Cerebrovascular dilation via selective targeting of the cholane steroid-recognition site in the bk channel β1-subunit by a novel nonsteroidal agents

Molecular Pharmacology

Volumn 83, Issue 5, 2013, Pages 1030-1044

  Bukiya, Anna N ^a   McMillan, Jacob E ^c   Fedinec, Alexander L ^b   Patil, Shivaputra A ^a   Miller, Duane D ^a   Leffler, Charles W ^b   Parrill, Abby L ^c   Dopico, Alex M ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF MEMPHIS   (United States)

^c University of Memphis   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLANE DERIVATIVE; COMPLEMENTARY DNA; LITHOCHOLIC ACID; NONSTEROID ANTIINFLAMMATORY AGENT; SODIUM 3 HYDROXYOLEAN 12 EN 30 OATE; UNCLASSIFIED DRUG; VOLTAGE GATED SODIUM CHANNEL BETA 1 SUBUNIT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BRAIN ARTERY; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENCY; ELECTROPHYSIOLOGY; FEMALE; MALE; MOLECULAR CLONING; MUSCLE CELL; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RAT; SCORING SYSTEM; VASODILATATION;

ANIMALS; CEREBRAL ARTERIES; CHOLANES; FEMALE; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL BETA SUBUNITS; LITHOCHOLIC ACID; MALE; MICE; MICE, INBRED C57BL; MONOCYTES; RATS; RATS, SPRAGUE-DAWLEY; STEROIDS; VASODILATION; XENOPUS LAEVIS;

EID: 84876587544     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.083519     Document Type: Article

References (60)

