K V2.1 and electrically silent K V channel subunits control excitability and contractility of guinea pig detrusor smooth muscle

American Journal of Physiology - Cell Physiology

Volumn 302, Issue 2, 2012, Pages

  Hristov, Kiril L ^a   Chen, Muyan ^a   Soder, Rupal P ^a   Parajuli, Shankar P ^a   Cheng, Qiuping ^a   Kellett, Whitney F ^a   Petkov, Georgi V ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Immunocytochemistry; Patch clamp; Reverse transcriptase polymerase chain reaction; Stromatoxin 1; Urinary bladder; Western blot

Indexed keywords

ELECTRICALLY SILENT KV CHANNEL SUBUNIT; MESSENGER RNA; POTASSIUM CHANNEL KV2.1; PROTEIN INHIBITOR; STROMATOXIN 1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; CARBACHOL; CARDIOTONIC AGENT; PEPTIDE; POTASSIUM CHLORIDE; SHAB POTASSIUM CHANNEL; SPIDER VENOM; STROMATOXIN PROTEIN, STROMATOPELMA CALCEATA;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; DETRUSOR MUSCLE; ELECTROPHYSIOLOGY; GENE EXPRESSION; GUINEA PIG; IMMUNOCYTOCHEMISTRY; MOLECULAR DYNAMICS; MUSCLE CONTRACTION; MUSCLE EXCITATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING; WHOLE CELL; ANIMAL; BLADDER; CELL MEMBRANE POTENTIAL; CHANNEL GATING; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GENETICS; HISTOLOGY; HUMAN; MALE; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER;

CAVIA;

ANIMALS; CARBACHOL; CARDIOTONIC AGENTS; FEMALE; GUINEA PIGS; HUMANS; ION CHANNEL GATING; MALE; MEMBRANE POTENTIALS; MUSCLE CONTRACTION; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; PATCH-CLAMP TECHNIQUES; PEPTIDES; POTASSIUM CHLORIDE; PROTEIN SUBUNITS; SHAB POTASSIUM CHANNELS; SPIDER VENOMS; URINARY BLADDER;

EID: 84855338217     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00303.2010     Document Type: Article

References (64)

