A recurrent KCNQ2 pore mutation causing early onset epileptic encephalopathy has a moderate effect on M current but alters subcellular localization of Kv7 channels

Neurobiology of Disease

Volumn 80, Issue , 2015, Pages 80-92

  Abidi, Affef ^a,b   Devaux, Jérôme J ^d   Molinari, Florence ^b,e   Alcaraz, Gisèle ^a,b   Michon, François Xavier ^b,e   Sutera Sardo, Julie ^a,b,c   Becq, Hélène ^b,e   Lacoste, Caroline ^a,b,c   Altuzarra, Cécilia ^f   Afenjar, Alexandra ^h,i   Mignot, Cyril ^g,h   Doummar, Diane ⁱ   Isidor, Bertrand ^j   Guyen, Sylvie N ^k   Colin, Estelle ^k   De La Vaissière, Sabine ^l   Haye, Damien ^l   Trauffler, Adeline ^m   Badens, Catherine ^a,b,c   Prieur, Fabienne ⁿ   Lesca, Gaetan ^o   Villard, Laurent ^a,b   Milh, Mathieu ^a,b,c   Aniksztejn, Laurent ^b,e   more..

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSERM   (France)

^c TIMONE HOSPITAL   (France)

^d University of Mediterranée   (France)

^e Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^f UNIVERSITY HOSPITAL OF BESANÇON   (France)

^g PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^h SORBONNE UNIVERSITÉ   (France)

ⁱ ARMAND TROUSSEAU HOSPITAL   (France)

^j NANTES UNIVERSITY HOSPITAL   (France)

^k ANGERS UNIVERSITY HOSPITAL   (France)

^l UNIVERSITY HOSPITAL OF TOURS   (France)

^m LILLE UNIVERSITY HOSPITAL   (France)

ⁿ UNIVERSITY HOSPITAL OF SAINT ETIENNE   (France)

^o HOSPICES CIVILS DE LYON   (France)

more..

Author keywords

Early epileptic encephalopathy; Kv7 channels; M current; P.A294G mutation; P.A294V mutation; Subcellular channel expression

Indexed keywords

POTASSIUM CHANNEL KCNQ2; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT POTASSIUM M CHANNEL KV7.2; VOLTAGE DEPENDENT POTASSIUM M CHANNEL KV7.3; VOLTAGE GATED POTASSIUM CHANNEL; KCNQ2 PROTEIN, HUMAN;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ELECTROENCEPHALOGRAPHY; GENE FUNCTION; GENE LOCATION; GENE MUTATION; GENETIC SCREENING; HUMAN; HUMAN CELL; INFANT; KCNQ2 GENE; LENNOX GASTAUT SYNDROME; MOLECULAR CLONING; NONHUMAN; ONSET AGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; WESTERN BLOTTING; ANIMAL; BRAIN; CELL CULTURE; CHO CELL LINE; CRICETULUS; EPILEPSY; GENETICS; HIPPOCAMPUS; METABOLISM; MUTATION; NERVE CELL; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY;

ANIMALS; BRAIN; CELLS, CULTURED; CHO CELLS; CRICETULUS; EPILEPSY; HIPPOCAMPUS; HUMANS; KCNQ2 POTASSIUM CHANNEL; MUTATION; NEURONS; PHENOTYPE;

EID: 84952064079     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.04.017     Document Type: Article

References (42)

