Forebrain deletion of the dystonia protein torsinA causes dystonic-like movements and loss of striatal cholinergic neurons

eLife

Volumn 4, Issue JUNE, 2015, Pages 1-25

  Pappas, Samuel S ^a   Darr, Katherine ^a   Holley, Sandra M ^b   Cepeda, Carlos ^b   Mabrouk, Omar S ^c   Wong, Jenny Marie T ^c   LeWitt, Tessa M ^a   Paudel, Reema ^d   Houlden, Henry ^d   Kennedy, Robert T ^c   Levine, Michael S ^b   Dauer, William T ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

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

AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR ASSESSMENT; CELL COUNTING; CELL DEATH; CELL DENSITY; CELL LOSS; CELL MATURATION; CELL SIZE; CELL SURVIVAL; CHROMOSOME ABERRATION; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DYSTONIA; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOLOGY; HUMAN; IMMUNOCHEMISTRY; LOSS OF FUNCTION MUTATION; MALE; MASS SPECTROMETRY; MOUSE; NERVE CELL DEGENERATION; NEUROCHEMISTRY; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STRIATE CORTEX; VERY ELDERLY; WESTERN BLOTTING; ANIMAL; CHOLINERGIC NERVE CELL; CORPUS STRIATUM; EMBRYOLOGY; FOREBRAIN; GENE DELETION; GENETICS; MOVEMENT (PHYSIOLOGY); PATHOLOGY;

ANIMALIA; MURINAE;

ANIMALS; CHOLINERGIC NEURONS; CORPUS STRIATUM; DYSTONIA; GENE DELETION; MICE; MOLECULAR CHAPERONES; MOVEMENT; PROSENCEPHALON;

EID: 85016002412     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08352     Document Type: Article

References (61)

