Optical measurement of gating pore currents in hypokalemic periodic paralysis model cells

Bezanilla, F. (2008). How membrane proteins sense voltage. Nat. Rev. Mol. Cell

Biol. 9, 323-332. doi:10.1038/nrm2376

Bulman, D. E., Scoggan, K. A., Van Oene, M. D., Nicolle, M. W., Hahn, A. F.,

Tollar, L. L. and Ebers, G. C. (1999). A novel sodium channel mutation in a family

with hypokalemic periodic paralysis. Neurology 53, 1932-1936. doi:10.1212/

WNL.53.9.1932

Campos, F. V., Chanda, B., Roux, B. and Bezanilla, F. (2007). Two atomic

constraints unambiguously position the S4 segment relative to S1 and S2

segments in the closed state of Shaker K channel. Proc. Natl. Acad. Sci. USA 104,

7904-7909. doi:10.1073/pnas.0702638104

Cannon, S. C. (2010). Voltage-sensor mutations in channelopathies of skeletal

muscle. J. Physiol. 588, 1887-1895. doi:10.1113/jphysiol.2010.186874

Cannon, S. C. (2015). Channelopathies of skeletal muscle excitability.

Comprehens. Physiol. 5, 761-790. doi:10.1002/cphy.c140062

Capes, D. L., Arcisio-Miranda, M., Jarecki, B. W., French, R. J. and Chanda, B.

(2012). Gating transitions in the selectivity filter region of a sodium channel are

coupled to the domain IV voltage sensor. Proc. Natl. Acad. Sci. USA 109,

2648-2653. doi:10.1073/pnas.1115575109

DiFranco, M., Yu, C., Quinonez,

M. and Vergara, J. L. (2015). Inward rectifier

potassium currents in mammalian skeletal muscle. J. Physiol. 593, 1213-1238.

doi:10.1113/jphysiol.2014.283648

Friend, K. L., Crimmins, D., Phan, T. G., Sue, C. M., Colley, A., Fung, V. S. C.,

Morris, J. G. L., Sutherland, G. R. and Richards, R. I. (1999). Detection of a

novel missense mutation and second recurrent mutation in the CACNA1A gene in

individuals with EA-2 and FHM. Hum. Genet. 105, 261-265. doi:10.1007/

s004399900101

Gamal El-Din, T. M., Lantin, T., Tschumi, C. W., Juarez, B., Quinlan, M.,

Hayano, J. H., Li, J., Zweifel, L. S. and Catterall, W. A. (2021). Autismassociated mutations in KV7 channels induce gating pore current. Proc. Natl.

Acad. Sci. USA 118, e2112666118. doi:10.1073/pnas.2112666118

Disease Models & Mechanisms

Proton transport assay

Disease Models & Mechanisms (2023) 16, dmm049704. doi:10.1242/dmm.049704

Gosselin-Badaroudine, P., Delemotte, L., Moreau, A., Klein, M. L. and

Chahine, M. (2012a). Gating pore currents and the resting state of Nav1.4

voltage sensor domains. Proc. Natl Acad. Sci. USA 109, 19250-19255. doi:10.

1073/pnas.1217990109

Gosselin-Badaroudine, P., Keller, D. I., Huang, H., Pouliot, V., Chatelier, A.,

Osswald, S., Brink, M. and Chahine, M. (2012b). A proton leak current through

the cardiac sodium channel is linked to mixed arrhythmia and the dilated

cardiomyopathy phenotype. PLoS ONE 7, e38331. doi:10.1371/journal.pone.

0038331

Groome, J. R., Lehmann-Horn, F., Fan, C., Wolf, M., Winston, V., Merlini, L. and

Jurkat-Rott, K. (2014). NaV1.4 mutations cause hypokalaemic periodic paralysis

by disrupting IIIS4 movement during recovery. Brain 137, 998-1008. doi:10.1093/

brain/awu015

Jehasse, K., Massotte, L., Hartmann, S., Vitello, R., Ringlet, S., Vitello, M.,

Chua, H. C., Pless, S. A., Engel, D., Lié geois, J.-F. et al. (2021). The gating pore

blocker 1-(2,4-xylyl)guanidinium selectively inhibits pacemaking of midbrain

dopaminergic neurons. Neuropharmacology 197, 108722. doi:10.1016/J.

