81
Views
2
CrossRef citations to date
0
Altmetric
Original Article

Kv7 channel inhibition increases hypoxic pulmonary vasoconstriction in endotoxemic mouse lungs

, , , & ORCID Icon
Pages 363-375 | Received 12 Mar 2020, Accepted 31 Aug 2020, Published online: 18 Sep 2020

References

  • Marshall BE, Hanson CW, Frasch F, Marshall C. Role of hypoxic pulmonary vasoconstriction in pulmonary gas exchange and blood flow distribution. 2. Pathophysiology. Intensive Care Med. 1994;20(5):379–389. doi:10.1007/BF01720916.
  • SRLF Trial Group. Hypoxemia in the ICU: prevalence, treatment, and outcome. Ann Intensive Care. 2018; 8:82.
  • Ogasawara H, Koizumi T, Yamamoto H, Kubo K. Effects of a selective nitric oxide synthase inhibitor on endotoxin-induced alteration in hypoxic pulmonary vasoconstriction in sheep. J Cardiovasc Pharmacol. 2003;42(4):521–526. doi:10.1097/00005344-200310000-00010.
  • Barnes PJ, Liu SF. Regulation of pulmonary vascular tone. Pharmacol Rev. 1995;47(1):87–131.
  • Solé L, Vallejo-Gracia A, Roig SR, et al. KCNE gene expression is dependent on the proliferation and mode of activation of leukocytes. Channels (Austin)). 2013;7(2):85–96. doi:10.4161/chan.23258.
  • Spöhr F, Cornelissen AJ, Busch C, et al. Role of endogenous nitric oxide in endotoxin-induced alteration of hypoxic pulmonary vasoconstriction in mice. Am J Physiol Heart Circ Physiol. 2005;289(2):H823–831. doi:10.1152/ajpheart.00605.2004.
  • Spöhr F, Busch CJ, Reich C, et al. 4-Aminopyridine restores impaired hypoxic pulmonary vasoconstriction in endotoxemic mice. Anesthesiology. 2007;107(4):597–604. doi:10.1097/01.anes.0000281897.13703.fd.
  • Bonnet S, Archer SL. Potassium channel diversity in the pulmonary arteries and pulmonary veins: implications for regulation of the pulmonary vasculature in health and during pulmonary hypertension. Pharmacol Ther. 2007;115(1):56–69. doi:10.1016/j.pharmthera.2007.03.014.
  • Weir EK, Archer SL. The mechanism of acute hypoxic pulmonary vasoconstriction: the tale of two channels. Faseb J. 1995;9(2):183–189. doi:10.1096/fasebj.9.2.7781921.
  • Sweeney M, Yuan JXJ. Hypoxic pulmonary vasoconstriction: role of voltage-gated potassium channels. Respir Res. 2000;1(1):40–48. doi:10.1186/rr11.
  • Gutman GA, Chandy KG, Grissmer S, et al. International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltage-gated potassium channels. Pharmacol Rev. 2005;57(4):473–508. doi:10.1124/pr.57.4.10.
  • Coppock EA, Martens JR, Tamkun MM. Molecular basis of hypoxia-induced pulmonary vasoconstriction: role of voltage-gated K + channels. Am J Physiol Lung Cell Mol Physiol. 2001;281(1):L1–12. doi:10.1152/ajplung.2001.281.1.L1.
  • Sommer N, Dietrich A, Schermuly RT, et al. Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms. Eur Respir J. 2008;32(6):1639–1651. doi:10.1183/09031936.00013908.
  • Sedivy V, Joshi S, Ghaly Y, et al. Role of Kv7 channels in responses of the pulmonary circulation to hypoxia. Am J Physiol Lung Cell Mol Physiol. 2015;308(1):L48–57. doi:10.1152/ajplung.00362.2013.
  • Joshi S, Sedivy V, Hodyc D, Herget J, Gurney AM. KCNQ modulators reveal a key role for KCNQ potassium channels in regulating the tone of rat pulmonary artery smooth muscle. J Pharmacol Exp Ther. 2009;329(1):368–376. doi:10.1124/jpet.108.147785.
  • Yeung SY, Pucovský V, Moffatt JD, et al. Molecular expression and pharmacological identification of a role for K(v)7 channels in murine vascular reactivity. Br J Pharmacol. 2007;151(6):758–770. doi:10.1038/sj.bjp.0707284.
  • Mackie AR, Brueggemann LI, Henderson KK, et al. Vascular KCNQ potassium channels as novel targets for the control of mesenteric artery constriction by vasopressin, based on studies in single cells, pressurized arteries, and in vivo measurements of mesenteric vascular resistance. J Pharmacol Exp Ther. 2008;325(2):475–483. doi:10.1124/jpet.107.135764.
