Human Slack Potassium Channel Mutations Increase Positive Cooperativity between Individual Channels

Cell Reports

Volumn 9, Issue 5, 2014, Pages 1661-1672

  Kim, Grace E ^a   Kronengold, Jack ^a   Barcia, Giulia ^b   Quraishi, Imran H ^a   Martin, Hilary C ^c   Blair, Edward ^d   Taylor, Jenny C ^c   Dulac, Olivier ^b   Colleaux, Laurence ^e   Nabbout, Rima ^b   Kaczmarek, Leonard K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^e IMAGINE INSTITUTE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SODIUM ACTIVATED POTASSIUM CHANNEL SLACK; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; KCNT1 PROTEIN, HUMAN; NERVE PROTEIN; POTASSIUM CHANNEL;

ADULT; AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; AUTOSOMAL DOMINANT NOCTURNAL FRONTAL LOBE EPILEPSY; CHANNEL GATING; CLINICAL ARTICLE; CONTROLLED STUDY; EPILEPSY; GENE MUTATION; HUMAN; KCNT1 GENE; MIGRATING MALIGNANT PARTIAL SEIZURES IN INFANCY; MOLECULAR INTERACTION; MUTANT; NONHUMAN; OHTAHARA SYNDROME; OOCYTE; POINT MUTATION; POTASSIUM CONDUCTANCE; WILD TYPE; XENOPUS; YOUNG ADULT; ANIMAL; CELL CULTURE; GENE EXPRESSION; GENETICS; INFANT; METABOLISM; MISSENSE MUTATION; NEWBORN; PRESCHOOL CHILD; RAT; XENOPUS LAEVIS;

ANIMALS; CELLS, CULTURED; CHILD, PRESCHOOL; EPILEPSY; GENE EXPRESSION; HUMANS; INFANT; INFANT, NEWBORN; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; POINT MUTATION; POTASSIUM CHANNELS; RATS; XENOPUS LAEVIS;

EID: 84915767652     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.11.015     Document Type: Article

References (44)

