Phosphorylation and protonation of neighboring MiRP2 sites: Function and pathophysiology of MiRP2-Kv3.4 potassium channels in periodic paralysis

FASEB Journal

Volumn 20, Issue 2, 2006, Pages 293-301

  Abbott, Geoffrey W ^a   Butler, Margaret H ^b   Goldstein, Steve A N ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

KCNE3; Kv3.4; MiRP2; Periodic paralysis

Indexed keywords

HISTIDINE; MINK RELATED PEPTIDE 2; POTASSIUM CHANNEL; PROTEIN KINASE C; PROTEIN SUBUNIT; SERINE; KCNC4 PROTEIN, HUMAN; KCNE3 PROTEIN, HUMAN; PROTON; SHAW POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CELL PH; CHANNEL GATING; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE MUTATION; IN VIVO STUDY; MISSENSE MUTATION; MOLECULAR MIMICRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PERIODIC PARALYSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN VARIANT; PROTON TRANSPORT; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CELL LINE; CHEMISTRY; GENETIC PREDISPOSITION; GENETICS; HAMSTER; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE;

MUSTELA VISON;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; CONSERVED SEQUENCE; CRICETINAE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; ION CHANNEL GATING; MOLECULAR SEQUENCE DATA; MUTATION; PARALYSES, FAMILIAL PERIODIC; PHOSPHORYLATION; POTASSIUM CHANNELS, VOLTAGE-GATED; PROTEIN STRUCTURE, TERTIARY; PROTONS; SHAW POTASSIUM CHANNELS;

EID: 33644891605     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-5070com     Document Type: Article

References (52)