1. Amberg GC, Santana LF. Kv2 channels oppose myogenic constriction of rat cerebral arteries. Am J Physiol Cell Physiol 291: C348-C356, 2006.
2. Andersson KE, Arner A. Urinary bladder contraction and relaxation: physiology and pathophysiology. Psychol Rev 84: 935-986, 2004.
3. Andersson KE, Wein AJ. Pharmacology of the lower urinary tract: basis for current and future treatments of urinary incontinence. Pharmacol Rev 56: 581-631, 2004.
4. + channels in resistance pulmonary arteries explains regional heterogeneity in hypoxic pulmonary vasoconstriction: ionic diversity in smooth muscle cells. Circ Res 95: 308-318, 2004.
5. Beech DJ, Bolton TB. Two components of potassium current activated by depolarization of single smooth muscle cells from the rabbit portal vein. J Physiol 418: 293-309, 1989.
6. Bocksteins E, Raes AL, Van de Vijver G, Bruyns T, Van Bogaert PP, Snyders DJ. Kv2.1 and silent Kv subunits underlie the delayed rectifier K+ current in cultured small mouse DRG neurons. Am J Physiol Cell Physiol 296: C1271-C1278, 2009.
7. + channel. Am J Physiol Renal Physiol 295: F1149-F1157, 2008.
8. Castellano A, Chiara MD, Mellstrom B, Molina A, Monje F, Naranjo JR, Lopez-Barneo J. Identification and functional characterization of a K+ channel alpha-subunit with regulatory properties specific to brain. J Neurosci 17: 4652-4661, 1997.
9. Chen M, Kellett WF, Petkov GV. Voltage-gated K+ channels sensitive to stromatoxin-1 regulate myogenic and neurogenic contractions of rat urinary bladder smooth muscle. Am J Physiol Regul Integr Comp Physiol 299: R177-R184, 2010.
10. Chen M, Petkov GV. Identification of large conductance calcium activated potassium channel accessory beta4 subunit in rat and mouse bladder smooth muscle. J Urol 182: 374-381, 2009.
11. Collier ML, Ji G, Wang Y, Kotlikoff MI. Calcium-induced calcium release in smooth muscle: loose coupling between the action potential and calcium release. J Gen Physiol 115: 653-662, 2000.
12. Coppock EA, Martens JR, Tamkun MM. Molecular basis of hypoxiainduced pulmonary vasoconstriction: role of voltage-gated K+ channels. Am J Physiol Lung Cell Mol Physiol 281: L1-L12, 2001.
13. Czirják G, Tóth ZE, Enyedi P. Characterization of the heteromeric potassium channel formed by Kv2.1 and the retinal subunit Kv8.2 in Xenopus oocytes. J Neurophysiol 98: 1213-1222, 2007.
14. Davies AM, Batchelor TJ, Eardley I, Beech DJ. Potassium channel KValpha1 subunit expression and function in human detrusor muscle. J Urol 167: 1881-1886, 2002.
15. Escoubas P, Diochot S, Celerier ML, Nakajima T, Lazdunski M. Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol Pharmacol 62: 48-57, 2002.
16. Escoubas P, Rash L. Tarantulas: eight-legged pharmacists and combinatorial chemists. Toxicon 43: 555-574, 2004.
17. Fujii K, Foster CD, Brading AF, Parekh AB. Potassium channel blockers and the effects of cromakalim on the smooth muscle of the guinea-pig bladder. Br J Pharmacol 99: 779-785, 1990.
18. Gan XG, An RH, Bai YF, Zong DB. Expressions of voltage-gated K+ channel 2.1 and 22 in rat bladder with detrusor hyperreflexia. Chin Med J (Engl) 121: 1574-1577, 2008.
19. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391: 85-100, 1981.
20. Hashitani H, Brading AF. Electrical properties of detrusor smooth muscles from the pig and human urinary bladder. Br J Pharmacol 140: 146-158, 2003.
21. Hashitani H, Brading AF. Ionic basis for the regulation of spontaneous excitation in detrusor smooth muscle cells of the guinea-pig urinary bladder. Br J Pharmacol 140: 159-169, 2003.
22. Hashitani H, Brading AF, Suzuki H. Correlation between spontaneous electrical, calcium and mechanical activity in detrusor smooth muscle of the guinea-pig bladder. Br J Pharmacol 141: 183-193, 2004.
23. Hashitani H, Fukuta H, Takano H, Klemm MF, Suzuki H. Origin and propagation of spontaneous excitation in smooth muscle of the guinea-pig urinary bladder. J Physiol 530: 273-286, 2001.