1. Baumbach GL and Heistad DD (1985) Regional, segmental, and temporal heterogeneity of cerebral vascular autoregulation. Ann Biomed Eng 13:303-310. (Pubitemid 15044597)
2. Bomzon A and Ljubuncic P (1995) Bile acids as endogenous vasodilators? Biochem Pharmacol 49:581-589.
3. Brenner R, Jegla TJ, Wickenden A, Liu Y, and Aldrich RW (2000a) Cloning and functional characterization of novel large conductance calcium-activated potassium channel beta subunits, hKCNMB3 and hKCNMB4. J Biol Chem 275:6453-6461. (Pubitemid 30129943)
4. Brenner R, Peréz GJ, Bonev AD, Eckman DM, Kosek JC, Wiler SW, Patterson AJ, Nelson MT, and Aldrich RW (2000b) Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature 407:870-876.
5. Bukiya AN, Liu J, and Dopico AM (2009b) The BK channel accessory beta1 subunit determines alcohol-induced cerebrovascular constriction. FEBS Lett 583: 2779-2784.
6. Bukiya AN, Liu J, Toro L, and Dopico AM (2007) Beta1 (KCNMB1) subunits mediate lithocholate activation of large-conductance Ca21-activated K1 channels and dilation in small, resistance-size arteries. Mol Pharmacol 72:359-369. (Pubitemid 47124116)
7. Bukiya AN, McMillan J, Parrill AL, and Dopico AM (2008a) Structural determinants of monohydroxylated bile acids to activate beta 1 subunit-containing BK channels. J Lipid Res 49:2441-2451.
8. Bukiya AN, Patil SA, Li W, Miller DD, and Dopico AM (2012) Calcium-and voltagegated potassium (BK) channel activators in the 5b-cholanic acid-3a-ol analogue series with modifications in the lateral chain. ChemMedChem 7:1784-1792 .
9. Bukiya AN, Singh AK, Parrill AL, and Dopico AM (2011) The steroid interaction site in transmembrane domain 2 of the large conductance, voltage-and calcium-gated potassium (BK) channel accessory b1 subunit. Proc Natl Acad Sci USA 108: 20207-20212.
10. Bukiya AN, Vaithianathan T, Toro L, and Dopico AM (2008b) The second transmembrane domain of the large conductance, voltage-and calcium-gated potassium channel b(1) subunit is a lithocholate sensor. FEBS Lett 582:673-678.
11. Bukiya AN, Vaithianathan T, Toro L, and Dopico AM (2009a) Channel b2-4 subunits fail to substitute for beta1 in sensitizing BK channels to lithocholate. Biochem Biophys Res Commun 390:995-1000.
12. Calderone V, Fiamingo FL, Amato G, Giorgi I, Livi O, Martelli A, and Martinotti E (2008) New amido derivatives as potential BKCa potassium channel activators. XI. Eur J Med Chem 43:792-799. (Pubitemid 351454052)
13. Dopico AM (2003) Ethanol sensitivity of BK(Ca) channels from arterial smooth muscle does not require the presence of the beta 1-subunit. Am J Physiol Cell Physiol 284: C1468-C1480. (Pubitemid 36583388)
14. Dopico AM, Bukiya AN, and Singh AK (2012). Differential contribution of BK subunits to nongenomic regulation of channel function by steroids, in Choesterol Regulaiton of Ion Channels and ReceptorsLevitan I and Barrantes F eds) pp 109-134, Wiley, New York.
15. Dopico AM, Walsh JV, Jr, and Singer JJ (2002) Natural bile acids and synthetic analogues modulate large conductance Ca21-activated K1 (BKCa) channel activity in smooth muscle cells. J Gen Physiol 119:251-273. (Pubitemid 34522239)
16. Dorsch N (2011) A clinical review of cerebral vasospasm and delayed ischaemia following aneurysm rupture. Acta Neurochir Suppl (Wien) 110:5-6.
17. Etminan N, Vergouwen MD, Ilodigwe D, and Macdonald RL (2011) Effect of pharmaceutical treatment on vasospasm, delayed cerebral ischemia, and clinical outcome in patients with aneurysmal subarachnoid hemorrhage: A systematic review and meta-analysis. J Cereb Blood Flow Metab 31:1443-1451.
18. Faraci FM and Sobey CG (1998) Role of potassium channels in regulation of cerebral vascular tone. J Cereb Blood Flow Metab 18:1047-1063. (Pubitemid 28465352)
19. Fernández-Fernández JM, Tomás M, Vázquez E, Orio P, Latorre R, Sentí M, Marrugat J, and Valverde MA (2004) Gain-of-function mutation in the KCNMB1 potassium channel subunit is associated with low prevalence of diastolic hypertension. J Clin Invest 113:1032-1039. (Pubitemid 38544125)
