S-glutathionylation of an auxiliary subunit confers redox sensitivity to Kv4 channel inactivation

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Jerng, Henry H ^a   Pfaffinger, Paul J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; DIPEPTIDYL PEPTIDASE; DIPEPTIDYL PEPTIDASE 10A; DIPEPTIDYL PEPTIDASE 6A; DITHIOTHREITOL; GLUTATHIONE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SERINE; SHAL POTASSIUM CHANNEL; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG; DIAMIDE; DPP10 PROTEIN, HUMAN; DPP6 PROTEIN, HUMAN; KCNIP3 PROTEIN, HUMAN; KV CHANNEL INTERACTING PROTEIN; NERVE PROTEIN; POTASSIUM CHANNEL; PROTEIN SUBUNIT; REPRESSOR PROTEIN;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; AMPLITUDE MODULATION; ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DISULFIDE BOND; ENZYME KINETICS; ENZYME REGULATION; ENZYME SUBUNIT; GENETIC CONSERVATION; GLUTATHIONE METABOLISM; GLUTATHIONYLATION; MUTATIONAL ANALYSIS; NONHUMAN; OOCYTE; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; XENOPUS; ACTION POTENTIAL; ANIMAL; ANTAGONISTS AND INHIBITORS; BOVINE; CYTOLOGY; DRUG EFFECTS; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PATCH CLAMP TECHNIQUE; PROTEIN SUBUNIT; SEQUENCE HOMOLOGY; XENOPUS LAEVIS;

ACTION POTENTIALS; AMINO ACID SEQUENCE; ANIMALS; CATTLE; DIAMIDE; DIPEPTIDYL-PEPTIDASES AND TRIPEPTIDYL-PEPTIDASES; DITHIOTHREITOL; FEMALE; GENE EXPRESSION; GLUTATHIONE; HUMANS; KV CHANNEL-INTERACTING PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; OOCYTES; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PROTEIN SUBUNITS; REACTIVE OXYGEN SPECIES; REPRESSOR PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SHAL POTASSIUM CHANNELS; TERT-BUTYLHYDROPEROXIDE; TRANSFECTION; XENOPUS LAEVIS;

EID: 84899799218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093315     Document Type: Article

References (67)