1. Allen A.S., Berkovic S.F., Cossette P., Delanty N., Dlugos D., Eichler E.E., Epstein M.P., Glauser T., Goldstein D.B., Han Y., et al. De novo mutations in epileptic encephalopathies. Nature 2013, 501:217-221. Epi4K Consortium, Epilepsy Phenome/Genome ProjectEpilepsy Phenome/Genome Project.
2. Barcia G., Fleming M.R., Deligniere A., Gazula V.R., Brown M.R., Langouet M., Chen H., Kronengold J., Abhyankar A., Cilio R., et al. De novo gain-of-function KCNT1 channel mutations cause malignant migrating partial seizures of infancy. Nat. Genet. 2012, 44:1255-1259.
3. Bhattacharjee A., Kaczmarek L.K. For K+ channels, Na+ is the new Ca2+. Trends Neurosci. 2005, 28:422-428.
4. Bhattacharjee A., Gan L., Kaczmarek L.K. Localization of the Slack potassium channel in the rat central nervous system. J.Comp. Neurol. 2002, 454:241-254.
5. Bröer S. Xenopus laevis Oocytes. Methods Mol. Biol. 2003, 227:245-258.
6. Brown M.R., Kaczmarek L.K. Potassium channel modulation and auditory processing. Hear. Res. 2011, 279:32-42.
7. Brown M.R., Kronengold J., Gazula V.R., Spilianakis C.G., Flavell R.A., von Hehn C.A., Bhattacharjee A., Kaczmarek L.K. Amino-termini isoforms of the Slack K+ channel, regulated by alternative promoters, differentially modulate rhythmic firing and adaptation. J.Physiol. 2008, 586:5161-5179.
8. Brown M.R., Kronengold J., Gazula V.R., Chen Y., Strumbos J.G., Sigworth F.J., Navaratnam D., Kaczmarek L.K. Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat. Neurosci. 2010, 13:819-821.
9. Budelli G., Hage T.A., Wei A., Rojas P., Jong Y.J., O'Malley K., Salkoff L. Na+-activated K+ channels express a large delayed outward current in neurons during normal physiology. Nat. Neurosci. 2009, 12:745-750.
10. Chen H., Kronengold J., Yan Y., Gazula V.R., Brown M.R., Ma L., Ferreira G., Yang Y., Bhattacharjee A., Sigworth F.J., et al. The N-terminal domain of Slack determines the formation and trafficking of Slick/Slack heteromeric sodium-activated potassium channels. J.Neurosci. 2009, 29:5654-5665.
11. Coppola G., Plouin P., Chiron C., Robain O., Dulac O. Migrating partial seizures in infancy: a malignant disorder with developmental arrest. Epilepsia 1995, 36:1017-1024.
12. Dekker J.P., Yellen G. Cooperative gating between single HCN pacemaker channels. J.Gen. Physiol. 2006, 128:561-567.
13. Deng P.Y., Rotman Z., Blundon J.A., Cho Y., Cui J., Cavalli V., Zakharenko S.S., Klyachko V.A. FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron 2013, 77:696-711.
14. Ding S., Sachs F. Evidence for non-independent gating of P2X2 receptors expressed in Xenopus oocytes. BMC Neurosci. 2002, 3:17.
15. Escayg A., MacDonald B.T., Meisler M.H., Baulac S., Huberfeld G., An-Gourfinkel I., Brice A., LeGuern E., Moulard B., Chaigne D., et al. Mutations of SCN1A, encoding a neuronal sodium channel, in two families with GEFS+2. Nat. Genet. 2000, 24:343-345.
16. Ferron L., Nieto-Rostro M., Cassidy J.S., Dolphin A.C. Fragile X mental retardation protein controls synaptic vesicle exocytosis by modulating N-type calcium channel density. Nat Commun 2014, 5:3628.
17. Heron S.E., Smith K.R., Bahlo M., Nobili L., Kahana E., Licchetta L., Oliver K.L., Mazarib A., Afawi Z., Korczyn A., et al. Missense mutations in the sodium-gated potassium channel gene KCNT1 cause severe autosomal dominant nocturnal frontal lobe epilepsy. Nat. Genet. 2012, 44:1188-1190.
18. Horio Y., Hibino H., Inanobe A., Yamada M., Ishii M., Tada Y., Satoh E., Hata Y., Takai Y., Kurachi Y. Clustering and enhanced activity of an inwardly rectifying potassium channel, Kir4.1, by an anchoring protein, PSD-95/SAP90. J.Biol. Chem. 1997, 272:12885-12888.
19. Huang F., Wang X., Ostertag E.M., Nuwal T., Huang B., Jan Y.N., Basbaum A.I., Jan L.Y. TMEM16C facilitates Na(+)-activated K+ currents in rat sensory neurons and regulates pain processing. Nat. Neurosci. 2013, 16:1284-1290.
20. Ishii A., Shioda M., Okumura A., Kidokoro H., Sakauchi M., Shimada S., Shimizu T., Osawa M., Hirose S., Yamamoto T. A recurrent KCNT1 mutation in two sporadic cases with malignant migrating partial seizures in infancy. Gene 2013, 531:467-471.
21. Joiner W.J., Tang M.D., Wang L.Y., Dworetzky S.I., Boissard C.G., Gan L., Gribkoff V.K., Kaczmarek L.K. Formation of intermediate-conductance calcium-activated potassium channels by interaction of Slack and Slo subunits. Nat. Neurosci. 1998, 1:462-469.
