Limited regional cerebellar dysfunction induces focal dystonia in mice

Neurobiology of Disease

Volumn 49, Issue 1, 2013, Pages 200-210

  Raike, Robert S ^a   Pizoli, Carolyn E ^b,d   Weisz, Catherine ^b,e   van den Maagdenberg, Arn M J M ^c   Jinnah, H A ^a   Hess, Ellen J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebellum; Cre recombinase; Electrical stimulation; Focal dystonia; Lentivirus

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY MOVEMENT; BODY POSTURE; CELL DENSITY; CELLULAR DISTRIBUTION; CEREBELLUM DISEASE; DISEASE SEVERITY; ELECTROSTIMULATION; FOCAL DYSTONIA; GENETIC MANIPULATION; HISTOPATHOLOGY; LIMB MOVEMENT; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; AGING; ANIMAL; C3H MOUSE; C57BL MOUSE; CEREBELLUM; COMPLICATION; DYSTONIC DISORDERS; FEMALE; GENETICS; LIMB; MALE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SEVERITY OF ILLNESS INDEX; TRANSGENIC MOUSE; WALKING;

CALBINDIN; CALCIUM CHANNEL N TYPE; MESSENGER RNA; VOLTAGE-DEPENDENT CALCIUM CHANNEL (P-Q TYPE);

AGING; ANIMALS; CALBINDINS; CALCIUM CHANNELS, N-TYPE; CEREBELLAR DISEASES; CEREBELLUM; DYSTONIC DISORDERS; EXTREMITIES; FEMALE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; POSTURE; PURKINJE CELLS; RNA, MESSENGER; SEVERITY OF ILLNESS INDEX; WALKING;

EID: 84866652556     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2012.07.019     Document Type: Article

References (54)