1. Rudy B (1988) Diversity and ubiquity of K channels. Neuroscience 25: 729-749.
2. Hoshi T, Zagotta WN, Aldrich RW (1990) Biophysical and molecular mechanisms of Shaker potassium channel inactivation. Science 250: 533-538.
3. Yellen G (1998) The moving parts of voltage-gated ion channels. Q Rev Biophys 31: 239-295.
4. Gebauer M, Isbrandt D, Sauter K, Callsen B, Nolting A, et al. (2004) N-type inactivation features of Kv4.2 channel gating. Biophys J 86: 210-223.
5. Lee TE, Philipson LH, Nelson DJ (1996) N-type inactivation in the mammalian Shaker K+ channel Kv1.4. J Membr Biol 151: 225-235.
6. Rasmusson RL, Wang S, Castellino RC, Morales MJ, Strauss HC (1997) The beta subunit, Kv beta 1.2, acts as a rapid open channel blocker of NH2-terminal deleted Kv1.4 alpha-subunits. Adv Exp Med Biol 430: 29-37.
7. Ruppersberg JP, Stocker M, Pongs O, Heinemann SH, Frank R, et al. (1991) Regulation of fast inactivation of cloned mammalian IK(A) channels by cysteine oxidation. Nature 352: 711-714.
8. Wissmann R, Baukrowitz T, Kalbacher H, Kalbitzer HR, Ruppersberg JP, et al. (1999) NMR structure and functional characteristics of the hydrophilic N terminus of the potassium channel beta-subunit Kvbeta1.1. J Biol Chem 274: 35521-35525.
9. Leicher T, Bahring R, Isbrandt D, Pongs O (1998) Coexpression of the KCNA3B gene product with Kv1.5 leads to a novel A-type potassium channel. J Biol Chem 273: 35095-35101.
10. Leicher T, Roeper J, Weber K, Wang X, Pongs O (1996) Structural and functional characterization of human potassium channel subunit beta 1 (KCNA1B). Neuropharmacology 35: 787-795.
11. Heinemann SH, Rettig J, Graack HR, Pongs O (1996) Functional characterization of Kv channel beta-subunits from rat brain. J Physiol 493 (Pt 3): 625-633.
12. Jerng HH, Dougherty K, Covarrubias M, Pfaffinger PJ (2009) A novel N-terminal motif of dipeptidyl peptidase-like proteins produces rapid inactivation of Kv4.2 channels by a pore-blocking mechanism. Channels (Austin) 3: 448-461.
13. Jerng HH, Pfaffinger PJ (2012) Incorporation of DPP6a and DPP6K variants in ternary Kv4 channel complex reconstitutes properties of A-type K current in rat cerebellar granule cells. PLoS One 7: e38205.
14. Serodio P, Kentros C, Rudy B (1994) Identification of molecular components of A-type channels activating at subthreshold potentials. J Neurophysiol 72: 1516-1529.
15. Duprat F, Guillemare E, Romey G, Fink M, Lesage F, et al. (1995) Susceptibility of cloned K+ channels to reactive oxygen species. Proc Natl Acad Sci U S A 92: 11796-11800.
16. Stephens GJ, 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 484 (Pt 1): 1-13.
17. Rettig J, Heinemann SH, Wunder F, Lorra C, Parcej DN, et al. (1994) Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature 369: 289-294.
18. Stephens GJ, Owen DG, Robertson B (1996) Cysteine-modifying reagents alter the gating of the rat cloned potassium channel Kv1.4. Pflugers Arch 431: 435-442.
19. Vega-Saenz de Miera E, Rudy B (1992) Modulation of K+ channels by hydrogen peroxide. Biochem Biophys Res Commun 186: 1681-1687.
20. Finkel T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15.
21. Gilbert HF (1984) Redox control of enzyme activities by thiol/disulfide exchange. Methods Enzymol 107: 330-351.
22. Ziegler DM (1985) Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu Rev Biochem 54: 305-329.
23. Chakravarthi S, Jessop CE, Bulleid NJ (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep 7: 271-275.
24. Kirichok YV, Nikolaev AV, Krishtal OA (1998) [K+]out accelerates inactivation of Shal-channels responsible for A-current in rat CA1 neurons. Neuroreport 9: 625-629.
25. Muller W, Bittner K (2002) Differential oxidative modulation of voltage-dependent K+ currents in rat hippocampal neurons. J Neurophysiol 87: 2990-2995.
26. Jerng HH, Pfaffinger PJ, Covarrubias M (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27: 343-369.
27. Covarrubias M, Bhattacharji A, De Santiago-Castillo JA, Dougherty K, Kaulin YA, et al. (2008) The neuronal Kv4 channel complex. Neurochem Res 33: 1558-1567.
28. Maffie J, Rudy B (2008) Weighing the evidence for a ternary protein complex mediating A-type K+ currents in neurons. J Physiol 586: 5609-5623.
29. Marionneau C, Townsend RR, Nerbonne JM (2010) Proteomic analysis highlights the molecular complexities of native Kv4 channel macromolecular complexes. Semin Cell Dev Biol 22: 145-152.
30. Beck EJ, Bowlby M, An WF, Rhodes KJ, Covarrubias M (2002) Remodelling inactivation gating of Kv4 channels by KChIP1, a small-molecular-weight calcium-binding protein. J Physiol 538: 691-706.
31. Pioletti M, Findeisen F, Hura GL, Minor DL, Jr (2006) Three-dimensional structure of the KChIP1-Kv4.3 T1 complex reveals a cross-shaped octamer. Nat Struct Mol Biol 13: 987-995.
32. Wang H, Yan Y, Liu Q, Huang Y, Shen Y, et al. (2007) Structural basis for modulation of Kv4 K+ channels by auxiliary KChIP subunits. Nat Neurosci 10: 32-39.
33. Maffie J, Blenkinsop T, Rudy B (2009) A novel DPP6 isoform (DPP6-E) can account for differences between neuronal and reconstituted A-type K(+) channels. Neurosci Lett 449: 189-194.
34. Jerng HH, Lauver AD, Pfaffinger PJ (2007) DPP10 splice variants are localized in distinct neuronal populations and act to differentially regulate the inactivation properties of Kv4-based ion channels. Mol Cell Neurosci 35: 604-624.
35. Jerng HH, Qian Y, Pfaffinger PJ (2004) Modulation of Kv4.2 channel expression and gating by dipeptidyl peptidase 10 (DPP10). Biophys J 87: 2380-2396.