22. Kaczmarek L.K. Slack, Slick and sodium-activated potassium channels. ISRN Neurosci 2013, 2013:354262.
23. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
24. Krouse M.E., Wine J.J. Evidence that CFTR channels can regulate the open duration of other CFTR channels: cooperativity. J.Membr. Biol. 2001, 182:223-232.
25. Laver D.R., O'Neill E.R., Lamb G.D. Luminal Ca2+-regulated Mg2+ inhibition of skeletal RyRs reconstituted as isolated channels or coupled clusters. J.Gen. Physiol. 2004, 124:741-758.
26. Lossin C. A catalog of SCN1A variants. Brain Dev. 2009, 31:114-130.
27. Martin H.C., Kim G.E., Pagnamenta A.T., Murakami Y., Carvill G.L., Meyer E., Copley R.R., Rimmer A., Barcia G., Fleming M.R., et al. Clinical whole-genome sequencing in severe early-onset epilepsy reveals new genes and improves molecular diagnosis. Hum. Mol. Genet. 2014, 23:3200-3211. WGS500 Consortium.
28. Marx S.O., Ondrias K., Marks A.R. Coupled gating between individual skeletal muscle Ca2+ release channels (ryanodine receptors). Science 1998, 281:818-821.
29. Marx S.O., Gaburjakova J., Gaburjakova M., Henrikson C., Ondrias K., Marks A.R. Coupled gating between cardiac calcium release channels (ryanodine receptors). Circ. Res. 2001, 88:1151-1158.
30. McTague A., Appleton R., Avula S., Cross J.H., King M.D., Jacques T.S., Bhate S., Cronin A., Curran A., Desurkar A., et al. Migrating partial seizures of infancy: expansion of the electroclinical, radiological and pathological disease spectrum. Brain 2013, 136:1578-1591.
31. Milligan C.J., Li M., Gazina E.V., Heron S.E., Nair U., Trager C., Reid C.A., Venkat A., Younkin D.P., Dlugos D.J., et al. KCNT1 gain of function in 2 epilepsy phenotypes is reversed by quinidine. Ann. Neurol. 2014, 75:581-590.
32. Molina M.L., Barrera F.N., Fernández A.M., Poveda J.A., Renart M.L., Encinar J.A., Riquelme G., González-Ros J.M. Clustering and coupled gating modulate the activity in KcsA, a potassium channel model. J.Biol. Chem. 2006, 281:18837-18848.
33. Naundorf B., Wolf F., Volgushev M. Unique features of action potential initiation in cortical neurons. Nature 2006, 440:1060-1063.
34. Navedo M.F., Cheng E.P., Yuan C., Votaw S., Molkentin J.D., Scott J.D., Santana L.F. Increased coupled gating of L-type Ca2+ channels during hypertension and Timothy syndrome. Circ. Res. 2010, 106:748-756.
35. Oliva M., Berkovic S.F., Petrou S. Sodium channels and the neurobiology of epilepsy. Epilepsia 2012, 53:1849-1859.
36. Ryan D.P., Ptácek L.J. Episodic neurological channelopathies. Neuron 2010, 68:282-292.
37. Scheffer I.E., Bhatia K.P., Lopes-Cendes I., Fish D.R., Marsden C.D., Andermann E., Andermann F., Desbiens R., Keene D., Cendes F., et al. Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical disorder. Brain 1995, 118:61-73.
38. Vacher H., Trimmer J.S. Trafficking mechanisms underlying neuronal voltage-gated ion channel localization at the axon initial segment. Epilepsia 2012, 53(Suppl 9):21-31.
39. Vaithianathan T., Manivannan K., Kleene R., Bahr B.A., Dey M.P., Dityatev A., Suppiramaniam V. Single channel recordings from synaptosomal AMPA receptors. Cell Biochem. Biophys. 2005, 42:75-85.
40. Vanderver A., Simons C., Schmidt J.L., Pearl P.L., Bloom M., Lavenstein B., Miller D., Grimmond S.M., Taft R.J. Identification of a novel de novo p.Phe932Ile KCNT1 mutation in a patient with leukoencephalopathy and severe epilepsy. Pediatr. Neurol. 2014, 50:112-114.
41. Wallén P., Robertson B., Cangiano L., Löw P., Bhattacharjee A., Kaczmarek L.K., Grillner S. Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J.Physiol. 2007, 585:75-90.
42. Yuan A., Santi C.M., Wei A., Wang Z.W., Pollak K., Nonet M., Kaczmarek L., Crowder C.M., Salkoff L. The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 2003, 37:765-773.
43. Yuan P., Leonetti M.D., Pico A.R., Hsiung Y., MacKinnon R. Structure of the human BK channel Ca2+-activation apparatus at 3.0 A resolution. Science 2010, 329:182-186.
44. Zhang Z., Rosenhouse-Dantsker A., Tang Q.Y., Noskov S., Logothetis D.E. The RCK2 domain uses a coordination site present in Kir channels to confer sodium sensitivity to Slo2.2 channels. J.Neurosci. 2010, 30:7554-7562.