20. Gerasimenko JV, Flowerdew SE, Voronina SG, Sukhomlin TK, Tepikin AV, Petersen OH, and Gerasimenko OV (2006) Bile acids induce Ca21 release from both the endoplasmic reticulum and acidic intracellular calcium stores through activation of inositol trisphosphate receptors and ryanodine receptors. J Biol Chem 281: 40154-40163. (Pubitemid 46041820)
21. Ghatta S, Nimmagadda D, Xu X, and O'Rourke ST (2006) Large-conductance, calcium-activated potassium channels: Structural and functional implications. Pharmacol Ther 110:103-116. (Pubitemid 43248728)
22. Gourley JK and Heistad DD (1984) Characteristics of reactive hyperemia in the cerebral circulation. Am J Physiol 246:H52-H58. (Pubitemid 14147888)
23. Holtzclaw JD, Grimm PR, and Sansom SC (2011) Role of BK channels in hypertension and potassium secretion. Curr Opin Nephrol Hypertens 20:512-517.
24. Hossmann KA (1994) Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557-565.
25. Jaggar JH, Li A, Parfenova H, Liu J, Umstot ES, Dopico AM, and Leffler CW (2005) Heme is a carbon monoxide receptor for large-conductance Ca21-activated K1 channels. Circ Res 97:805-812. (Pubitemid 41447131)
26. Jaggar JH, Wellman GC, Heppner TJ, Porter VA, Perez GJ, Gollasch M, Kleppisch T, Rubart M, Stevenson AS, and Lederer WJ et al. (1998) Ca21 channels, ryanodine receptors and Ca(21)-activated K1 channels: A functional unit for regulating arterial tone. Acta Physiol Scand 164:577-587. (Pubitemid 29015676)
27. Jordan JD and Nyquist P (2010) Biomarkers and vasospasm after aneurysmal subarachnoid hemorrhage. Neurosurg Clin N Am 21:381-391.
28. Ju YE and Schwedt TJ (2010) Abrupt-onset severe headaches. Semin Neurol 30: 192-200.
29. Kaneda N, Pezzuto JM, Kinghorn AD, Farnsworth NR, Santisuk T, Tuchinda P, Udchachon J, and Reutrakul V (1992) Plant anticancer agents, L. cytotoxic triterpenes from Sandoricum koetjape stems. J Nat Prod 55:654-659.
30. Knot HJ and Nelson MT (1998) Regulation of arterial diameter and wall [Ca21] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol 508:199-209. (Pubitemid 28167582)
31. Korovkina VP, Brainard AM, Ismail P, Schmidt TJ, and England SK (2004) Estradiol binding to maxi-K channels induces their down-regulation via proteasomal degradation. J Biol Chem 279:1217-1223. (Pubitemid 38082645)
32. Lee BC, Lim HH, Kim S, Youn HS, Lee Y, Kim YC, Eom SH, Lee KW, and Park CS (2012) Localization of a site of action for benzofuroindole-induced potentiation of BKCa channels. Mol Pharmacol 82:143-155.
33. Lee RM (1995) Morphology of cerebral arteries. Pharmacol Ther 66:149-173.
34. Liang Z, Zhang L, Li L, Liu J, Li H, Zhang L, Chen L, Cheng K, Zheng M, and Wen X et al. (2011) Identification of pentacyclic triterpenes derivatives as potent inhibitors against glycogen phosphorylase based on 3D-QSAR studies. Eur J Med Chem 46:2011-2021.
35. Liu P, Xi Q, Ahmed A, Jaggar JH, and Dopico AM (2004) Essential role for smooth muscle BK channels in alcohol-induced cerebrovascular constriction. Proc Natl Acad Sci USA 101:18217-18222. (Pubitemid 40054100)
36. Makishima M, Lu TT, Xie W, Whitfield GK, Domoto H, Evans RM, Haussler MR, and Mangelsdorf DJ (2002) Vitamin D receptor as an intestinal bile acid sensor. Science 296:1313-1316. (Pubitemid 34522785)
37. Maruyama T, Miyamoto Y, Nakamura T, Tamai Y, Okada H, Sugiyama E, Nakamura T, Itadani H, and Tanaka K (2002) Identification of membranetype receptor for bile acids (M-BAR). Biochem Biophys Res Commun 298: 714-719. (Pubitemid 35356798)
38. McManus OB, Harris GH, Giangiacomo KM, Feigenbaum P, Reuben JP, Addy ME, Burka JF, Kaczorowski GJ, and Garcia ML (1993) An activator of calciumdependent potassium channels isolated from a medicinal herb. Biochemistry 32: 6128-6133. (Pubitemid 23196865)
39. McManus OB, Helms LM, Pallanck L, Ganetzky B, Swanson R, and Leonard RJ (1995) Functional role of the beta subunit of high conductance calcium-activated potassium channels. Neuron 14:645-650.
40. Meera P, Wallner M, and Toro L (2000) A neuronal beta subunit (KCNMB4) makes the large conductance, voltage-and Ca21-activated K1 channel resistant to charybdotoxin and iberiotoxin. Proc Natl Acad Sci USA 97:5562-5567. (Pubitemid 30313758)
41. Modica S and Moschetta A (2006) Nuclear bile acid receptor FXR as pharmacological target: Are we there yet? FEBS Lett 580:5492-5499. (Pubitemid 44488553)