1. Allen N.M., Mannion M., Conroy J., Lynch S.A., Shahwan A., Lynch B., King M.D. The variable phenotypes of KCNQ-related epilepsy. Epilepsia 2014, 55:99-105.
2. Battefeld A., Tran B.T., Gavrilis J., Cooper E.C., Kole M.H. Heteromeric Kv7.2/7.3 channels differentially regulate action potential initiation and conduction in neocortical myelinated axons. J. Neurosci. 2014, 34:3719-3732.
3. Biervert C., Schroeder B.C., Kubisch C., Berkovic S.F., Proooing P., Jentsch T.J., Steinlein O.K. A potassium channel mutation in neonatal human epilepsy. Science 1998, 279:403-406.
4. Borgatti R., Zucca C., Cavallini A., Ferrario M., Panzeri C., Castaldo P., Soldovieri M.V., Baschirotto C., Bresolin N., Dalla Bernardina B., Tagalialatela M., Bassi M.T. A novel mutation in KCNQ2 associated with BFNC, drug reistant epilepsy, and menral retardation. Neurology 2004, 63:57-65.
5. Brown D.A., Passmore G.M. Neural KCNQ (Kv7) channels. Br. J. Pharmacol. 2009, 156:1185-1195.
6. Cavaretta J.P., Sherer K.R., Lee K.Y., Kim E.H., Issema R.S., Chung H.J. Polarized axonal surface expression of neuronal KCNQ potassium channels is regulated by calmodulin interaction with KCNQ2 subunit. PLoS One 2014, 9:e103655.
7. Charlier C., Singh N.A., Ryan S.G., Lewis T.B., Reus B.E., Leach R.J., Leppert R.M. A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat. Genet. 1998, 18:53-55.
8. Chung H.J., Jan Y.N., Jan L.Y. Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8870-8875.
9. + channel mutation in benign neonatal convulsions and centrotemporal spikes. Neurology 2003, 61:131-134.
10. Dalen Meurs-van der Schoor C., van Weissenbruch M., van Kempen M., Bugiani M., Aronica E., Ronner H., Vermeulen R.J. Severe neonatal epileptic encephalopathy and KCNQ2 mutation: neuropathological substrate?. Front. Pediatr. 2014, 2:136.
11. + channel. J. Neurosci. 2004, 24:1236-1244.
12. Etxeberria A., Aivar P., Rodriguez-Alfaro J.A., Alaimo A., Villace P., Gomez-Posada J.C., Areso P., Villaroel A. Calmodulin regulates the trafficking of KCNQ2 potassium channels. FASEB J. 2008, 22:1135-1143.
13. Hu H., Vervaeke K., Storm J.F. M-channels (Kv7/KCNQ channels) that regulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic region. J. Neurosci. 2007, 27:1853-1867.
14. Jentsch T.J. Neuronal KCNQ potassium channels: physiology and role in disease. Nat. Rev. Neurosci. 2000, 1:21-30.
15. Kato M., Yamagata T., Kubota M., Arai H., Yamashita S., Nakagawa T., Fujii T., Imai K., Uster T., Chitayat D., Weiss S., Kashii H., Kusano R., Matsumoto A., Nakamura K., Oyazato Y., Maeno M., Nishiyama K., Kodera H., Nakashima M., Tsurusaki Y., Miyake N., Saito K., Hayasaka K., Matsumoto N., Saitsu H. Clinical spectrum of early onset epileptic encephalopathies caused by KCNQ2 mutation. Epilepsia 2013, 54:1282-1287.
16. + channels. Mol. Pharmacol. 2009, 275:272-280.
17. Liu W., Devaux J.J. Calmodulin orchestrates the heteromeric assembly and the trafficking of KCNQ2/3 (Kv7.2/3) channels in neurons. Mol. Cell. Neurosci. 2014, 58:40-52.
18. Lonigro A., Devaux J.J. Disruption of neurofascin and gliomedin at nodes of Ranvier precedes demyelination in experimental allergic neuritis. Brain 2009, 132:260-273.
19. Magee J.C. Dendritic integration of excitatory synaptic input. Nat. Rev. Neurosci. 2000, 1:181-190.
20. Maljevic S., Lerche H. Potassium channel genes and benign familial neonatal epilepsy. Prog. Brain Res. 2014, 213:17-53.
21. Maljevic S., Wuttke T.V., Lerche H. Nervous system KV7 disorders: breakdown of a subthreshold brake. J. Physiol. 2008, 586:1791-1801.
22. Miceli F., Soldovieri M.V., Ambrosino P., Ambrosino P., Barrese V., Migliore M., Cilio M.R., Taglialatela M. Genotype-phenotype correlations in neonatal epilepsies caused by mutations in the voltage sensor of K(v)7.2 potassium channel subunits. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4386-4391.
23. Miceli F., Soldovieri M.V., Ambrosino P., De Maria M., Migliore M., Migliore R., Taglialatela M. Early-onset epeilptic encephalopathy caused by gain of function mutations in the voltage sensor of Kv7.2 and Kv7.3 potassium channel subunits. J. Neurosci. 2015, 35:3782-3793.
24. Milh M., Boutry-Kryza N., Sutera-Sardo J., Mignot C., Auvin S., Lacoste C., Villeneuve N., Roubertie A., Heron B., Carneiro M., Kaminska A., Altuzarra C., et al. Similar early characteristics but variable neurological outcome of patients with a de novo mutation of KCNQ2. Orphanet J. Rare Dis. 2013, 8:80.