NEUROPHARM.2021.108722

Jitpimolmard, N., Matthews, E. and Fialho, D. (2020). Treatment updates for

neuromuscular channelopathies. Curr. Treatment Opt. Neurol. 22, 34. doi:10.

1007/s11940-020-00644-2

Jurkat-Rott, K., Mitrovic, N., Hang, C., Kouzmenkine, A., Iaizzo, P., Herzog, J.,

Lerche, H., Nicole, S., Vale-Santos, J., Chauveau, D. et al. (2000). Voltagesensor sodium channel mutations cause hypokalemic periodic paralysis type 2 by

enhanced inactivation and reduced current. Proc. Natl Acad. Sci. USA 97,

9549-9554. doi:10.1073/pnas.97.17.9549

Kirkton, R. D. and Bursac, N. (2011). Engineering biosynthetic excitable tissues

from unexcitable cells for electrophysiological and cell therapy studies. Nat.

Commun. 2, 300. doi:10.1038/NCOMMS1302

Kowarz, E., Lö scher, D. and Marschalek, R. (2015). Optimized Sleeping Beauty

transposons rapidly generate stable transgenic cell lines. Biotechnol. J. 10,

647-653. doi:10.1002/biot.201400821

Lacroix, J. J., Clark Hyde, H., Campos, F. V. and Bezanilla, F. (2014). Moving

gating charges through the gating pore in a Kv channel voltage sensor. Proc. Natl.

Acad. Sci. USA 111, E1950-E1959. doi:10.1073/pnas.1406161111

Leisgen, C., Kuester, M. and Methfessel, C. (2007). The roboocyte: automated

electrophysiology based on Xenopus oocytes. Methods Mol. Biol. 403, 87-109.

doi:10.1007/978-1-59745-529-9_6

Li, Q., Wanderling, S., Paduch, M., Medovoy, D., Singharoy, A., Mcgreevy, R.,

Villalba-Galea, C. A., Hulse, R. E., Roux, B., Schulten, K. et al. (2014).

Structural mechanism of voltage-dependent gating in an isolated voltage-sensing

domain. Nat. Struct. Mol. Biol. 21, 244-252. doi:10.1038/nsmb.2768

Mä nnikkö , R., Shenkarev, Z. O., Thor, M. G., Berkut, A. A., Myshkin, M. Y.,

Paramonov, A. S., Kulbatskii, D. S., Kuzmin, D. A., Castañeda, M. S., King, L.

et al. (2018). Spider toxin inhibits gating pore currents underlying periodic

paralysis. Proc. Natl. Acad. Sci. USA 115, 4495-4500. doi:10.1073/pnas.

1720185115

Matthews, E., Labrum, R., Sweeney, M. G., Sud, R., Haworth, A., Chinnery, P. F.,

Meola, G., Schorge, S., Kullmann, D. M., Davis, M. B. et al. (2009). Voltage

sensor charge loss accounts for most cases of hypokalemic periodic paralysis.

Neurology 72, 1544-1547. doi:10.1212/01.wnl.0000342387.65477.46

Matthews, E., Portaro, S., Ke, Q., Sud, R., Haworth, A., Davis, M. B.,

Griggs, R. C. and Hanna, M. G. (2011). Acetazolamide efficacy in

hypokalemic periodic paralysis and the predictive role of genotype. Neurology

77, 1960-1964. doi:10.1212/WNL.0b013e31823a0cb6

Moreau, A., Gosselin-Badaroudine, P., Boutjdir, M. and Chahine, M. (2015a).

Mutations in the voltage sensors of domains I and II of Nav1.5 that are associated

with arrhythmias and dilated cardiomyopathy generate gating pore currents. Front.

Pharmacol. 6, 301. doi:10.3389/FPHAR.2015.00301

Moreau, A., Gosselin-Badaroudine, P., Delemotte, L., Klein, M. L. and

Chahine, M. (2015b). Gating pore currents are defects in common with two

Nav1.5 mutations in patients with mixed arrhythmias and dilated cardiomyopathy.