24. Hayama E, Imamura S, Wu C, Nakazawa M, Matsuoka R, Nakanishi T. Analysis of voltage-gated potassium channel beta1 subunits in the porcine neonatal ductus arteriosus. Pediatr Res 59: 167-174, 2006.
25. Hayase M, Hashitani H, Kohri K, Suzuki H. Role of K+ channels in regulating spontaneous activity in detrusor smooth muscle in situ in the mouse bladder. J Urol 181: 2355-2365, 2009.
26. Heppner TJ, Bonev AD, Nelson MT. Ca2+-activated K+ channels regulate action potential repolarization in urinary bladder smooth muscle. Am J Physiol Cell Physiol 273: C110-C117, 1997.
27. Heppner TJ, Bonev AD, Nelson MT. Elementary purinergic Ca2+ transients evoked by nerve stimulation in rat urinary bladder smooth muscle. J Physiol 564: 201-212, 2005.
28. Heppner TJ, Herrera GM, Bonev AD, Hill-Eubanks D, Nelson MT. Ca2+ sparks and KCa channels: novel mechanisms to relax urinary bladder smooth muscle. Adv Exp Med Biol 539: 347-357, 2003.
29. Herrera GM, Pozo MJ, Zvara P, Petkov GV, Bond CT, Adelman JP, Nelson MT. Urinary bladder instability induced by selective suppression of the murine small conductance calcium-activated potassium (SK3) channel. J Physiol 551: 893-903, 2003.
30. Horn R, Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92: 145-159, 1988.
31. Hristov KL, Chen M, Kellett WF, Rovner ES, Petkov GV. Largeconductance voltage- and Ca2+-activated K+ channels regulate human detrusor smooth muscle function. Am J Physiol Cell Physiol 301: C903- C912, 2011.
32. Hristov KL, Cui X, Brown SM, Liu L, Kellett WF, Petkov GV. Stimulation of β3-adrenoceptors relaxes rat urinary bladder smooth muscle via activation of the large-conductance Ca2+-activated K+ channels. Am J Physiol Cell Physiol 295: C1344-C1353, 2008.
33. Hulme JT, Coppock EA, Felipe A, Martens JR, Tamkun MM. Oxygen sensitivity of cloned voltage-gated K(+) channels expressed in the pulmonary vasculature. Circ Res 85: 489-497, 1999.
34. Kerschensteiner D, Monje F, Stocker M. Structural determinants of the regulation of the voltage-gated potassium channel Kv2.1 by the modulatory alpha-subunit Kv9.3. J Biol Chem 278: 18154-18161, 2003.
35. Kerschensteiner D, Soto F, Stocker M. Fluorescence measurements reveal stoichiometry of K+ channels formed by modulatory and delayed rectifier alpha-subunits. Proc Natl Acad Sci USA 102: 6160-6165, 2005.
36. Kerschensteiner D, Stocker M. Heteromeric assembly of Kv2.1 with Kv9.3: effect on the state dependence of inactivation. Biophys J 77: 248-257, 1999.
37. Kotlikoff MI. Calcium-induced calcium release in smooth muscle: the case for loose coupling. Prog Biophys Mol Biol 83: 171-191, 2003.
38. Kramer JW, Post MA, Brown AM, Kirsch GE. Modulation of potassium channel gating by coexpression of Kv2.1 with regulatory Kv5.1 or Kv6.1 α-subunits. Am J Physiol Cell Physiol 274: C1501-C1510, 1998.
39. Kyle B, Bradley E, Ohya S, Sergeant GP, McHale NG, Thornbury KD, Hollywood MA. Contribution of Kv2.1 channels to the delayed rectifier current in freshly dispersed smooth muscle cells from rabbit urethra. Am J Physiol Cell Physiol 301: C1186-C1200, 2011.
40. McDaniel SS, Platoshyn O, Yu Y, Sweeney M, Miriel VA, Golovina VA, Krick S, Lapp BR, Wang JY, Yuan JX. Anorexic effect of K+ channel blockade in mesenteric arterial smooth muscle and intestinal epithelial cells. J Appl Physiol 91: 2322-2333, 2001.
41. Michelakis ED, Rebeyka I, Wu X, Nsair A, Thebaud B, Hashimoto K, Dyck JR, Haromy A, Harry G, Barr A, Archer SL. O2 sensing in the human ductus arteriosus: regulation of voltage-gated K+ channels in smooth muscle cells by a mitochondrial redox sensor. Circ Res 91: 478-486, 2002.
42. Moreno-Dominguez A, Cidad P, Miguel-Velado E, Lopez-Lopez JR, Perez-Garcia MT. De novo expression of Kv6.3 contributes to changes in vascular smooth muscle cell excitability in a hypertensive mice strain. J Physiol 587: 625-640, 2009.
43. Ohya S, Tanaka M, Watanabe M, Maizumi Y. Diverse expression of delayed rectifier K+ channel subtype transcripts in several types of smooth muscles of the rat. J Smooth Muscle Res 36: 101-115, 2000.