1. Apps R., Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat. Rev. Neurosci. 2005, 6:297-311.
2. Argyelan M., Carbon M., Niethammer M., Ulug A.M., Voss H.U., Bressman S.B., Dhawan V., Eidelberg D. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J. Neurosci. 2009, 29:9740-9747.
3. Arpa J., Cuesta A., Cruz-Martinez A., Santiago S., Sarria J., Palau F. Clinical features and genetic analysis of a Spanish family with spinocerebellar ataxia 6. Acta Neurol. Scand. 1999, 99:43-47.
4. Bara-Jimenez W., Catalan M.J., Hallett M., Gerloff C. Abnormal somatosensory homunculus in dystonia of the hand. Ann. Neurol. 1998, 44:828-831.
5. Bressman S.B., Raymond D., Fuchs T., Heiman G.A., Ozelius L.J., Saunders-Pullman R. Mutations in THAP1 (DYT6) in early-onset dystonia: a genetic screening study. Lancet Neurol. 2009, 8:441-446.
6. Brown L.L., Lorden J.F. Regional cerebral glucose utilization reveals widespread abnormalities in the motor system of the rat mutant dystonic. J. Neurosci. 1989, 9:4033-4041.
7. Calderon D.P., Fremont R., Kraenzlin F., Khodakhah K. The neural substrates of rapid-onset Dystonia-Parkinsonism. Nat. Neurosci. 2011, 14:357-365.
8. Camargos S., Scholz S., Simon-Sanchez J., Paisan-Ruiz C., Lewis P., Hernandez D., Ding J., Gibbs J.R., Cookson M.R., Bras J., Guerreiro R., Oliveira C.R., Lees A., Hardy J., Cardoso F., Singleton A.B. DYT16, a novel young-onset dystonia-parkinsonism disorder: identification of a segregating mutation in the stress-response protein PRKRA. Lancet Neurol. 2008, 7:207-215.
9. Campbell D.B., Hess E.J. Cerebellar circuitry is activated during convulsive episodes in the tottering (tg/tg) mutant mouse. Neuroscience 1998, 85:773-783.
10. Campbell D.B., North J.B., Hess E.J. Tottering mouse motor dysfunction is abolished on the Purkinje cell degeneration (pcd) mutant background. Exp. Neurol. 1999, 160:268-278.
11. Ceballos-Baumann A.O., Passingham R.E., Marsden C.D., Brooks D.J. Motor reorganization in acquired hemidystonia. Ann. Neurol. 1995, 37:746-757.
12. Cicirata F., Angaut P., Serapide M.F., Panto M.R., Nicotra G. Multiple representation in the nucleus lateralis of the cerebellum: an electrophysiologic study in the rat. Exp. Brain Res. 1992, 89:352-362.
13. Cuenca-Leon E., Banchs I., Serra S.A., Latorre P., Fernandez-Castillo N., Corominas R., Valverde M.A., Volpini V., Fernandez-Fernandez J.M., Macaya A., Cormand B. Late-onset episodic ataxia type 2 associated with a novel loss-of-function mutation in the CACNA1A gene. J. Neurol. Sci. 2009, 280:10-14.
14. Defazio G., Abbruzzese G., Livrea P., Berardelli A. Epidemiology of primary dystonia. Lancet Neurol. 2004, 3:673-678.
15. Delmaire C., Krainik A., Tezenas du Montcel S., Gerardin E., Meunier S., Mangin J.F., Sangla S., Garnero L., Vidailhet M., Lehericy S. Disorganized somatotopy in the putamen of patients with focal hand dystonia. Neurology 2005, 64:1391-1396.
16. Devanagondi R., Egami K., LeDoux M.S., Hess E.J., Jinnah H.A. Neuroanatomical substrates for paroxysmal dyskinesia in lethargic mice. Neurobiol. Dis. 2007, 27:249-257.
17. Eidelberg D., Moeller J.R., Antonini A., Kazumata K., Nakamura T., Dhawan V., Spetsieris P., deLeon D., Bressman S.B., Fahn S. Functional brain networks in DYT1 dystonia. Ann. Neurol. 1998, 44:303-312.
18. Fan X., Hughes K.E., Jinnah H.A., Hess E.J. Selective and sustained AMPA receptor activation in cerebellum induces dystonia in mice. J. Pharmacol. Exp. Ther. 2012, 340:733-741.
19. Feddersen R.M., Ehlenfeldt M., Yunis W.S., Clark H.B., Orr H.T. Disrupted cerebellar cortical development and progressive degeneration of Purkinje cells in SV40 T antigen transgenic mice. Neuron 1992, 9:955-966.
20. Fletcher C.F., Lutz C.M., O'Sullivan T.N., Shaughnessy J.D., Hawkes R., Frankel W.N., Copeland N.G., Jenkins N.A. Absence epilepsy in tottering mutant mice is associated with calcium channel defects. Cell 1996, 87:607-617.
21. Fureman B.E., Jinnah H.A., Hess E.J. Triggers of paroxysmal dyskinesia in the calcium channel mouse mutant tottering. Pharmacol. Biochem. Behav. 2002, 73:631-637.
22. Galardi G., Perani D., Grassi F., Bressi S., Amadio S., Antoni M., Comi G.C., Canal N., Fazio F. Basal ganglia and thalamo-cortical hypermetabolism in patients with spasmodic torticollis. Acta Neurol. Scand. 1996, 94:172-176.
23. Giffin N.J., Benton S., Goadsby P.J. Benign paroxysmal torticollis of infancy: four new cases and linkage to CACNA1A mutation. Dev. Med. Child Neurol. 2002, 44:490-493.
24. Hadj-Sahraoui N., Frederic F., Zanjani H., Herrup K., Delhaye-Bouchaud N., Mariani J. Purkinje cell loss in heterozygous staggerer mutant mice during aging. Brain Res. Dev. Brain Res. 1997, 98:1-8.
25. Heckroth J.A., Goldowitz D., Eisenman L.M. Purkinje cell reduction in the reeler mutant mouse: a quantitative immunohistochemical study. J. Comp. Neurol. 1989, 279:546-555.
