RNAi silencing of P/Q-type calcium channels in Purkinje neurons of adult mouse leads to episodic ataxia type 2

Neurobiology of Disease

Volumn 68, Issue , 2014, Pages 47-56

  Salvi, Julie ^a,b   Bertaso, Federica ^a   Mausset Bonnefont, Anne Laure ^c   Metz, Alexandra ^a,b   Lemmers, Céline ^a,b   Ango, Fabrice ^a   Fagni, Laurent ^a   Lory, Philippe ^a,b   Mezghrani, Alexandre ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b Laboratory of Excellence in Ion Channel Science and Therapeutics   (France)

^c INSERM   (France)

Author keywords

Acetazolamide; Ataxia; Cerebellum; Mouse; P Q type calcium channel; Purkinje neuron; RNA interference

Indexed keywords

ACETAZOLAMIDE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM CHANNEL N TYPE; GREEN FLUORESCENT PROTEIN; SMALL INTERFERING RNA; VOLTAGE-DEPENDENT CALCIUM CHANNEL (P-Q TYPE);

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; ATAXIC GAIT; BALANCE DISORDER; BETA ADRENERGIC STIMULATION; CEREBELLUM; CONTROLLED STUDY; EMBRYO; EPISODIC ATAXIA TYPE 2; EXERCISE; GENE SILENCING; HUMAN; HUMAN CELL; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; RNA INTERFERENCE; STRESS INDUCED ATAXIA; ANIMAL; BODY EQUILIBRIUM; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETIC TRANSDUCTION; GENETICS; HEK293 CELL LINE; MALE; MEMBRANE POTENTIAL; METABOLISM; MOVEMENT (PHYSIOLOGY); NYSTAGMUS, PATHOLOGIC; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ATAXIA; CALCIUM CHANNELS, N-TYPE; CEREBELLUM; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOVEMENT; NYSTAGMUS, PATHOLOGIC; POSTURAL BALANCE; PURKINJE CELLS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRANSDUCTION, GENETIC;

EID: 84899930112     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.04.005     Document Type: Article

References (54)