  • Hedegaard ER, Nielsen BD, Kun A, et al. KV 7 channels are involved in hypoxia-induced vasodilatation of porcine coronary arteries . Br J Pharmacol. 2014;171(1):69–82. doi:10.1111/bph.12424.
  • Zhong XZ, Harhun MI, Olesen SP, et al. Participation of KCNQ (Kv7) potassium channels in myogenic control of cerebral arterial diameter. J Physiol (Lond).). 2010;588(Pt 17):3277–3293. doi:10.1113/jphysiol.2010.192823.
  • Schroeder BC, Waldegger S, Fehr S, et al. A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature. 2000;403(6766):196–199. doi:10.1038/35003200.
  • McCrossan ZA, Lewis A, Panaghie G, et al. MinK-related peptide 2 modulates Kv2.1 and Kv3.1 potassium channels in mammalian brain. J Neurosci. 2003;23(22):8077–8091. doi:10.1523/JNEUROSCI.23-22-08077.2003.
  • Zhang M, Jiang M, Tseng GN. minK-related peptide 1 associates with Kv4.2 and modulates its gating function: potential role as beta subunit of cardiac transient outward channel?. Circ Res. 2001;88(10):1012–1019. doi:10.1161/hh1001.090839.
  • Kanda VA, Abbott GW. KCNE Regulation of K(+) channel trafficking – a Sisyphean task. ? Front Physiol. 2012; 3:231doi:10.3389/fphys.2012.00231.
  • de Castro MP, Aránega A, Franco D. Protein distribution of Kcnq1, Kcnh2, and Kcne3 potassium channel subunits during mouse embryonic development. Anat Rec A Discov Mol Cell Evol Biol. 2006;288(3):304–315. doi:10.1002/ar.a.20312.
  • Cidad P, Moreno-Dominguez A, Novensa L, et al. Characterization of ion channels involved in the proliferative response of femoral artery smooth muscle cells. Arterioscler Thromb Vasc Biol. 2010;30(6):1203–1211. doi:10.1161/ATVBAHA.110.205187.
  • Lippi G, Montagnana M, Meschi T, Comelli I, Cervellin G. Genetic and clinical aspects of Brugada syndrome: an update. Adv Clin Chem. 2012; 56:197–208. doi:10.1016/b978-0-12-394317-0.00009-1.
  • Grahammer F, Warth R, Barhanin J, Bleich M, Hug MJ. The small conductance K + channel, KCNQ1: expression, function, and subunit composition in murine trachea. J Biol Chem. 2001;276(45):42268–42275. doi:10.1074/jbc.M105014200.
  • MacVinish LJ, Guo Y, Dixon AK, Murrell-Lagnado RD, Cuthbert AW. Xe991 reveals differences in K(+) channels regulating chloride secretion in murine airway and colonic epithelium. Mol Pharmacol. 2001; 60:753–760.
  • Wang W, Kim HJ, Lee JH, et al. Functional Significance of K + Channel β-Subunit KCNE3 in Auditory Neurons. J Biol Chem. 2014;289(24):16802–16813. doi:10.1074/jbc.M113.545236.
  • Zhang X, Hughes BA. KCNQ and KCNE potassium channel subunit expression in bovine retinal pigment epithelium. Exp Eye Res. 2013; 116:424–432.
  • Thomas GP, Gerlach U, Antzelevitch C. HMR 1556, a potent and selective blocker of slowly activating delayed rectifier potassium current. J Cardiovasc Pharmacol. 2003;41(1):140–147. doi:10.1097/00005344-200301000-00018.
  • Andersen MN, Krzystanek K, Jespersen T, Olesen SP, Rasmussen HB. AMP-activated protein kinase downregulates Kv7.1 cell surface expression. Traffic. 2012;13(1):143–156. doi:10.1111/j.1600-0854.2011.01295.x.
  • Brueggemann LI, Mackie AR, Cribbs LL, et al. Differential protein kinase C-dependent modulation of Kv7.4 and Kv7.5 subunits of vascular Kv7 channels. J Biol Chem. 2014;289(4):2099–2111. doi:10.1074/jbc.M113.527820.
  • Kilpatrick LE, Standage SW, Li H, et al. Protection against sepsis-induced lung injury by selective inhibition of protein kinase C-δ (δ-PKC). J Leukoc Biol. 2011;89(1):3–10. doi:10.1189/jlb.0510281.
  • Strutz-Seebohm N, Seebohm G, Fedorenko O, et al. Functional coassembly of KCNQ4 with KCNE-beta- subunits in Xenopus oocytes. Cell Physiol Biochem. 2006;18(1-3):57–66. doi:10.1159/000095158.
  • Roura-Ferrer M, Etxebarria A, Solé L, et al. Functional Implications of KCNE subunit expression for the Kv7.5 (KCNQ5) channel. Cell Physiol Biochem. 2009;24(5-6):325–334. doi:10.1159/000257425.
