AMP-activated protein kinase inhibits Kv1.5 channel currents of pulmonary arterial myocytes in response to hypoxia and inhibition of mitochondrial oxidative phosphorylation

Journal of Physiology

Volumn 594, Issue 17, 2016, Pages 4901-4915

  Moral Sanz, Javier ^a   Mahmoud, Amira D ^a   Ross, Fiona A ^b   Eldstrom, Jodene ^c   Fedida, David ^c   Hardie, D Grahame ^b   Evans, A Mark ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; POTASSIUM CHANNEL KV1.5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL HYPOXIA; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HEK293 CELL LINE; INHIBITION KINETICS; MALE; MITOCHONDRIAL RESPIRATION; MUSCLE CELL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERIAL MYOCYTE; RAT;

EID: 84986278349     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP272032     Document Type: Article

References (82)

1. Andersen MN, Skibsbye L, Tang C, Petersen F, MacAulay N, Rasmussen HB & Jespersen T (2015). PKC and AMPK regulation of Kv1.5 potassium channels. Channels (Austin) 9, 121–128.
2. + channels, Kv1.5 and Kv2.1, in hypoxic pulmonary vasoconstriction and control of resting membrane potential in rat pulmonary artery myocytes. J Clin Invest 101, 2319–2330.
3. + channels in resistance pulmonary arteries explains regional heterogeneity in hypoxic pulmonary vasoconstriction: ionic diversity in smooth muscle cells. Circ Res 95, 308–318.
4. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR & Cohen P (2007). The selectivity of protein kinase inhibitors: a further update. Biochem J 408, 297–315.
5. Bartsch P, Mairbaurl H, Maggiorini M & Swenson ER (2005). Physiological aspects of high-altitude pulmonary edema. J Appl Physiol (1985) 98, 1101–1110.
6. Blom N, Gammeltoft S & Brunak S (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294, 1351–1362.
7. + channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11, 37–51.
8. Bonnet S, Michelakis ED, Porter CJ, Andrade-Navarro MA, Thebaud B, Bonnet S, Haromy A, Harry G, Moudgil R, McMurtry MS, Weir EK & Archer SL (2006). An abnormal mitochondrial-hypoxia inducible factor-1α-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: similarities to human pulmonary arterial hypertension. Circulation 113, 2630–2641.
9. K(V) and enhances apoptosis. Am J Physiol Cell Physiol 287, C715-722.
10. Burg ED, Platoshyn O, Tsigelny IF, Lozano-Ruiz B, Rana BK & Yuan JX (2010). Tetramerization domain mutations in KCNA5 affect channel kinetics and cause abnormal trafficking patterns. Am J Physiol Cell Physiol 298, C496–509.
11. ATP channel and insulin secretion in rats. Diabetologia 52, 1112–1121.
12. Cheung PC, Salt IP, Davies SP, Hardie DG & Carling D (2000). Characterization of AMP-activated protein kinase γ-subunit isoforms and their role in AMP binding. Biochem J 346, 659–669.
13. Cidad P, Jimenez-Perez L, Garcia-Arribas D, Miguel-Velado E, Tajada S, Ruiz-McDavitt C, Lopez-Lopez JR & Perez-Garcia MT (2012). Kv1.3 channels can modulate cell proliferation during phenotypic switch by an ion-flux independent mechanism. Arterioscler Thromb Vasc Biol 32, 1299–1307.
14. Cidad P, Miguel-Velado E, Ruiz-McDavitt C, Alonso E, Jimenez-Perez L, Asuaje A, Carmona Y, Garcia-Arribas D, Lopez J, Marroquin Y, Fernandez M, Roque M, Perez-Garcia MT & Lopez-Lopez JR (2015). Kv1.3 channels modulate human vascular smooth muscle cells proliferation independently of mTOR signaling pathway. Pflugers Arch 467, 1711–1722.
15. + channels Kv1.3 and Kv1.5 in human cancer. Front Physiol 4, 283.
16. Corton JM, Gillespie JG, Hawley SA & Hardie DG (1995). 5-Aminoimidazole-4-carboxamide ribonucleoside: a specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229, 558–565.
17. David M, Macias A, Moreno C, Prieto A, Martinez-Marmol R, Vicente R, Gonzalez T, Felipe A, Tamkun MM & Valenzuela C (2012). Protein kinase C (PKC) activity regulates functional effects of Kvβ1.3 subunit on KV1.5 channels: identification of a cardiac Kv1.5 channelosome. J Biol Chem 287, 21416–21428.
18. Dipp M, Nye PC & Evans AM (2001). Hypoxic release of calcium from the sarcoplasmic reticulum of pulmonary artery smooth muscle. Am J Physiol Lung Cell Mol Physiol 281, L318–325.
19. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M & Shaw RJ (2011). Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331, 456–461.
20. + channel activity and enhances survival in vascular smooth muscle cells. Am J Physiol Cell Physiol 281, C157–165.
21. + currents. Am J Physiol Cell Physiol 284, C1405–1410.
22. El-Mir MY, Nogueira V, Fontaine E, Averet N, Rigoulet M & Leverve X (2000). Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J Biol Chem 275, 223–228.
23. Evans AM (2006). AMP-activated protein kinase underpins hypoxic pulmonary vasoconstriction and carotid body excitation by hypoxia in mammals. Exp Physiol 91, 821–827.
24. Evans AM, Hardie DG, Peers C, Wyatt CN, Viollet B, Kumar P, Dallas ML, Ross F, Ikematsu N, Jordan HL, Barr BL, Rafferty JN & Ogunbayo O (2009). Ion channel regulation by AMPK: the route of hypoxia-response coupling in thecarotid body and pulmonary artery. Ann NY Acad Sci 1177, 89–100.
25. 2-sensing cells? J Biol Chem 280, 41504–41511.
26. Firth AL, Gordienko DV, Yuill KH & Smirnov SV (2009). Cellular localization of mitochondria contributes to Kv channel-mediated regulation of cellular excitability in pulmonary but not mesenteric circulation. Am J Physiol Lung Cell Mol Physiol 296, L347–360.
27. Firth AL, Remillard CV, Platoshyn O, Fantozzi I, Ko EA & Yuan JX (2011). Functional ion channels in human pulmonary artery smooth muscle cells: voltage-dependent cation channels. Pulm Circ 1, 48–71.
28. Firth AL, Yuill KH & Smirnov SV (2008). Mitochondria-dependent regulation of Kv currents in rat pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 295, L61–70.
29. Gomez-Galeno JE, Dang Q, Nguyen TH, Boyer SH, Grote MP, Sun Z, Chen M, Craigo WA, van Poelje PD, MacKenna DA, Cable EE, Rolzin PA, Finn PD, Chi B, Linemeyer DL, Hecker SJ & Erion MD (2010). A potent and selective AMPK activator that inhibits de novo lipogenesis. ACS Med Chem Lett 1, 478–482.
30. Goncharov DA, Kudryashova TV, Ziai H, Ihida-Stansbury K, DeLisser H, Krymskaya VP, Tuder RM, Kawut SM & Goncharova EA (2014). Mammalian target of rapamycin complex 2 (mTORC2) coordinates pulmonary artery smooth muscle cell metabolism, proliferation, and survival in pulmonary arterial hypertension. Circulation 129, 864–874.
31. Goransson O, McBride A, Hawley SA, Ross FA, Shpiro N, Foretz M, Viollet B, Hardie DG & Sakamoto K (2007). Mechanism of action of A-769662, a valuable tool for activation of AMP-activated protein kinase. J Biol Chem 282, 32549–32560.
32. Gowans GJ, Hawley SA, Ross FA & Hardie DG (2013). AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab 18, 556–566.
33. Hardie DG (2014a). AMP-activated protein kinase: a key regulator of energy balance with many roles in human disease. J Intern Med 276, 543–559.
34. Hardie DG (2014b). AMPK–sensing energy while talking to other signaling pathways. Cell Metab 20, 939–952.
35. Hardie DG (2014c). AMPK: positive and negative regulation, and its role in whole-body energy homeostasis. Curr Opin Cell Biol 33C, 1–7.
36. Hardie DG, Schaffer BE & Brunet A (2016). AMPK: an energy-sensing pathway with multiple inputs and outputs. Trends Cell Biol 26, 190–201.
37. Hawley SA, Ross FA, Chevtzoff C, Green KA, Evans A, Fogarty S, Towler MC, Brown LJ, Ogunbayo OA, Evans AM & Hardie DG (2010). Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab 11, 554–565.
38. Holmes TC, Fadool DA, Ren R & Levitan IB (1996). Association of Src tyrosine kinase with a human potassium channel mediated by SH3 domain. Science 274, 2089–2091.
39. Hunter RW, Foretz M, Bultot L, Fullerton MD, Deak M, Ross FA, Hawley SA, Shpiro N, Viollet B, Barron D, Kemp BE, Steinberg GR, Hardie DG & Sakamoto K (2014). Mechanism of action of Compound-13: an α1-selective small molecule activator of AMPK. Chem Biol 21, 866–879.
40. Ibe JC, Zhou Q, Chen T, Tang H, Yuan JX, Raj JU & Zhou G (2013). Adenosine monophosphate-activated protein kinase is required for pulmonary artery smooth muscle cell survival and the development of hypoxic pulmonary hypertension. Am J Resp Cell Mol Biol 49, 609–618.