1. Alvina K., Khodakhah K. KCa channels as therapeutic targets in episodic ataxia type-2. J. Neurosci. 2010, 30:7249-7257.
2. Ango F., Prezeau L., Muller T., Tu J.C., Xiao B., Worley P.F., Pin J.P., Bockaert J., Fagni L. Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer. Nature 2001, 411:962-965.
3. Baloh R.W. Episodic ataxias 1 and 2. Handb. Clin. Neurol. 2012, 103:595-602.
4. Blomer U., Naldini L., Kafri T., Trono D., Verma I.M., Gage F.H. Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. J. Virol. 1997, 71:6641-6649.
5. Bloom F.E., Hoffer B.J., Siggins G.R. Studies on norepinephrine-containing afferents to Purkinje cells of art cerebellum. I. Localization of the fibers and their synapses. Brain Res. 1971, 25:501-521.
6. Browne D.L., Gancher S.T., Nutt J.G., Brunt E.R., Smith E.A., Kramer P., Litt M. Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat. Genet. 1994, 8:136-140.
7. Cahill L., Prins B., Weber M., Mcgaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371:702-704.
8. 2+ channelopathy. Neuron 2004, 43:387-400.
9. Chen G., Gao W., Reinert K.C., Popa L.S., Hendrix C.M., Ross M.E., Ebner T.J. Involvement of kv1 potassium channels in spreading acidification and depression in the cerebellar cortex. J. Neurophysiol. 2005, 94:1287-1298.
10. Cheun J.E., Yeh H.H. Modulation of GABAA receptor-activated current by norepinephrine in cerebellar Purkinje cells. Neuroscience 1992, 51:951-960.
11. Cheun J.E., Yeh H.H. Noradrenergic potentiation of cerebellar Purkinje cell responses to GABA: cyclic AMP as intracellular intermediary. Neuroscience 1996, 74:835-844.
12. Deumens R., Jaken R.J., Marcus M.A., Joosten E.A. The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J. Neurosci. Methods 2007, 164:120-130.
13. Ferdinandusse S., Zomer A.W., Komen J.C., van den Brink C.E., Thanos M., Hamers F.P., Wanders R.J., van der Saag P.T., Poll-The B.T., Brites P. Ataxia with loss of Purkinje cells in a mouse model for Refsum disease. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:17712-17717.
14. Fletcher C.F., Tottene A., Lennon V.A., Wilson S.M., Dubel S.J., Paylor R., Hosford D.A., Tessarollo L., Mcenery M.W., Pietrobon D., Copeland N.G., Jenkins N.A. Dystonia and cerebellar atrophy in Cacna1a null mice lacking P/Q calcium channel activity. FASEB J. 2001, 15:1288-1290.
15. Galliano E., Gao Z., Schonewille M., Todorov B., Simons E., Pop A.S., D'angelo E., van den Maagdenberg A.M., Hoebeek F.E., De Zeeuw C.I. Silencing the majority of cerebellar granule cells uncovers their essential role in motor learning and consolidation. Cell Rep. 2013, 3:1239-1251.
16. +-channel activators in Cacna1a(S218L) mutant mice. J. Neurosci. 2012, 32:15533-15546.
17. Guida S., Trettel F., Pagnutti S., Mantuano E., Tottene A., Veneziano L., Fellin T., Spadaro M., Stauderman K., Williams M., Volsen S., Ophoff R., Frants R., Jodice C., Frontali M., Pietrobon D. 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.
18. 2+ channel in Purkinje cell mediates synaptic competition and elimination in developing cerebellum. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:9987-9992.
19. Hausser M., Clark B.A. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 1997, 19:665-678.
20. Herrup K., Wilczynski S.L. Cerebellar cell degeneration in the leaner mutant mouse. Neuroscience 1982, 7:2185-2196.
21. Herson P.S., Virk M., Rustay N.R., Bond C.T., Crabbe J.C., Adelman J.P., Maylie J. A mouse model of episodic ataxia type-1. Nat. Neurosci. 2003, 6:378-383.
22. Hess E.J., Wilson M.C. Tottering and leaner mutations perturb transient developmental expression of tyrosine hydroxylase in embryologically distinct Purkinje cells. Neuron 1991, 6:123-132.
23. Hoebeek F.E., Stahl J.S., van Alphen A.M., Schonewille M., Luo C., Rutteman M., van den Maagdenberg A.M., Molenaar P.C., Goossens H.H., Frens M.A., De Zeeuw C.I. Increased noise level of purkinje cell activities minimizes impact of their modulation during sensorimotor control. Neuron 2005, 45:953-965.
24. Jen J., Yue Q., Nelson S.F., Yu H., Litt M., Nutt J., Baloh R.W. A novel nonsense mutation in CACNA1A causes episodic ataxia and hemiplegia. Neurology 1999, 53:34-37.
25. Jen J., Kim G.W., Baloh R.W. Clinical spectrum of episodic ataxia type 2. Neurology 2004, 62:17-22.
26. 2+ channel mutations associated with episodic ataxia type 2. Am. J. Physiol. Cell Physiol. 2006, 290:C1209-C1220.
27. Jouvenceau A., Eunson L.H., Spauschus A., Ramesh V., Zuberi S.M., Kullmann D.M., Hanna M.G. Human epilepsy associated with dysfunction of the brain P/Q-type calcium channel. Lancet 2001, 358:801-807.