44. Ottschytsch N, Raes A, Van Hoorick D, Snyders DJ. Obligatory heterotetramerization of three previously uncharacterized Kv channel alpha-subunits identified in the human genome. Proc Natl Acad Sci USA 99: 7986-7991, 2002.
45. Patel AJ, Honore E. Molecular physiology of oxygen-sensitive potassium channels. Eur Respir J 18: 221-227, 2001.
46. Patel AJ, Lazdunski M, Honore E. Kv2.1/Kv9.3, a novel ATP-dependent delayed-rectifier K+ channel in oxygen-sensitive pulmonary artery myocytes. EMBO J 16: 6615-6625, 1997.
47. Petkov GV. Ion channels. In: Pharmacology: Principles and Practice, edited by Hacker M, Messer W, Bachmann K. Boston, MA: Elsevier/ Academic, 2009, chapt. 16, p. 385-425.
48. Petkov GV, Bonev AD, Heppner TJ, Brenner R, Aldrich RW, Nelson MT. Beta1-subunit of the Ca2+-activated K+ channel regulates contractile activity of mouse urinary bladder smooth muscle. J Physiol 537: 443-452, 2001.
49. Petkov GV, Heppner TJ, Bonev AD, Herrera GM, Nelson MT. Low levels of KATP channel activation decrease excitability and contractility of urinary bladder. Am J Physiol Regul Integr Comp Physiol 280: R1427-R1433, 2001.
50. Petkov GV, Nelson MT. Differential regulation of Ca2+-activated K+ channels by β-adrenoceptors in guinea pig urinary bladder smooth muscle. Am J Physiol Cell Physiol 288: C1255-C1263, 2005.
51. Platoshyn O, Yu Y, Golovina VA, McDaniel SS, Krick S, Li L, Wang JY, Rubin LJ, Yuan JX. Chronic hypoxia decreases KV channel expression and function in pulmonary artery myocytes. Am J Physiol Lung Cell Mol Physiol 280: L801-L812, 2001.
52. Robertson BE, Nelson MT. Aminopyridine inhibition and voltage dependence of K+ currents in smooth muscle cells from cerebral arteries. Am J Physiol Cell Physiol 267: C1589-C1597, 1994.
53. Salinas M, de Weille J, Guillemare E, Lazdunski M, Hugnot JP. Modes of regulation of shab K+ channel activity by the Kv8.1 subunit. J Biol Chem 272: 8774-8780, 1997.
54. Salinas M, Duprat F, Heurteaux C, Hugnot JP, Lazdunski M. New modulatory alpha subunits for mammalian Shab K+ channels. J Biol Chem 272: 24371-24379, 1997.
55. Sano Y, Mochizuki S, Miyake A, Kitada C, Inamura K, Yokoi H, Nozawa K, Matsushime H, Furuichi K. Molecular cloning and characterization of Kv6.3, a novel modulatory subunit for voltage-gated K(+) channel Kv2.1. FEBS Lett 512: 230-234, 2002.
56. Smirnov SV, Beck R, Tammaro P, Ishii T, Aaronson PI. Electrophysiologically distinct smooth muscle cell subtypes in rat conduit and resistance pulmonary arteries. J Physiol 538: 867-878, 2002.
57. Stocker M, Hellwig M, Kerschensteiner D. Subunit assembly and domain analysis of electrically silent K+ channel alpha-subunits of the rat Kv9 subfamily. J Neurochem 72: 1725-1734, 1999.
58. Stocker M, Kerschensteiner D. Cloning and tissue distribution of two new potassium channel alpha-subunits from rat brain. Biochem Biophys Res Commun 248: 927-934, 1998.
59. Thorneloe KS, Nelson MT. Properties and molecular basis of the mouse urinary bladder voltage-gated K+ current. J Physiol 549: 65-74, 2003.
60. Wang J, Weigand L, Wang W, Sylvester JT, Shimoda LA. Chronic hypoxia inhibits Kv channel gene expression in rat distal pulmonary artery. Am J Physiol Lung Cell Mol Physiol 288: L1049-L1058, 2005.
61. Wareing M, Bai X, Seghier F, Turner CM, Greenwood SL, Baker PN, Taggart MJ, Fyfe GK. Expression and function of potassium channels in the human placental vasculature. Am J Physiol Regul Integr Comp Physiol 291: R437-R446, 2006.
62. Wulff H, Castle NA, Pardo LA. Voltage-gated potassium channels as therapeutic targets. Nat Rev Drug Discov 8: 982-1001, 2009.
63. Zhong XZ, Abd-Elrahman KS, Liao CH, El-Yazbi AF, Walsh EJ, Walsh MP, Cole WC. Stromatoxin-sensitive, heteromultimeric Kv2.1/ Kv9.3 channels contribute to myogenic control of cerebral arterial diameter. J Physiol 588: 4519-4537, 2010.
64. Zhu XR, Netzer R, Böhlke K, Liu Q, Pongs O. Structural and functional characterization of Kv6.2 a new gamma-subunit of voltage-gated potassium channel. Receptors Channels 6: 337-350, 1999.