1. Abbott, G. W., and Goldstein, S. A. (1998) A superfamily of small potassium channel subunits: form and function of the MinK-related peptides (MiRPs). Q. Rev. Biophys. 31, 357-398
2. McCrossan, Z. A., and Abbott, G. W. (2004) The MinK-Related Peptides. Neuropharmacology 47, 787-821
3. Barhanin, J., Lesage, F., Guillemare, E., Fink, M., Lazdunski, M., and Romey, G. (1996) K(V)LQT1 and lsK (minK) proteins associate to form the I(Ks) cardiac potassium current. Nature (London) 384, 78-80
4. Sanguinetti, M. C., Curran, M. E., Zou, A., Shen, J., Spector, P. S., Atkinson, D. L., and Keating, M. T. (1996) Coassembly of K(V)LQT1 and minK (IsK) proteins to form cardiac I(Ks) potassium channel. Nature (London) 384, 80-83
5. Abbott, G. W., Sesti, F., Splawski, I., Buck, M. E., Lehmann, M. H., Timothy, K. W., Keating, M. T., and Goldstein, S. A. (1999) MiRP1 Forms IKr Potassium Channels with HERG and Is Associated with Cardiac Arrhythmia. Cell 97, 175-187
6. Abbott, G. W., Butler, M. H., Bendahhou, S., Dalakas, M. C., Ptacek, L. J., and Goldstein, S. A. (2001) MiRP2 forms potassium channels in skeletal muscle with Kv3.4 and is associated with periodic paralysis. Cell 104, 217-231
7. Isbrandt, D., Friederich, P., Solth, A., Haverkamp, W., Ebneth, A., Borggrefe, M., Funke, H., Sauter, K., Breithardt, G., Pongs, O., et al. (2002) Identification and functional characterization of a novel KCNE2 (MiRP1) mutation that alters HERG channel kinetics. J. Mol. Med. 80, 524-532
8. Sesti, F., Abbott, G. W., Wei, J., Murray, K. T., Saksena, S., Schwartz, P. J., Priori, S. G., Roden, D. M., George, A. L., Jr., and Goldstein, S. A. (2000) A common polymorphism associated with antibiotic-induced cardiac arrhythmia. Proc. Natl. Acad. Sci. USA 97, 10613-10618
9. Splawski, I., Timothy, K. W., Vincent, G. M., Atkinson, D. L., and Keating, M. T. (1997) Molecular basis of the long-QT syndrome associated with deafness. N. Engl. J. Med. 336, 1562-1567
10. Splawski, I., Tristani-Firouzi, M., Lehmann, M. H., Sanguinetti, M. C., and Keating, M. T. (1997) Mutations in the hminK gene cause long QT syndrome and suppress IKs function. Nat. Genet. 17, 338-340
11. Tyson, J., Tranebjaerg, L., Bellman, S., Wren, C., Taylor, J. F., Bathen, J., Aslaksen, B., Sorland, S. J., Lund, O., Malcolm, S., et al. (1997) IsK and KvLQT1: mutation in either of the two subunits of the slow component of the delayed rectifier potassium channel can cause Jervell and Lange-Nielsen syndrome. Hum. Mol. Genet. 6, 2179-2185
12. Ptacek, L. (1998) The familial periodic paralyses and nondystrophic myotonias. Am. J. Med. 105, 58-70
13. Ptacek, L. J. (1999) Channelopathies: ion channel disorders of muscle as a paradigm for paroxysmal disorders of the nervous system. Dig. Dis. Sci. 44, 94S-96S
14. Sesti, F., and Goldstein, S. A. (1998) Single-channel characteristics of wild-type IKs channels and channels formed with two minK mutants that cause long QT syndrome. J. Gen. Physiol. 112, 651-663
15. Abbott, G. W., and Goldstein, S. A. (2002) Disease-associated mutations in KCNE potassium channel subunits (MiRPs) reveal promiscuous disruption of multiple currents and conservation of mechanism. FASEB J. 16, 390-400
16. Park, K. H., Kwok, S. M., Sharon, C., Berga, R., and Sesti, F. (2003) N-glycosylation-dependent block is a novel mechanism for drug-induced cardiac arrhythmia. FASEB J. 17, 2308-2309
17. Splawski, I., Timothy, K. W., Tateyama, M., Clancy, C. E., Malhotra, A., Beggs, A. H., Cappuccio, F. P., Sagnella, G. A., Kass, R. S., and Keating, M. T. (2002) Variant of SCN5A sodium channel implicated in risk of cardiac arrhythmia. Science 297, 1333-1336
18. Plant, L. D., Bowers, P. N., Liu, Q., Morgan, T., Zhang, T., State, M. W., Chen, W., Kittles, R. A., and Goldstein, S. A. N. (2005) A common cardiac sodium channel variant associated with sudden infant death in African Americans, SCN5A-S1103Y. J. Clin. Invest. In press
19. Kuzmenkin, A., Muncan, V., Jurkat-Rott, K., Hang, C., Lerche, H., Lehmann-Horn, F., and Mitrovic, N. (2002) Enhanced inactivation and pH sensitivity of Na(+) channel mutations causing hypokalaemic periodic paralysis type II. Brain 125, 835-843
20. Landau, E. M., Gavish, B., Nachshen, D. A., and Lotan, I. (1981) pH dependence of the acetylcholine receptor channel: a species variation. J. Gen. Physiol. 77, 647-666
21. Lopes, C. M., Zilberberg, N., and Goldstein, S. A. (2001) Block of Kcnk3 by protons. Evidence that 2-P-domain potassium channel subunits function as homodimers. J. Biol. Chem. 276, 24449-24452
22. Schroter, K. H., Ruppersberg, J. P., Wunder, F., Rettig, J., Stocker, M., and Pongs, O. (1991) Cloning and functional expression of a TEA-sensitive A-type potassium channel from rat brain. FEBS Lett. 278, 211-216
23. Covarrubias, M., Wei, A., Salkoff, L., and Vyas, T. B. (1994) Elimination of rapid potassium channel inactivation by phosphorylation of the inactivation gate. Neuron 13, 1403-1412
24. Stephens, G. J., and Robertson, B. (1995) Inactivation of the cloned potassium channel mouse Kv1.1 by the human Kv3.4 "ball" peptide and its chemical modification. J. Physiol. (London) 484, 1-13
25. Antz, C., Bauer, T., Kalbacher, H., Frank, R., Covarrubias, M., Kalbitzer, H. R., Ruppersberg, J. P., Baukrowitz, T., and Fakler, B. (1999) Control of K+ channel gating by protein phosphorylation: structural switches of the inactivation gate. Nat. Struct. Biol. 6, 146-150