1. Albin RL, Cross D, Cornblath WT, Wald JA, Wernette K, Frey KA, Minoshima S. 2003. Diminished striatal [123I] iodobenzovesamicol binding in idiopathic cervical dystonia. Ann Neurol 53:528-532.
2. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience 9:357-381. doi: 10.1146/annurev.ne.09.030186.002041.
3. Berke JD. 2011. Functional properties of striatal fast-spiking interneurons. Frontiers in Systems Neuroscience 5:45. doi: 10.3389/fnsys.2011.00045.
4. Bressman SB, Sabatti C, Raymond D, de Leon D, Klein C, Kramer PL, Brin MF, Fahn S, Breakefield X, Ozelius LJ, Risch NJ. 2000. The DYT1 phenotype and guidelines for diagnostic testing. Neurology 54:1746-1752. doi: 10. 1212/WNL.54.9.1746.
5. Burke RE, Fahn S, Marsden CD. 1986. Torsion dystonia: a double-blind, prospective trial of high-dosage trihexyphenidyl. Neurology 36:160-164. doi: 10.1212/WNL.36.2.160.
6. Burke RE, Karanas AL. 1990. Quantitative morphological analysis of striatal cholinergic neurons in perinatal asphyxia. Annals of Neurology 27:81-88. doi: 10.1002/ana.410270113.
7. Carbon M, Argyelan M, Ghilardi MF, Mattis P, Dhawan V, Bressman S, Eidelberg D. 2011. Impaired sequence learning in dystonia mutation carriers: a genotypic effect. Brain 134:1416-1427. doi: 10.1093/brain/awr060.
8. Cepeda C, Galvan L, Holley SM, Rao SP, Andre VM, Botelho EP, Chen JY, Watson JB, Deisseroth K, Levine MS. 2013. Multiple sources of striatal inhibition are differentially affected in Huntington's disease mouse models. The Journal of Neuroscience 33:7393-7406. doi: 10.1523/JNEUROSCI.2137-12.2013.
9. Chen P, Burdette AJ, Porter JC, Ricketts JC, Fox SA, Nery FC, Hewett JW, Berkowitz LA, Breakefield XO, Caldwell KA, Caldwell GA. 2010. The early-onset torsion dystonia-associated protein, torsinA, is a homeostatic regulator of endoplasmic reticulum stress response. Human Molecular Genetics 19:3502-3515. doi: 10.1093/hmg/ddq266.
10. Chesselet MF, Plotkin JL, Wu N, Levine MS. 2007. Development of striatal fast-spiking GABAergic interneurons. Progress in Brain Research 160:261-272. doi: 10.1016/S0079-6123(06)60015-0.
11. Dauer W. 2014. Inherited isolated dystonia: clinical genetics and gene function. Neurotherapeutics 11:807-816. doi: 10.1007/s13311-014-0297-7.
12. Eskow Jaunarajs KL, Bonsi P, Chesselet MF, Standaert DG, Pisani A. 2015. Striatal cholinergic dysfunction as a unifying theme in the pathophysiology of dystonia. Progress in Neurobiology 127-128C:91-107. doi: 10.1016/j. pneurobio.2015.02.002.
13. Gage GJ, Stoetzner CR, Wiltschko AB, Berke JD. 2010. Selective activation of striatal fast-spiking interneurons during choice execution. Neuron 67:466-479. doi: 10.1016/j.neuron.2010.06.034.
14. Geneser FA. 1987. Distribution of acetylcholinesterase in the hippocampal region of the rabbit: II. Subiculum and hippocampus. The Journal of Comparative Neurology 262:90-104. doi: 10.1002/cne.902620108.
15. Gerace L. 2004. TorsinA and torsion dystonia: unraveling the architecture of the nuclear envelope. Proceedings of the National Academy of Sciences of USA 101:8839-8840. doi: 10.1073/pnas.0402441101.
16. Gittis AH, Leventhal DK, Fensterheim BA, Pettibone JR, Berke JD, Kreitzer AC. 2011. Selective inhibition of striatal fast-spiking interneurons causes dyskinesias. The Journal of Neuroscience 31:15727-15731. doi: 10.1523/ JNEUROSCI.3875-11.2011.
17. 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.
18. Grundmann K, Glockle N, Martella G, Sciamanna G, Hauser TK, Yu L, Castaneda S, Pichler B, Fehrenbacher B, Schaller M, Nuscher B, Haass C, Hettich J, Yue Z, Nguyen HP, Pisani A, Riess O, Ott T. 2012. Generation of a novel rodent model for DYT1 dystonia. Neurobiology of Disease 47:61-74. doi: 10.1016/j.nbd.2012.03.024.
19. Hattori T, McGeer PL. 1973. Synaptogenesis in the corpus striatum of infant rat. Experimental Neurology 38: 70-79. doi: 10.1016/0014-4886(73)90008-3.
20. Hewett JW, Nery FC, Niland B, Ge P, Tan P, Hadwiger P, Tannous BA, Sah DW, Breakefield XO. 2008. siRNA knock-down of mutant torsinA restores processing through secretory pathway in DYT1 dystonia cells. Human Molecular Genetics 17:1436-1445. doi: 10.1093/hmg/ddn032.
21. Hewett JW, Tannous B, Niland BP, Nery FC, Zeng J, Li Y, Breakefield XO. 2007. Mutant torsinA interferes with protein processing through the secretory pathway in DYT1 dystonia cells. Proceedings of the National Academy of Sciences of USA 104:7271-7276. doi: 10.1073/pnas.0701185104.