26. Hutchinson M., Nakamura T., Moeller J.R., Antonini A., Belakhlef A., Dhawan V., Eidelberg D. The metabolic topography of essential blepharospasm. Neurology 2000, 55:673-677.
27. Jen J.C., Graves T.D., Hess E.J., Hanna M.G., Griggs R.C., Baloh R.W. Primary episodic ataxias: diagnosis, pathogenesis and treatment. Brain 2007, 130:2484-2493.
28. Kamm C. Early onset torsion dystonia (Oppenheim's dystonia). Orphanet J. Rare Dis. 2006, 1:48.
29. Kluge A., Kettner B., Zschenderlein R., Sandrock D., Munz D.L., Hesse S., Meierkord H. Changes in perfusion pattern using ECD-SPECT indicate frontal lobe and cerebellar involvement in exercise-induced paroxysmal dystonia. Mov. Disord. 1998, 13:125-134.
30. LeDoux M.S., Lorden J.F., Ervin J. Cerebellectomy eliminates the motor syndrome of the genetically dystonic rat. Exp. Neurol. 1993, 120:302-310.
31. Logan K., Robertson L.T. Somatosensory representation of the cerebellar climbing fiber system in the rat. Brain Res. 1986, 372:290-300.
32. Maguschak K.A., Ressler K.J. Beta-catenin is required for memory consolidation. Nat. Neurosci. 2008, 11:1319-1326.
33. Nemeth A.H. The genetics of primary dystonias and related disorders. Brain 2002, 125:695-721.
34. Neychev V.K., Fan X., Mitev V.I., Hess E.J., Jinnah H.A. The basal ganglia and cerebellum interact in the expression of dystonic movement. Brain 2008, 131:2499-2509.
35. Neychev V.K., Gross R.E., Lehericy S., Hess E.J., Jinnah H.A. The functional neuroanatomy of dystonia. Neurobiol. Dis. 2011, 42:185-201.
36. Odergren T., Stone-Elander S., Ingvar M. Cerebral and cerebellar activation in correlation to the action-induced dystonia in writer's cramp. Mov. Disord. 1998, 13:497-508.
37. Pizoli C.E., Jinnah H.A., Billingsley M.L., Hess E.J. Abnormal cerebellar signaling induces dystonia in mice. J. Neurosci. 2002, 22:7825-7833.
38. Preibisch C., Berg D., Hofmann E., Solymosi L., Naumann M. Cerebral activation patterns in patients with writer's cramp: a functional magnetic resonance imaging study. J. Neurol. 2001, 248:10-17.
39. Raike R.S., Jinnah H.A., Hess E.J. Animal models of generalized dystonia. NeuroRx 2005, 2:504-512.
40. Ranck J.B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 1975, 98:417-440.
41. Robertson L.T., Laxer K.D. Localization of cutaneously elicited climbing fiber responses in lobule V of the monkey cerebellum. Brain Behav. Evol. 1981, 18:157-168.
42. Roubertie A., Echenne B., Leydet J., Soete S., Krams B., Rivier F., Riant F., Tournier-Lasserve E. Benign paroxysmal tonic upgaze, benign paroxysmal torticollis, episodic ataxia and CACNA1A mutation in a family. J. Neurol. 2008, 255:1600-1602.
43. Scholle H.C., Jinnah H.A., Arnold D., Biedermann F.H., Faenger B., Grassme R., Hess E.J., Schumann N.P. Kinematic and electromyographic tools for characterizing movement disorders in mice. Mov. Disord. 2010, 25:265-274.
44. Sethi K.D., Jankovic J. Dystonia in spinocerebellar ataxia type 6. Mov. Disord. 2002, 17:150-153.
45. Shirley T.L., Rao L.M., Hess E.J., Jinnah H.A. Paroxysmal dyskinesias in mice. Mov. Disord. 2008, 23:259-264.
46. Spacey S.D., Materek L.A., Szczygielski B.I., Bird T.D. Two novel CACNA1A gene mutations associated with episodic ataxia type 2 and interictal dystonia. Arch. Neurol. 2005, 62:314-316.
47. 2+-channels: four subtypes of a1 and b-subunits in developing and mature rat brain. Brain Res. Mol. Brain Res. 1995, 30:1-16.
48. Thickbroom G.W., Byrnes M.L., Stell R., Mastaglia F.L. Reversible reorganisation of the motor cortical representation of the hand in cervical dystonia. Mov. Disord. 2003, 18:395-402.
49. Todorov B., van de Ven R.C., Kaja S., Broos L.A., Verbeek S.J., Plomp J.J., Ferrari M.D., Frants R.R., van den Maagdenberg A.M. Conditional inactivation of the Cacna1a gene in transgenic mice. Genesis 2006, 44:589-594.
50. Todorov B., Kros L., Shyti R., Plak P., Haasdijk E.D., Raike R.S., Frants R.R., Hess E.J., Hoebeek F.E., De Zeeuw C.I., van den Maagdenberg A.M. Purkinje cell-specific ablation of Ca(V)2.1 channels is sufficient to cause cerebellar ataxia in mice. Cerebellum 2012, 11:246-258.
51. Ulug A.M., Vo A., Argyelan M., Tanabe L., Schiffer W.K., Dewey S., Dauer W.T., Eidelberg D. Cerebellothalamocortical pathway abnormalities in torsinA DYT1 knock-in mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:6638-6643.
52. Wakamori M., Yamazaki K., Matsunodaira H. Single tottering mutations responsible for the neuropathic phenotype of the P-type calcium channel. J. Biol. Chem. 1998, 52:34857-34867.
53. Zhao Y., Sharma N., LeDoux M.S. The DYT1 carrier state increases energy demand in the olivocerebellar network. Neuroscience 2011, 177:183-194.
54. Zoons E., Booij J., Nederveen A.J., Dijk J.M., Tijssen M.A. Structural, functional and molecular imaging of the brain in primary focal dystonia-a review. Neuroimage 2011, 56:1011-1020.