28. Kondo S., Marty A. Differential effects of noradrenaline on evoked, spontaneous and miniature IPSCs in rat cerebellar stellate cells. J. Physiol. 1998, 509(Pt 1):233-243.
29. Levitt P., Noebels J.L. Mutant mouse tottering: selective increase of locus ceruleus axons in a defined single-locus mutation. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:4630-4634.
30. Lory P., Mezghrani A. Calcium channelopathies in inherited neurological disorders: relevance to drug screening for acquired channel disorders. IDrugs 2010, 13:467-471.
31. Mark M.D., Maejima T., Kuckelsberg D., Yoo J.W., Hyde R.A., Shah V., Gutierrez D., Moreno R.L., Kruse W., Noebels J.L., Herlitze S. Delayed postnatal loss of P/Q-type calcium channels recapitulates the absence epilepsy, dyskinesia, and ataxia phenotypes of genomic Cacna1a mutations. J. Neurosci. 2011, 31:4311-4326.
32. Mezghrani A., Monteil A., Watschinger K., Sinnegger-Brauns M.J., Barrere C., Bourinet E., Nargeot J., Striessnig J., Lory P. A destructive interaction mechanism accounts for dominant-negative effects of misfolded mutants of voltage-gated calcium channels. J. Neurosci. 2008, 28:4501-4511.
33. v2.1 in cerebellar Purkinje cells regulates competitive excitatory synaptic wiring, cell survival, and cerebellar biochemical compartmentalization. J. Neurosci. 2012, 32:1311-1328.
34. Naldini L., Blomer U., Gage F.H., Trono D., Verma I.M. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11382-11388.
35. Olson L., Fuxe K. On the projections from the locus coeruleus noradrenaline neurons: the cerebellar innervation. Brain Res. 1971, 28:165-171.
36. 2+ channel gene CACNL1A4. Cell 1996, 87:543-552.
37. 2+ channel mutant mice. Cerebellum 2012, 11:666-680.
38. Page K.M., Heblich F., Davies A., Butcher A.J., Leroy J., Bertaso F., Pratt W.S., Dolphin A.C. Dominant-negative calcium channel suppression by truncated constructs involves a kinase implicated in the unfolded protein response. J. Neurosci. 2004, 24:5400-5409.
39. Page K.M., Heblich F., Margas W., Pratt W.S., Nieto-Rostro M., Chaggar K., Sandhu K., Davies A., Dolphin A.C. N terminus is key to the dominant negative suppression of Ca(V)2 calcium channels: implications for episodic ataxia type 2. J. Biol. Chem. 2010, 285:835-844.
40. V2.1 channelopathies. Pflugers Arch. 2010, 460:375-393.
41. Raike R.S., Weisz C., Hoebeek F.E., Terzi M.C., De Zeeuw C.I., van den Maagdenberg A.M., Jinnah H.A., Hess E.J. Stress, caffeine and ethanol trigger transient neurological dysfunction through shared mechanisms in a mouse calcium channelopathy. Neurobiol. Dis. 2013, 50:151-159.
42. Rajakulendran S., Kaski D., Hanna M.G. Neuronal P/Q-type calcium channel dysfunction in inherited disorders of the CNS. Nat. Rev. Neurol. 2012, 8:86-96.
43. Raman I.M., Bean B.P. Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J. Neurosci. 1999, 19:1663-1674.
44. v2.1 calcium channels is sufficient to induce neurological disorders observed in natural occurring Cacna1a mutants in mice. Biochem. Biophys. Res. Commun. 2009, 390:1029-1033.
45. Sakurai T., Hell J.W., Woppmann A., Miljanich G.P., Catterall W.A. Immunochemical identification and differential phosphorylation of alternatively spliced forms of the alpha 1A subunit of brain calcium channels. J. Biol. Chem. 1995, 270:21234-21242.
46. Sawada K., Kalam Azad A., Sakata-Haga H., Lee N.S., Jeong Y.G., Fukui Y. Striking pattern of Purkinje cell loss in cerebellum of an ataxic mutant mouse, tottering. Acta Neurobiol. Exp. (Wars.) 2009, 69:138-145.
47. Shirley T.L., Rao L.M., Hess E.J., Jinnah H.A. Paroxysmal dyskinesias in mice. Mov. Disord. 2008, 23:259-264.
48. Siggins G.R., Hoffer B.J., Oliver A.P., Bloom F.E. Activation of a central noradrenergic projection to cerebellum. Nature 1971, 233:481-483.
49. Strupp M., Zwergal A., Brandt T. Episodic ataxia type 2. Neurotherapeutics 2007, 4:267-273.
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. Torashima T., Okoyama S., Nishizaki T., Hirai H. In vivo transduction of murine cerebellar Purkinje cells by HIV-derived lentiviral vectors. Brain Res. 2006, 1082:11-22.
52. 2+ channels. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3491-3496.
53. Walter J.T., Alvina K., Womack M.D., Chevez C., Khodakhah K. Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia. Nat. Neurosci. 2006, 9:389-397.
54. Wan J., Mamsa H., Johnston J.L., Spriggs E.L., Singer H.S., Zee D.S., Al-Bayati A.R., Baloh R.W., Jen J.C. Large genomic deletions in CACNA1A cause episodic ataxia type 2. Front. Neurol. 2011, 2:51.