22. Holley SM, Joshi PR, Parievsky A, Galvan L, Chen JY, Fisher YE, Huynh MN, Cepeda C, Levine MS. 2015. Enhanced GABAergic inputs contribute to functional alterations of cholinergic interneurons in the R6/2 mouse model of Huntington disease. Eneuro. doi: 10.1523/ENEURO.0008-14.2015.
23. Jankovic J. 2013. Medical treatment of dystonia. Movement Disorders 28:1001-1012. doi: 10.1002/mds.25552.
24. Jokhi V, Ashley J, Nunnari J, Noma A, Ito N, Wakabayashi-Ito N, Moore MJ, Budnik V. 2013. Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Reports 3:988-995. doi: 10.1016/j.celrep.2013.03.015.
25. Kaneko S, Hikida T, Watanabe D, Ichinose H, Nagatsu T, Kreitman RJ, Pastan I, Nakanishi S. 2000. Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. Science 289:633-637. doi: 10. 1126/science.289.5479.633.
26. Koos T, Tepper JM. 2002. Dual cholinergic control of fast-spiking interneurons in the neostriatum. The Journal of Neuroscience 22:529-535.
27. Kreitzer AC. 2009. Physiology and pharmacology of striatal neurons. Annual Review of Neuroscience 32:127-147. doi: 10.1146/annurev.neuro.051508.135422.
28. Lee H, Sawatari A. 2011. Medium spiny neurons of the neostriatal matrix exhibit specific, stereotyped changes in dendritic arborization during a critical developmental period in mice. The European Journal of Neuroscience 34: 1345-1354. doi: 10.1111/j.1460-9568.2011.07852.x.
29. Liang CC, Tanabe LM, Jou S, Chi F, Dauer WT. 2014. TorsinA hypofunction causes abnormal twisting movements and sensorimotor circuit neurodegeneration. The Journal of Clinical Investigation 124:3080-3092. doi: 10.1172/ JCI72830.
30. Marsden CD, Obeso JA, Zarranz JJ, Lang AE. 1985. The anatomical basis of symptomatic hemidystonia. Brain 108: 463-483. doi: 10.1093/brain/108.2.463.
31. Martella G, Tassone A, Sciamanna G, Platania P, Cuomo D, Viscomi MT, Bonsi P, Cacci E, Biagioni S, Usiello A, Bernardi G, Sharma N, Standaert DG, Pisani A. 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.
32. McNaught KS, Kapustin A, Jackson T, Jengelley TA, Jnobaptiste R, Shashidharan P, Perl DP, Pasik P, Olanow CW. 2004. Brainstem pathology in DYT1 primary torsion dystonia. Annals of Neurology 56:540-547. doi: 10.1002/ana.20225.
33. Monory K, Massa F, Egertova M, Eder M, Blaudzun H, Westenbroek R, Kelsch W, Jacob W, Marsch R, Ekker M, Long J, Rubenstein JL, Goebbels S, Nave KA, During M, Klugmann M, Wolfel B, Dodt HU, Zieglgansberger W, Wotjak CT, Mackie K, Elphick MR, Marsicano G, Lutz B. 2006. The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51:455-466. doi: 10.1016/j.neuron.2006.07.006.
34. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007. A global double-fluorescent Cre reporter mouse. Genesis 45:593-605. doi: 10.1002/dvg.20335.
35. Nery FC, Armata IA, Farley JE, Cho JA, Yaqub U, Chen P, da Hora CC, Wang Q, Tagaya M, Klein C, Tannous B, Caldwell KA, Caldwell GA, Lencer WI, Ye Y, Breakefield XO. 2011. TorsinA participates in endoplasmic reticulumassociated degradation. Nature Communications 2:393. doi: 10.1038/ncomms1383.
36. Ozelius LJ, Hewett JW, Page CE, Bressman SB, Kramer PL, Shalish C, de Leon D, Brin MF, Raymond D, Corey DP, Fahn S, Risch NJ, Buckler AJ, Gusella JF, Breakefield XO. 1997. The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nature Genetics 17:40-48. doi: 10.1038/ng0997-40.
37. Pappas SS, Leventhal DK, Albin RL, Dauer WT. 2014. Mouse models of neurodevelopmental disease of the basal ganglia and associated circuits. Current Topics in Developmental Biology 109:97-169. doi: 10.1016/B978-0-12-397920-9.00001-9.
38. Paudel R, Hardy J, Revesz T, Holton JL, Houlden H. 2012. Review: genetics and neuropathology of primary pure dystonia. Neuropathology and Applied Neurobiology 38:520-534. doi: 10.1111/j.1365-2990.2012.01298.x.
39. Phelps PE, Brady DR, Vaughn JE. 1989. The generation and differentiation of cholinergic neurons in rat caudateputamen. Brain Research. Developmental Brain Research 46:47-60. doi: 10.1016/0165-3806(89)90142-9.
40. Pisani A, Martella G, Tscherter A, Bonsi P, Sharma N, Bernardi G, Standaert DG. 2006. Altered responses to dopaminergic D2 receptor activation and N-type calcium currents in striatal cholinergic interneurons in a mouse model of DYT1 dystonia. Neurobiology of Disease 24:318-325. doi: 10.1016/j.nbd.2006.07.006.
41. Quartarone A, Pisani A. 2011. Abnormal plasticity in dystonia: Disruption of synaptic homeostasis. Neurobiology of Disease 42:162-170. doi: 10.1016/j.nbd.2010.12.011.