J. Gen. Physiol. 145, 93-106. doi:10.1085/jgp.201411304

Moreau, A., Gosselin-Badaroudine, P., Mercier, A., Burger, B., Keller, D. I. and

Chahine, M. (2018). A leaky voltage sensor domain of cardiac sodium channels

causes arrhythmias associated with dilated cardiomyopathy. Sci. Rep. 8, 13804.

doi:10.1038/S41598-018-31772-0

Nguyen, H. X., Kirkton, R. D. and Bursac, N. (2016). Engineering prokaryotic

channels for control of mammalian tissue excitability. Nat. Commun. 7, 13132.

doi:10.1038/NCOMMS13132

Pan, X., Li, Z., Zhou, Q., Shen, H., Wu, K., Huang, X., Chen, J., Zhang, J., Zhu, X.,

Lei, J. et al. (2018). Structure of the human voltage-gated sodium channel Nav1.4

in complex with β1. Science 362, eaau2486. doi:10.1126/science.aau2486

Perni, S., Lavorato, M. and Beam, K. G. (2017). De novo reconstitution reveals the

proteins required for skeletal muscle voltage-induced Ca2+ release. Proc. Natl.

Acad. Sci. USA 114, 13822-13827. doi:10.1073/pnas.1716461115

Rouillard, A. D., Gundersen, G. W., Fernandez, N. F., Wang, Z., Monteiro, C. D.,

McDermott, M. G. and Ma’ayan, A. (2016). The harmonizome: a collection of

processed datasets gathered to serve and mine knowledge about genes and

proteins. Database 2016, baw100. doi:10.1093/database/baw100

Rü del, R., Lehmann-Horn, F., Ricker, K. and Kü ther, G. (1984). Hypokalemic

periodic paralysis: In vitro investigation of muscle fiber membrane parameters.

Muscle Nerve 7, 110-120. doi:10.1002/mus.880070205

Sansone, V. A., Burge, J., Mcdermott, M. P., Smith, P. C., Herr, B., Tawil, R.,

Pandya, S., Kissel, J., Ciafaloni, E., Shieh, P. et al. (2016). Randomized,

placebo-controlled trials of dichlorphenamide in periodic paralysis. Neurology 86,

1408-1416. doi:10.1212/WNL.0000000000002416

Sansone, V. A., Johnson, N. E., Hanna, M. G., Ciafaloni, E., Statland, J. M.,

Shieh, P. B., Cohen, F. and Griggs, R. C. (2021). Long-term efficacy and safety

of dichlorphenamide for treatment of primary periodic paralysis. Muscle Nerve 64,

342-346. doi:10.1002/mus.27354

Sasaki, R., Nakaza, M., Furuta, M., Fujino, H., Kubota, T. and

Takahashi, M. P. (2020). Mutation spectrum and health status in skeletal

muscle channelopathies in Japan. Neuromuscul. Disord. 30, 546-553. doi:10.

1016/j.nmd.2020.06.001

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M.,

Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al.

(2012). Fiji: An open-source platform for biological-image analysis. Nat. Methods

9, 676-682. doi:10.1038/nmeth.2019

Schlief, T., Schö nherr, R., Imoto, K. and Heinemann, S. H. (1996). Pore

properties of rat brain II sodium channels mutated in the selectivity filter domain.

Eur. Biophys. J. 25, 75-91. doi:10.1007/s002490050020

Sokolov, S., Scheuer, T. and Catterall, W. A. (2007). Gating pore current in an

inherited ion channelopathy. Nature 446, 76-78. doi:10.1038/nature05598

Sokolov, S., Scheuer, T. and Catterall, W. A. (2008). Depolarization-activated

gating pore current conducted by mutant sodium channels in potassium-sensitive

normokalemic periodic paralysis. Proc. Natl. Acad. Sci. USA 105, 19980-19985.

doi:10.1073/pnas.0810562105

Sokolov, S., Scheuer, T. and Catterall, W. A. (2010). Ion permeation and block of

the gating pore in the voltage sensor of NaV1.4 channels with hypokalemic

periodic paralysis mutations. J. Gen. Physiol. 136, 225-236. doi:10.1085/jgp.

201010414

Starace, D. M. and Bezanilla, F. (2004). A proton pore in a potassium channel

voltage sensor reveals a focused electric field. Nature 427, 548-553. doi:10.1038/

nature02270

Statland, J. M., Fontaine, B., Hanna, M. G., Johnson, N. E., Kissel, J. T.,

Sansone, V. A., Shieh, P. B., Tawil, R. N., Trivedi, J., Cannon, S. C. et al.

(2018). Review of the diagnosis and treatment of periodic paralysis. Muscle Nerve

57, 522-530. doi:10.1002/mus.26009

Stefani, E. and Bezanilla, F. (1998). [17] Cut-open oocyte voltage-clamp technique.