42. Morimoto T, Sakamoto K, Sade H, Ohya S, Muraki K, and Imaizumi Y (2007) Voltage-sensitive oxonol dyes are novel large-conductance Ca21-activated K1 channel activators selective for beta1 and beta4 but not for beta2 subunits. Mol Pharmacol 71:1075-1088. (Pubitemid 46457011)
43. Nielsen T, Burgdorf KS, Grarup N, Borch-Johnsen K, Hansen T, Jørgensen T, Pedersen O, and Andersen G (2008) The KCNMB1 Glu65Lys polymorphism associates with reduced systolic and diastolic blood pressure in the Inter99 study of 5729 Danes. J Hypertens 26:2142-2146.
44. Nieves-Cintrón M, Amberg GC, Nichols CB, Molkentin JD, and Santana LF (2007) Activation of NFATc3 down-regulates the b1 subunit of large conductance, calcium-activated K1 channels in arterial smooth muscle and contributes to hypertension. J Biol Chem 282:3231-3240. (Pubitemid 47084356)
45. Orio P, Rojas P, Ferreira G, and Latorre R (2002) New disguises for an old channel: MaxiK channel beta-subunits. News Physiol Sci 17:156-161.
46. Papassotiriou J, Köhler R, Prenen J, Krause H, Akbar M, Eggermont J, Paul M, Distler A, Nilius B, and Hoyer J (2000) Endothelial K(1) channel lacks the Ca(21) sensitivity-regulating beta subunit. FASEB J 14:885-894. (Pubitemid 30241665)
47. Pérez GJ, Bonev AD, and Nelson MT (2001) Micromolar Ca(21) from sparks activates Ca(21)-sensitive K(1) channels in rat cerebral artery smooth muscle. Am J Physiol Cell Physiol 281:C1769-C1775.
48. Plüger S, Faulhaber J, Fürstenau M, Löhn M, Waldschütz R, Gollasch M, Haller H, Luft FC, Ehmke H, and Pongs O (2000) Mice with disrupted BK channel beta1 subunit gene feature abnormal Ca(21) spark/STOC coupling and elevated blood pressure. Circ Res 87:E53-E60.
49. Ponte CG, McManus OB, Schmalhofer WA, Shen DM, Dai G, Stevenson A, Sur S, Shah T, Kiss L, and Shu M et al. (2012) Selective, direct activation of highconductance, calcium-activated potassium channels causes smooth muscle relaxation. Mol Pharmacol 81:567-577.
50. Qi W, Ding D, and Salvi RJ (2008) Cytotoxic effects of dimethyl sulphoxide (DMSO) on cochlear organotypic cultures. Hear Res 236:52-60.
51. Roy S, Morayo Akande A, Large RJ, Webb TI, Camarasu C, Sergeant GP, McHale NG, Thornbury KD, and Hollywood MA (2012) Structure-activity relationships of a novel group of large-conductance Ca(21)-activated K(1) (BK) channel modulators: The GoSlo-SR family. ChemMedChem 7:1763-1769 .
52. Rusch NJ (2009) BK channels in cardiovascular disease: A complex story of channel dysregulation. Am J Physiol Heart Circ Physiol 297:H1580-H1582.
53. Salkoff L, Butler A, Ferreira G, Santi C, and Wei A (2006) High-conductance potassium channels of the SLO family. Nat Rev Neurosci 7:921-931.
54. Sattar A, Manousakis G, and Jensen MB (2010) Systematic review of reversible cerebral vasoconstriction syndrome. Expert Rev Cardiovasc Ther 8:1417-1421.
55. Sekine T, Ikeda K, Hirayama T, Suzuki A, and Iwasaki Y (2012) Transient splenial lesion after recovery of cerebral vasoconstriction and posterior reversible encephalopathy syndrome: A case report of eclampsia. Intern Med 51:1407-1411.
56. Shahlaie K, Boggan JE, Latchaw RE, Ji C, and Muizelaar JP (2009) Posttraumatic vasospasm detected by continuous brain tissue oxygen monitoring: Treatment with intraarterial verapamil and balloon angioplasty. Neurocrit Care 10:61-69.
57. Strøbaek D, Christophersen P, Holm NR, Moldt P, Ahring PK, Johansen TE, and Olesen SP (1996) Modulation of the Ca(21)-dependent K1 channel, hslo, by the substituted diphenylurea NS 1608, paxilline and internal Ca21. Neuropharmacology 35:903-914. (Pubitemid 26377677)
58. Terasawa T, Okada T, Hara T, and Itoh K (1992) Glycyrrhetinic acid derivatives as potent inhibitors of Na1-, K1-ATPase. Synthesis and structure-activity relationships. Eur J Med Chem 27:345-351 DOI: 10.1016/0223-5234(92)90147-S.
59. Valverde MA, Rojas P, Amigo J, Cosmelli D, Orio P, Bahamonde MI, Mann GE, Vergara C, and Latorre R (1999) Acute activation of Maxi-K channels (hSlo) by estradiol binding to the beta subunit. Science 285:1929-1931.
60. Yan J and Aldrich RW (2012) BK potassium channel modulation by leucine-rich repeat-containing proteins. Proc Natl Acad Sci USA 109:7917-7922.