42. Ramdhani RA, Simonyan K. 2013. Primary dystonia: conceptualizing the disorder through a structural brain imaging lens. Tremor and other hyperkinetic movements 3:.
43. Sanchez-Ortiz E, Yui D, Song D, Li Y, Rubenstein JL, Reichardt LF, Parada LF. 2012. TrkA gene ablation in basal forebrain results in dysfunction of the cholinergic circuitry. The Journal of Neuroscience 32:4065-4079. doi: 10. 1523/JNEUROSCI.6314-11.2012.
44. Santos M, Silva-Fernandes A, Oliveira P, Sousa N, Maciel P. 2007. Evidence for abnormal early development in a mouse model of Rett syndrome. Genes, Brain, and Behavior 6:277-286. doi: 10.1111/j.1601-183X.2006.00258.x.
45. Sciamanna G, Hollis R, Ball C, Martella G, Tassone A, Marshall A, Parsons D, Li X, Yokoi F, Zhang L, Li Y, Pisani A, Standaert DG. 2012a. Cholinergic dysregulation produced by selective inactivation of the dystonia-associated protein torsinA. Neurobiology of Disease 47:416-427. doi: 10.1016/j.nbd.2012.04.015.
46. Sciamanna G, Tassone A, Mandolesi G, Puglisi F, Ponterio G, Martella G, Madeo G, Bernardi G, Standaert DG, Bonsi P, Pisani A. 2012b. Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. The Journal of Neuroscience 32:11991-12004. doi: 10.1523/JNEUROSCI. 0041-12.2012.
47. Sciamanna G, Tassone A, Martella G, Mandolesi G, Puglisi F, Cuomo D, Madeo G, Ponterio G, Standaert DG, Bonsi P, Pisani A. 2011. Developmental profile of the aberrant dopamine D2 receptor response in striatal cholinergic interneurons in DYT1 dystonia. PLOS ONE 6:e24261. doi: 10.1371/journal.pone.0024261.
48. Sharma N, Baxter MG, Petravicz J, Bragg DC, Schienda A, Standaert DG, Breakefield XO. 2005. Impaired motor learning in mice expressing torsinA with the DYT1 dystonia mutation. The Journal of Neuroscience 25: 5351-5355. doi: 10.1523/JNEUROSCI.0855-05.2005.
49. Sobreviela T, Clary DO, Reichardt LF, Brandabur MM, Kordower JH, Mufson EJ. 1994. TrkA-immunoreactive profiles in the central nervous system: colocalization with neurons containing p75 nerve growth factor receptor, choline acetyltransferase, and serotonin. The Journal of Comparative Neurology 350:587-611. doi: 10.1002/cne.903500407.
50. Song CH, Bernhard D, Bolarinwa C, Hess EJ, Smith Y, Jinnah HA. 2013. Subtle microstructural changes of the striatum in a DYT1 knock-in mouse model of dystonia. Neurobiology of Disease 54:362-371. doi: 10.1016/j.nbd. 2013.01.008.
51. Song P, Mabrouk OS, Hershey ND, Kennedy RT. 2012. In vivo neurochemical monitoring using benzoyl chloride derivatization and liquid chromatography-mass spectrometry. Analytical Chemistry 84:412-419. doi: 10.1021/ ac202794q.
52. Soriano P. 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genetics 21:70-71. doi: 10.1038/5007.
53. Tanabe LM, Martin C, Dauer WT. 2012. Genetic background modulates the phenotype of a mouse model of DYT1 dystonia. PLOS ONE 7:e32245. doi: 10.1371/journal.pone.0032245.
54. Tepper JM, Sharpe NA, Koos TZ, Trent F. 1998. Postnatal development of the rat neostriatum: electrophysiological, light-and electron-microscopic studies. Developmental Neuroscience 20:125-145. doi: 10. 1159/000017308.
55. 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. Proceedings of the National Academy of Sciences of USA 101:15650-15655. doi: 10.1073/pnas.0308088101.
56. Vidailhet M, Jutras MF, Grabli D, Roze E. 2013. Deep brain stimulation for dystonia. Journal of Neurology, Neurosurgery, and Psychiatry 84:1029-1042. doi: 10.1136/jnnp-2011-301714.
57. Worman HJ, Gundersen GG. 2006. Here come the SUNs: a nucleocytoskeletal missing link. Trends in Cell Biology 16:67-69. doi: 10.1016/j.tcb.2005.12.006.
58. Xu M, Kobets A, Du JC, Lennington J, Li L, Banasr M, Duman RS, Vaccarino FM, DiLeone RJ, Pittenger C. 2015. Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome. Proceedings of the National Academy of Sciences of USA 112:893-898. doi: 10.1073/pnas. 1419533112.
59. Yokoi F, Dang MT, Li J, Standaert DG, Li Y. 2011. Motor deficits and decreased striatal dopamine receptor 2 binding activity in the striatum-specific Dyt1 conditional knockout mice. PLOS ONE 6:e24539. doi: 10.1371/ journal.pone.0024539.
60. Yokoi F, Dang MT, Mitsui S, Li J, Li Y. 2008. Motor deficits and hyperactivity in cerebral cortex-specific Dyt1 conditional knockout mice. Journal of Biochemistry 143:39-47. doi: 10.1093/jb/mvm191.
61. Zhang L, Yokoi F, Jin YH, DeAndrade MP, Hashimoto K, Standaert DG, Li Y. 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.