41. Ikematsu N, Dallas ML, Ross FA, Lewis RW, Rafferty JN, David JA, Suman R, Peers C, Hardie DG & Evans AM (2011). Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability. Proc Natl Acad Sci USA 108, 18132–18137.
42. Jones RG, Plas DR, Kubek S, Buzzai M, Mu J, Xu Y, Birnbaum MJ & Thompson CB (2005). AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 18, 283–293.
43. Kato M & Staub NC (1966). Response of small pulmonary arteries to unilobar hypoxia and hypercapnia. Circ Res 19, 426–440.
44. + channels induces apoptosis in vascular smooth muscle cells. Am J Physiol Cell Physiol 280, C970–979.
45. + channel function by the Kvβ1.3 subunit. J Biol Chem 274, 25355–25361.
46. Lahm T, Tuder RM & Petrache I (2014). Progress in solving the sex hormone paradox in pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 307, L7–26.
47. Lang F & Foller M (2014). Regulation of ion channels and transporters by AMP-activated kinase (AMPK). Channels (Austin) 8, 20–28.
48. 2+ responses to hypoxia. Am J Physiol Lung Cell Mol Physiol 295, L104–113.
49. Macias A, de la Cruz A, Prieto A, Peraza DA, Tamkun MM, Gonzalez T & Valenzuela C (2014). PKC inhibition results in a Kv 1.5 + Kv β1.3 pharmacology closer to Kv 1.5 channels. Br J Pharmacol 171, 4914–4926.
50. Martens JR, Kwak YG & Tamkun MM (1999). Modulation of Kv channel α/β subunit interactions. Trends Cardiovasc Med 9, 253–258.
51. Mia S, Munoz C, Pakladok T, Siraskar G, Voelkl J, Alesutan I & Lang F (2012). Downregulation of Kv1.5 K channels by the AMP-activated protein kinase. Cell Physiol Biochem 30, 1039–1050.
52. Michelakis ED, McMurtry MS, Wu XC, Dyck JR, Moudgil R, Hopkins TA, Lopaschuk GD, Puttagunta L, Waite R & Archer SL (2002). Dichloroacetate, a metabolic modulator, prevents and reverses chronic hypoxic pulmonary hypertension in rats: role of increased expression and activity of voltage-gated potassium channels. Circulation 105, 244–250.
53. 2-sensor in resistance artery smooth muscle cells. J Mol Cell Cardiol 37, 1119–1136.
54. Moral-Sanz J, Gonzalez T, Menendez C, David M, Moreno L, Macias A, Cortijo J, Valenzuela C, Perez-Vizcaino F & Cogolludo A (2011). Ceramide inhibits Kv currents and contributes to TP-receptor-induced vasoconstriction in rat and human pulmonary arteries. Am J Physiol Cell Physiol 301, C186–194.
55. Morales-Cano D, Menendez C, Moreno E, Moral-Sanz J, Barreira B, Galindo P, Pandolfi R, Jimenez R, Moreno L, Cogolludo A, Duarte J & Perez-Vizcaino F (2014). The flavonoid quercetin reverses pulmonary hypertension in rats. PloS ONE 9, e114492.
56. + channels in determining pulmonary vascular tone, oxygen sensing, cell proliferation, and apoptosis: implications in hypoxic pulmonary vasoconstriction and pulmonary arterial hypertension. Microcirculation 13, 615–632.
57. Olschewski A, Papp R, Nagaraj C & Olschewski H (2014). Ion channels and transporters as therapeutic targets in the pulmonary circulation. Pharmacol Ther 144, 349–368.
58. Owen MR, Doran E & Halestrap AP (2000). Evidence that metformin exerts its anti-diabetic effects through inhibition of complex 1 of the mitochondrial respiratory chain. Biochem J 348, 607–614.
59. Platoshyn O, Brevnova EE, Burg ED, Yu Y, Remillard CV & Yuan JX (2006). Acute hypoxia selectively inhibits KCNA5 channels in pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 290, C907–916.
60. + channels in human pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 287, L226–238.
61. V channel expression and function in pulmonary artery myocytes. Am J Physiol Lung Cell Mol Physiol 280, L801–812.
62. Post JM, Hume JR, Archer SL & Weir EK (1992). Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction. Am J Physiol 262, C882–890.
63. 2-sensitive potassium channel Kv1.5 reduces pulmonary hypertension and restores hypoxic pulmonary vasoconstriction in chronically hypoxic rats. Circulation 107, 2037–2044.