26. Gamper, G., Stulnig, T., and Weissel, M. (1998) Thyrotoxic hypokalemic periodic paralysis in a male Kurd. Acta Med. Austriaca 25, 106-108
27. Tengan, C. H., De Oliveira, A. S., and Gabbai, A. A. (1994) Periodic paralysis. Clinical analysis in 20 patients. Arq. Neuropsiquiatr. 52, 501-509
28. Connett, R. J. (1987) Glycolytic regulation during an aerobic rest-to-work transition in dog gracilis muscle. J. Appl. Physiol. 63, 2366-2374
29. Connett, R. J. (1987) Cytosolic pH during a rest-to-work transition in red muscle: application of enzyme equilibria. J. Appl. Physiol. 63, 2360-2365
30. Adams, G. R., Foley, J. M., and Meyer, R. A. (1990) Muscle buffer capacity estimated from pH changes during rest-to-work transitions. J. Appl. Physiol. 69, 968-972
31. Barstow, T. J., Buchthal, S., Zanconato, S., and Cooper, D. M. (1994) Muscle energetics and pulmonary oxygen uptake kinetics during moderate exercise. J. Appl. Physiol. 77, 1742-1749
32. Wasserman, K., Stringer, W. W., Casaburi, R., and Zhang, Y. Y. (1997) Mechanism of the exercise hyperkalemia: an alternate hypothesis. J. Appl. Physiol. 83, 631-643
33. Chuang, M. L., Ting, H., Otsuka, T., Sun, X. G., Chiu, F. Y., Beaver, W. L., Hansen, J. E., Lewis, D. A., and Wasserman, K. (1999) Aerobically generated CO(2) stored during early exercise. J. Appl. Physiol. 87, 1048-1058
34. Stringer, W., Wasserman, K., Casaburi, R., Porszasz, J., Maehara, K., and French, W. (1994) Lactic acidosis as a facilitator of oxyhemoglobin dissociation during exercise. J. Appl. Physiol. 76, 1462-1467
35. Walter, G., Vandenborne, K., Elliott, M., and Leigh, J. S. (1999) In vivo ATP synthesis rates in single human muscles during high intensity exercise. J. Physiol. (London) 519, 901-910
36. Kowalchuk, J. M., Smith, S. A., Weening, B. S., Marsh, G. D., and Paterson, D. H. (2000) Forearm muscle metabolism studied using (31)P-MRS during progressive exercise to fatigue after Acz administration. J. Appl. Physiol. 89, 200-209
37. Gutmann, L. (2000) Periodic paralyses. Neurol. Clin. 18, 195-202
38. Ikeda, K., Iwasaki, Y., Kinoshita, M., Yabuki, D., Igarashi, O., Ichikawa, Y., and Satoyoshi, E. (2002) Acetazolamide-induced muscle weakness in hypokalemic periodic paralysis. Intern. Med. 41, 743-745
39. Ptacek, L. J. (1999) Ion channel diseases: episodic disorders of the nervous system. Semin. Neurol. 19, 363-369
40. Tawil, R., McDermott, M. P., Brown, R., Jr., Shapiro, B. C., Ptacek, L. J., McManis, P. G., Dalakas, M. C., Spector, S. A., Mendell, J. R., Hahn, A. F., et al. (2000) Randomized trials of dichlorphenamide in the periodic paralyses. Working Group on Periodic Paralysis. Ann. Neurol. 47, 46-53
41. Fontaine, B., Vale-Santos, J., Jurkat-Rott, K., Reboul, J., Plassart, E., Rime, C. S., Elbaz, A., Heine, R., Guimaraes, J., and Weissenbach, J. (1994) Mapping of the hypokalaemic periodic paralysis (HypoPP) locus to chromosome 1q31-32 in three European families. Nat. Genet. 6, 267-272
42. Ptacek, L. J., Tawil, R., Griggs, R. C., Engel, A. G., Layzer, R. B., Kwiecinski, H., McManis, P. G., Santiago, L., Moore, M., and Fouad, G. (1994) Dihydropyridine receptor mutations cause hypokalemic periodic paralysis. Cell 77, 863-868
43. 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
44. Jurkat-Rott, K., Mitrovic, N., Hang, C., Kouzmekine, A., Iaizzo, P., Herzog, J., Lerche, H., Nicole, S., Vale-Santos, J., Chauveau, D., et al. (2000) Voltage-sensor sodium channel mutations cause hypokalemic periodic paralysis type 2 by enhanced inactivation and reduced current. Proc. Natl. Acad. Sci. USA 97, 9549-9554
45. Ptacek, L. J., Tyler, F., Trimmer, J. S., Agnew, W. S., and Leppert, M. (1991) Analysis in a large hyperkalemic periodic paralysis pedigree supports tight linkage to a sodium channel locus. Am. J. Hum. Genet. 49, 378-382
46. Ptacek, L. J., Trimmer, J. S., Agnew, W. S., Roberts, J. W., Petajan, J. H., and Leppert, M. (1991) Paramyotonia congenita and hyperkalemic periodic paralysis map to the same sodium-channel gene locus. Am. J. Hum. Genet. 49, 851-854
47. Rojas, C. V., Wang, J. Z., Schwartz, L. S., Hoffman, E. P., Powell, B. R., and Brown, R. H., Jr. (1991) A Met-to-Val mutation in the skeletal muscle Na+ channel alpha-subunit in hyperkalaemic periodic paralysis. Nature (London) 354, 387-389
48. Koch, M. C., Steinmeyer, K., Lorenz, C., Ricker, K., Wolf, F., Otto, M., Zoll, B., Lehmann-Horn, F., Grzeschik, K. H., and Jentsch, T. J. (1992) The skeletal muscle chloride channel in dominant and recessive human myotonia. Science 257, 797-800
49. George, A. L., Jr., Crackower, M. A., Abdalla, J. A., Hudson, A. J., and Ebers, G. C. (1993) Molecular basis of Thomsen's disease (autosomal dominant myotonia congenita). Nat. Genet. 3, 305-310
50. Plaster, N. M., Tawil, R., Tristani-Firouzi, M., Canun, S., Bendahhou, S., Tsunoda, A., Donaldson, M. R., Iannaccone, S. T., Brunt, E., Barohn, R., et al. (2001) Mutations in Kir2.1 cause the developmental and episodic electrical phenotypes of Andersen's syndrome. Cell 105, 511-519
51. Jurkat-Rott, K., and Lehmann-Horn, F. (2004) Periodic paralysis mutation MiRP2-R83H in controls: Interpretations and general recommendation. Neurology 62, 1012-1015
52. McCrossan, Z. A., Lewis, A., Panaghie, G., Jordan, P. N., Christini, D. J., Lerner, D. J., and Abbott, G. W. (2003) MinK-related peptide 2 modulates Kv2.1 and Kv3.1 potassium channels in mammalian brain. J. Neurosci. 23, 8077-8091