Methods Enzymol. 293, 300-318. doi:10.1016/S0076-6879(98)93020-8

Struyk, A. F. and Cannon, S. C. (2007). A Na+ channel mutation linked to

hypokalemic periodic paralysis exposes a proton-selective gating pore. J. Gen.

Physiol. 130, 11-20. doi:10.1085/jgp.200709755

Struyk, A. F., Markin, V. S., Francis, D. and Cannon, S. C. (2008). Gating pore

currents in DIIS4 mutations of NaV1.4 associated with periodic paralysis:

saturation of ion flux and implications for disease pathogenesis. J. Gen.

Physiol. 132, 447-464. doi:10.1085/jgp.200809967

Tantsis, E. M., Gill, D., Griffiths, L., Gupta, S., Lawson, J., Maksemous, N.,

Ouvrier, R., Riant, F., Smith, R., Troedson, C. et al. (2016). Eye movement

disorders are an early manifestation of CACNA1A mutations in children. Dev.

Med. Child Neurol. 58, 639-644. doi:10.1111/dmcn.13033

Tao, X., Lee, A., Limapichat, W., Dougherty, D. A. and Mackinnon, R. (2010).

A gating charge transfer center in voltage sensors. Science 328, 67-73. doi:10.

1126/science.1185954

Torres, C. F., Griggs, R. C., Moxley, R. T. and Bender, A. N. (1981). Hypokalemic

periodic paralysis exacerbated by acetazolamide. Neurology 31, 1423-1428.

doi:10.1212/WNL.31.11.1423

Villalba-Galea, C. A., Sandtner, W., Starace, D. M. and Bezanilla, F. (2008). S4based voltage sensors have three major conformations. Proc. Natl. Acad. Sci.

USA 105, 17600-17607. doi:10.1073/pnas.0807387105

Wasano, K., Takahashi, S., Rosenberg, S. K., Kojima, T., Mutai, H.,

Matsunaga, T., Ogawa, K. and Homma, K. (2020). Systematic quantification

of the anion transport function of pendrin (SLC26A4) and its disease-associated

variants. Hum. Mutat. 41, 316-331. doi:10.1002/humu.23930

Wu, F., Mi, W., Burns, D. K., Fu, Y., Gray, H. F., Struyk, A. F. and Cannon, S. C.

(2011). A sodium channel knockin mutant (NaV1.4-R669H) mouse model of

hypokalemic periodic paralysis. J. Clin. Investig. 121, 4082-4094. doi:10.1172/

JCI57398

Wu, F., Mi, W., Herná ndez-Ochoa, E. O., Burns, D. K., Fu, Y., Gray, H. F.,

Struyk, A. F., Schneider, M. F. and Cannon, S. C. (2012). A calcium channel

mutant mouse model of hypokalemic periodic paralysis. J. Clin. Investig. 122,

4580-4591. doi:10.1172/JCI66091

Wu, F., Mi, W. and Cannon, S. C. (2013a). Bumetanide prevents transient

decreases in muscle force in murine hypokalemic periodic paralysis. Neurology

80, 1110-1116. doi:10.1212/WNL.0b013e3182886a0e

Wu, F., Mi, W. and Cannon, S. C. (2013b). Beneficial effects of bumetanide in a

CaV1.1-R528H mouse model of hypokalaemic periodic paralysis. Brain 136,

3766-3774. doi:10.1093/brain/awt280

10

Disease Models & Mechanisms

RESOURCE ARTICLE

Disease Models & Mechanisms (2023) 16, dmm049704. doi:10.1242/dmm.049704

Yoon, J. S., Park, H.-J., Yoo, S.-Y., Namkung, W., Jo, M. J., Koo, S. K., Park, H.Y., Lee, W.-S., Kim, K. H. and Lee, M. G. (2008). Heterogeneity in the processing

defect of SLC26A4 mutants. J. Med. Genet. 45, 411-419. doi:10.1136/jmg.2007.

054635

Zaharieva, I. T., Thor, M. G., Oates, E. C., Van Karnebeek, C., Hendson, G.,

Blom, E., Witting, N., Rasmussen, M., Gabbett, M. T., Ravenscroft, G. et al.

(2016). Loss-of-function mutations in SCN4A cause severe foetal hypokinesia or

‘classical’ congenital myopathy. Brain 139, 674-691. doi:10.1093/brain/awv352

Disease Models & Mechanisms

RESOURCE ARTICLE

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