64. Prieto-Lloret J, Ramirez M, Olea E, Moral-Sanz J, Cogolludo A, Castaneda J, Yubero S, Agapito T, Gomez-Nino A, Rocher A, Rigual R, Obeso A, Perez-Vizcaino F & Gonzalez C (2015). Hypoxic pulmonary vasoconstriction, carotid body function and erythropoietin production in adult rats perinatally exposed to hyperoxia. J Physiol 593, 2459–2477.
65. Remillard CV, Tigno DD, Platoshyn O, Burg ED, Brevnova EE, Conger D, Nicholson A, Rana BK, Channick RN, Rubin LJ, O'Connor D T & Yuan JX (2007). Function of Kv1.5 channels and genetic variations of KCNA5 in patients with idiopathic pulmonary arterial hypertension. Am J Physiol Cell Physiol 292, C1837–1853.
66. Robertson TP, Mustard KJ, Lewis TH, Clark JH, Wyatt CN, Blanco EA, Peers C, Hardie DG & Evans AM (2008). AMP-activated protein kinase and hypoxic pulmonary vasoconstriction. Eur J Pharmacol 595, 39–43.
67. Ross FA, Jensen TE & Hardie DG (2016). Differential regulation by AMP and ADP of AMPK complexes containing different gamma subunit isoforms. Biochem J 473, 189–199.
68. Ross FA, Rafferty JN, Dallas ML, Ogunbayo O, Ikematsu N, McClafferty H, Tian L, Widmer H, Rowe IC, Wyatt CN, Shipston MJ, Peers C, Hardie DG & Evans AM (2011). Selective expression in carotid body type I cells of a single splice variant of the large conductance calcium- and voltage-activated potassium channel confers regulation by AMP-activated protein kinase. J Biol Chem 286, 11929–11936.
69. Sakamoto K, Goransson O, Hardie DG & Alessi DR (2004). Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR. Am J Physiol Endocrinol Metab 287, E310–E317.
70. Scott JW, Ling N, Issa SM, Dite TA, O'Brien MT, Chen ZP, Galic S, Langendorf CG, Steinberg GR, Kemp BE & Oakhill JS (2014). Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling. Chem Biol 21, 619–627.
71. Scott JW, van Denderen BJ, Jorgensen SB, Honeyman JE, Steinberg GR, Oakhill JS, Iseli TJ, Koay A, Gooley PR, Stapleton D & Kemp BE (2008). Thienopyridone drugs are selective activators of AMP-activated protein kinase β1-containing complexes. Chem Biol 15, 1220–1230.
72. Smirnov SV, Beck R, Tammaro P, Ishii T & Aaronson PI (2002). Electrophysiologically distinct smooth muscle cell subtypes in rat conduit and resistance pulmonary arteries. J Physiol 538, 867–878.
73. Sweeney M & Yuan JX (2000). Hypoxic pulmonary vasoconstriction: role of voltage-gated potassium channels. Respir Res 1, 40–48.
74. Tipparaju SM, Li XP, Kilfoil PJ, Xue B, Uversky VN, Bhatnagar A & Barski OA (2012). Interactions between the C-terminus of Kv1.5 and Kvβ regulate pyridine nucleotide-dependent changes in channel gating. Pflugers Arch 463, 799–818.
75. + channel Kv1.5 in B-lymphocyte physiology: expression associated with human lymphoma malignancy. J Leukocyte Biol 94, 779–789.
76. von Euler US & Liljestrand G (1946). Observations on the pulmonary arterial blood pressure in the cat. Acta Physiol Scand 12, 301–320.
77. Wang J, Shimoda LA & Sylvester JT (2004). Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 286, L848–858.
78. Williams CP, Hu N, Shen W, Mashburn AB & Murray KT (2002). Modulation of the human Kv1.5 channel by protein kinase C activation: role of the Kvβ1.2 subunit. J Pharmacol Exp Ther 302, 545–550.
79. Wilson SM, Mason HS, Smith GD, Nicholson N, Johnston L, Janiak R & Hume JR (2002). Comparative capacitative calcium entry mechanisms in canine pulmonary and renal arterial smooth muscle cells. J Physiol 543, 917–931.
80. Xiao B, Sanders MJ, Carmena D, Bright NJ, Haire LF, Underwood E, Patel BR, Heath RB, Walker PA, Hallen S, Giordanetto F, Martin SR, Carling D & Gamblin SJ (2013). Structural basis of AMPK regulation by small molecule activators. Nat Commun 4, 3017.
81. + channels in pulmonary artery smooth muscle cells of patients with primary pulmonary hypertension. Circulation 98, 1400–1406.
82. Yuan XJ, Goldman WF, Tod ML, Rubin LJ & Blaustein MP (1993). Hypoxia reduces potassium currents in cultured rat pulmonary but not mesenteric arterial myocytes. Am J Physiol 264, L116–123.