25. Numis A.L., Angriman M., Sullivan J.E., Lewis A.J., Striano P., Nabbout R., Cilio M.R. KCNQ2 encephalopathy: delineation of the electroclinical phenotype and treatment response. Neurology 2014, 82:368-370.
26. Orhan G., Bock M., Schepers D., Llina E.I., Reichel S.N., Löffler H., Jezutkovic N., Wechhuysen S., Mandelstam S., Danker T., Guenther E., Scheffer I.E., de Jonghe P., Lerche H., Maljevic S. Dominant-negative effects of KCNQ2 mutations are associated with epileptic encephalopathy. Ann. Neurol. 2014, 75:382-394.
27. Pan Z., Kao T., Horvath Z., Lemos J., Sul J.Y., Cranstoun S.D., Bennett V., Scherer S.S., Cooper E.C. A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J. Neurosci. 2006, 26:2599-2613.
28. Peters H.C., Hu H., Pongs O., Storm J.F., Isbrandt D. Conditional transgenic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behavior. Nat. Neurosci. 2005, 8:51-60.
29. Rasmussen H.B., Frøkjaer-Jensen C., Jensen C.S., Jensen H.S., Jorgensen N.K., Misonou H., Trimmer J.S., Olesen S.P., Schmitt N. Requirement of subunit co-assembly and ankyrin-G for M-channel localization at the axon initial segment. J. Cell Sci. 2007, 120:953-963.
30. Safiulina V.F., Zacchi P., Taglialatela M., Yaari Y., Cherubini E. Low expression of Kv7/M channels facilitates intrinsic and network bursting in the developing rat hippocampus. J. Physiol. 2008, 586:5437-5453.
31. Shah M.M., Migliore M., Valencia I., Cooper E.C., Brown D.A. Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7869-7874.
32. Shah M.M., Migliore M., Brown D.A. Differential effects of Kv7 (M-) channels on synaptic integration in distinct subcellular compartments of rat hippocampal pyramidal neurons. J. Physiol. 2011, 589:6029-6038.
33. Singh N.A., Charlier C., Stauffer D., DuPont B.R., Leach R.J., Melis R., Ronen G.M., Bjerre I., Quattlebaum T., Murphy J.V., McHarg M.L., Gagnon D., Rosales T.O., Peiffer A., Anderson V.E., Leppert M. A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat. Genet. 1998, 18:25-29.
34. Soh H., Pant R., LoTurco J.J., Tzingounis A.V. Conditional deletions of epilepsy-associated KCNQ2 and KCNQ3 channels from cerebral cortex cause differential effects on neuronal excitability. J. Neurosci. 2014, 34:5311-5321.
35. Soldovieri M.V., Castaldo P., Iodice L., Miceli F., Barrese V., Bellini G., Miraglia del Giudice E., Pascotto A., Annunziato L., Taglialatela M. Decreased subunit stability as a novel mechanism for potassium current impairment by a KCNQ2 C terminus mutation causing benign familial neonatal convulsions. J. Biol. Chem. 2006, 281:418-428.
36. Soldovieri M.V., Boutry-Kryza N., Milh M., Doummar D., Heron B., Bourel E., Ambrosino P., Miceli F., De Maria M., Dorison N., Auvin S., Echenne B., Oertel J., Riquet A., Lambert L., Gerard M., Roubergue A., Calender A., Mignot C., Taglialatela M., Lesca G. Novel KCNQ2 and KCNQ3 mutations in a large cohort of families with benign neonatal epilepsy: first evidence for an altered channel regulation by syntaxin 1A. Hum. Mutat. 2014, 35:356-367.
37. Steinlein O.K., Conrad C., Weidner B. Benign familial neonatal convulsions: always beningn?. Epilepsy Res. 2007, 73:245-249.
38. Wang H.S., Pan Z., Shi W., Brown B.S., Wymore R.S., Cohne I.S., Dixon J.E., McKinnon D. KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 1998, 282:1890-1893.
39. Weckhuysen S., Mandelstam S., Suls A., Audenaert D., Deconinck T., Claes L.R., Deprez L., Smets K., Hristova D., Roelens F., Lagae L., Yendle S., Stanley T., Heron S.E., Mulley J.C., Berkovic S.F., Scheffer I.E., De Jonghe P. KCNQ2 encephalopathy: emerging phenotype of a neonatal epileptic encephalopathy. Ann. Neurol. 2012, 71:15-25.
40. Wen H., Levitan I.B. Calmodulin is an auxiliary subunit of KCNQ2/3 potassium channels. J. Neurosci. 2002, 22:7991-8001.
41. Xiong Q., Sun H., Zhang Y., Nan F., Li M. Combinatorial augmentation of voltage-gated KCNQ potassium channels by chemical openers. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3128-3133.
42. Yue C., Yaari Y. Axo-somatic and apical dendritic Kv7/M channels differentially regulate the intrinsic excitability of adult rat CA1 pyramidal cells. J. Neurophysiol. 2006, 95:3480-3495.