36. Sambrook J, Fritsch E, Maniatis T (1989) Molecular Cloning, a Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory.
37. Yang Y, Shi W, Cui N, Wu Z, Jiang C (2010) Oxidative stress inhibits vascular K(ATP) channels by S-glutathionylation. J Biol Chem 285: 38641-38648.
38. Kiehn J, Lacerda AE, Wible B, Brown AM (1996) Molecular physiology and pharmacology of HERG. Single-channel currents and block by dofetilide. Circulation 94: 2572-2579.
39. Wang Z, Kiehn J, Yang Q, Brown AM, Wible BA (1996) Comparison of binding and block produced by alternatively spliced Kvbeta1 subunits. J Biol Chem 271: 28311-28317.
40. Stephens GJ, Garratt JC, Robertson B, Owen DG (1994) On the mechanism of 4-aminopyridine action on the cloned mouse brain potassium channel mKv1.1. J Physiol 477 (Pt 2): 187-196.
41. Kolbe K, Schonherr R, Gessner G, Sahoo N, Hoshi T, et al. (2010) Cysteine 723 in the C-linker segment confers oxidative inhibition of hERG1 potassium channels. J Physiol 588: 2999-3009.
42. Bahring R, Boland LM, Varghese A, Gebauer M, Pongs O (2001) Kinetic analysis of open- and closed-state inactivation transitions in human Kv4.2 A-type potassium channels. J Physiol 535: 65-81.
43. Keck RG (1996) The use of t-butyl hydroperoxide as a probe for methionine oxidation in proteins. Anal Biochem 236: 56-62.
44. Kosower NS, Kosower EM (1995) Diamide: an oxidant probe for thiols. Methods Enzymol 251: 123-133.
45. Kosower NS, Kosower EM, Wertheim B, Correa WS (1969) Diamide, a new reagent for the intracellular oxidation of glutathione to the disulfide. Biochem Biophys Res Commun 37: 593-596.
46. Kurantsin-Mills J, Lessin LS (1981) Aggregation of intramembrane particles in erythrocyte membranes treated with diamide. Biochim Biophys Acta 641: 129-137.
47. Wang G, Shahidullah M, Rocha CA, Strang C, Pfaffinger PJ, et al. (2005) Functionally active t1-t1 interfaces revealed by the accessibility of intracellular thiolate groups in kv4 channels. J Gen Physiol 126: 55-69.
48. Strop P, Bankovich AJ, Hansen KC, Garcia KC, Brunger AT (2004) Structure of a human A-type potassium channel interacting protein DPPX, a member of the dipeptidyl aminopeptidase family. J Mol Biol 343: 1055-1065.
49. Brigelius R, Muckel C, Akerboom TP, Sies H (1983) Identification and quantitation of glutathione in hepatic protein mixed disulfides and its relationship to glutathione disulfide. Biochem Pharmacol 32: 2529-2534.
50. Brigelius R (1983) Glutathione oxidation and activation of pentose phosphate cycle during hydroperoxide metabolism. A comparison of livers from fed and fasted rats. Hoppe Seylers Z Physiol Chem 364: 989-996.
51. Collison MW, Beidler D, Grimm LM, Thomas JA (1986) A comparison of protein S-thiolation (protein mixed-disulfide formation) in heart cells treated with t-butyl hydroperoxide or diamide. Biochim Biophys Acta 885: 58-67.
52. Ochi T (1993) Mechanism for the changes in levels of glutathione upon exposure of cultured mammalian cells to tertiary-butylhydroperoxide and diamide. Arch Toxicol 67: 401-410.
53. Schuppe I, Moldeus P, Cotgreave IA (1992) Protein-specific S-thiolation in human endothelial cells during oxidative stress. Biochem Pharmacol 44: 1757-1764.
54. Chen J, Avdonin V, Ciorba MA, Heinemann SH, Hoshi T (2000) Acceleration of P/C-type inactivation in voltage-gated K(+) channels by methionine oxidation. Biophys J 78: 174-187.
55. Zhang ZH, Rhodes KJ, Childers WE, Argentieri TM, Wang Q (2004) Disinactivation of N-type inactivation of voltage-gated K channels by an erbstatin analogue. J Biol Chem 279: 29226-29230.
56. Barghaan J, Bahring R (2009) Dynamic coupling of voltage sensor and gate involved in closed-state inactivation of kv4.2 channels. J Gen Physiol 133: 205-224.
57. Lock JT, Sinkins WG, Schilling WP (2012) Protein S-Glutathionylation enhances Ca2+-induced Ca2+ release via the IP3 Receptor in Cultured Aortic Endothelial Cells. J Physiol.
58. Figtree GA, Liu CC, Bibert S, Hamilton EJ, Garcia A, et al. (2009) Reversible oxidative modification: a key mechanism of Na +-K+ pump regulation. Circ Res 105: 185-193.
59. Wang W, Oliva C, Li G, Holmgren A, Lillig CH, et al. (2005) Reversible silencing of CFTR chloride channels by glutathionylation. J Gen Physiol 125: 127-141.
60. Zhou M, Morais-Cabral JH, Mann S, MacKinnon R (2001) Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors. Nature 411: 657-661.
61. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K + channel. Science 309: 897-903.
62. Hsieh CP (2008) Redox modulation of A-type K+ currents in pain-sensing dorsal root ganglion neurons. Biochem Biophys Res Commun 370: 445-449.
63. Massaad CA, Klann E (2011) Reactive oxygen species in the regulation of synaptic plasticity and memory. Antioxid Redox Signal 14: 2013-2054.
64. Jiao S, Wu MM, Hu CL, Zhang ZH, Mei YA (2004) Melatonin receptor agonist 2-iodomelatonin prevents apoptosis of cerebellar granule neurons via K(+) current inhibition. J Pineal Res 36: 109-116.
65. Hu CL, Liu Z, Gao ZY, Zhang ZH, Mei YA (2005) 2-iodomelatonin prevents apoptosis of cerebellar granule neurons via inhibition of A-type transient outward K+ currents. J Pineal Res 38: 53-61.
66. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443: 787-795.
67. Sesti F, Liu S, Cai SQ (2009) Oxidation of potassium channels by ROS: a general mechanism of aging and neurodegeneration? Trends Cell Biol 20: 45-51.