaptic structure underlie the developmental speeding of AMPA receptor-mediated EPSCs. Nat Neurosci 8: 1310-1318. doi:10.1038/nn1534. PubMed: 16172604.
54. Granata A, Schiavo G, Warner TT, (2009) TorsinA and dystonia: from nuclear envelope to synapse. J Neurochem 109: 1596-1609. doi:10.1111/j.1471-4159.2009.06095.x. PubMed: 19457118.
55. Bramham CR, Wells DG, (2007) Dendritic mRNA: transport, translation and function. Nat Rev Neurosci 8: 776-789. doi:10.1038/nrg2172. PubMed: 17848965.
56. Martella G, Tassone A, Sciamanna G, Platania P, Cuomo D, et al. (2009) Impairment of bidirectional synaptic plasticity in the striatum of a mouse model of DYT1 dystonia: role of endogenous acetylcholine. Brain 132: 2336-2349. doi:10.1093/brain/awp194. PubMed: 19641103.
57. Zhang L, Yokoi F, Jin YH, DeAndrade MP, Hashimoto K, et al. (2011) Altered dendritic morphology of Purkinje cells in Dyt1 DeltaGAG knock-in and purkinje cell-specific Dyt1 conditional knockout mice. PLOS ONE 6: e18357. doi:10.1371/journal.pone.0018357. PubMed: 21479250.
58. Lippman Bell JJ, Lordkipanidze T, Cobb N, Dunaevsky A, (2010) Bergmann glial ensheathment of dendritic spines regulates synapse number without affecting spine motility. Neuron Glia Biol 6: 193-200. doi:10.1017/S1740925X10000165. PubMed: 21044397.
59. de Blas AL, (1984) Monoclonal antibodies to specific astroglial and neuronal antigens reveal the cytoarchitecture of the Bergmann glia fibers in the cerebellum. J Neurosci 4: 265-273. PubMed: 6693942.
60. Grosche J, Kettenmann H, Reichenbach A, (2002) Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res 68: 138-149. doi:10.1002/jnr.10197. PubMed: 11948659.
61. Zhao Y, Xiao J, Ueda M, Wang Y, Hines M, et al. (2008) Glial elements contribute to stress-induced torsinA expression in the CNS and peripheral nervous system. Neuroscience 155: 439-453. doi:10.1016/j.neuroscience.2008.04.053. PubMed: 18538941.
62. Ziefer P, Leung J, Razzano T, Shalish C, LeDoux MS, et al. (2002) Molecular cloning and expression of rat torsinA in the normal and genetically dystonic (dt) rat. Brain Res Mol Brain Res 101: 132-135. doi:10.1016/S0169-328X(02)00176-6. PubMed: 12007841.
63. Augood SJ, Martin DM, Ozelius LJ, Breakefield XO, Penney JB Jr., et al. (1999) Distribution of the mRNAs encoding torsinA and torsinB in the normal adult human brain. Ann Neurol 46: 761-769. doi:10.1002/1531-8249(199911)46:5. PubMed: 10553994.
64. McAllister AK, (2007) Dynamic aspects of CNS synapse formation. Annu Rev Neurosci 30: 425-450. doi:10.1146/annurev.neuro.29.051605.112830. PubMed: 17417940.
65. Waites CL, Craig AM, Garner CC, (2005) Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci 28: 251-274. doi:10.1146/annurev.neuro.27.070203.144336. PubMed: 16022596.
66. Yuzaki M, (2010) Synapse formation and maintenance by C1q family proteins: a new class of secreted synapse organizers. Eur J Neurosci 32: 191-197. doi:10.1111/j.1460-9568.2010.07346.x. PubMed: 20646056.
67. Esapa CT, Waite A, Locke M, Benson MA, Kraus M, et al. (2007) SGCE missense mutations that cause myoclonus-dystonia syndrome impair epsilon-sarcoglycan trafficking to the plasma membrane: modulation by ubiquitination and torsinA. Hum Mol Genet 16: 327-342. PubMed: 17200151.
68. Patrizi A, Scelfo B, Viltono L, Briatore F, Fukaya M, et al. (2008) Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc Natl Acad Sci U S A 105: 13151-13156. doi:10.1073/pnas.0802390105. PubMed: 18723687.
69. Craig AM, Lichtman JW, (2001) Getting a bead on receptor movements. Nat Neurosci 4: 219-220. doi:10.1038/85042. PubMed: 11224530.
70. Lohof AM, Delhaye-Bouchaud N, Mariani J, (1996) Synapse elimination in the central nervous system: functional significance and cellular mechanisms. Rev Neurosci 7: 85-101. PubMed: 8819204.
71. Breakefield XO, Blood AJ, Li Y, Hallett M, Hanson PI, et al. (2008) The pathophysiological basis of dystonias. Nat Rev Neurosci 9: 222-234. doi:10.1038/nrn2337. PubMed: 18285800.