  • Brouillette J, Lupien MA, St-Michel C, Fiset C. Characterization of ventricular repolarization in male and female guinea pigs. J Mol Cell Cardiol. 2007;42(2):357–366. doi:10.1016/j.yjmcc.2006.11.004.
  • Weimann J, Bloch KD, Takata M, Steudel W, Zapol WM. Congenital NOS2 deficiency protects mice from LPS-induced hyporesponsiveness to inhaled nitric oxide. Anesthesiology. 1999; 91:1744–1753.
  • Ullrich R, Bloch KD, Ichinose F, Steudel W, Zapol WM. Hypoxic pulmonary blood flow redistribution and arterial oxygenation in endotoxin-challenged NOS2-deficient mice. J Clin Invest. 1999;104(10):1421–1429. doi:10.1172/JCI6590.
  • Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol. 2008;295(3):L379–399. doi:10.1152/ajplung.00010.2008.
  • Leeman M, de Beyl VZ, Biarent D, Maggiorini M, Mélot C, Naeije R. Inhibition of cyclooxygenase and nitric oxide synthase in hypoxic vasoconstriction and oleic acid-induced lung injury. Am J Respir Crit Care Med. 1999;159(5 Pt 1):1383–1390. doi:10.1164/ajrccm.159.5.9807114.
  • Ichinose F, Ullrich R, Sapirstein A, et al. Cytosolic phospholipase A(2) in hypoxic pulmonary vasoconstriction. J Clin Invest. 2002;109(11):1493–1500. doi:10.1172/JCI0214294.
  • Uzun O, Demiryurek AT. Role of NO and prostaglandins in acute hypoxic vasoconstriction in sheep pulmonary veins. Pharmacology. 2006;77(3):122–129. doi:10.1159/000093521.
  • Sprague RS, Stephenson AH, Dimmitt RA, et al. Effect of L-NAME on pressure-flow relationships in isolated rabbit lungs: role of red blood cells. Am J Physiol. 1995;269(6 Pt 2):H1941–H1948. doi:10.1152/ajpheart.1995.269.6.H1941.
  • Weissmann N, Akkayagil E, Quanz K, et al. Basic features of hypoxic pulmonary vasoconstriction in mice. Respir Physiol Neurobiol. 2004;139(2):191–202. doi:10.1016/j.resp.2003.10.003.
  • Francis BN, Wilkins MR, Zhao L. Tetrahydrobiopterin and the regulation of hypoxic pulmonary vasoconstriction. Eur Respir J. 2010;36(2):323–330. doi:10.1183/09031936.00188809.
  • Uncles DR, Daugherty MO, Frank DU, Roos CM, Rich GF. Nitric oxide modulation of pulmonary vascular resistance is red blood cell dependent in isolated rat lungs. Anesth Analg. 1996;83(6):1212–1217. doi:10.1097/00000539-199612000-00014.
  • Linehan JH, Haworth ST, Nelin LD, Krenz GS, Dawson CA. A simple distensible vessel model for interpreting pulmonary vascular pressure-flow curves. J Appl Physiol. 1992;73(3):987–994. doi:10.1152/jappl.1992.73.3.987.
  • Fischer LG, Freise H, Hilpert JH, et al. Modulation of hypoxic pulmonary vasoconstriction is time and nitric oxide dependent in a peritonitis model of sepsis. Intensive Care Med. 2004;30(9):1821–1828. doi:10.1007/s00134-004-2351-0.
  • Sylvester JT, Harabin AL, Peake MD, Frank RS. Vasodilator and constrictor responses to hypoxia in isolated pig lungs. J Appl Physiol Respir Environ Exerc Physiol. 1980;49(5):820–825. doi:10.1152/jappl.1980.49.5.820.
  • Spohr F, Busch CJ, Teschendorf P, Weimann J. Selective inhibition of guanylate cyclase prevents impairment of hypoxic pulmonary vasoconstriction in endotoxemic mice. J Physiol Pharmacol. 2009; 60:107–112.
  • Petersen B, Austen KF, Bloch KD, et al. Cysteinyl leukotrienes impair hypoxic pulmonary vasoconstriction in endotoxemic mice. Anesthesiology. 2011; 115:804–811.
  • Peretz A, Degani N, Nachman R, et al. Meclofenamic acid and diclofenac, novel templates of KCNQ2/Q3 potassium channel openers, depress cortical neuron activity and exhibit anticonvulsant properties. Mol Pharmacol. 2005;67(4):1053–1066. doi:10.1124/mol.104.007112.
  • Chadha PS, Zunke F, Davis AJ, et al. Pharmacological dissection of K(v)7.1 channels in systemic and pulmonary arteries. Br J Pharmacol. 2012;166(4):1377–1387. doi:10.1111/j.1476-5381.2012.01863.x.
  • Mikkelsen ME, Shah CV, Meyer NJ, et al. The epidemiology of acute respiratory distress syndrome in patients presenting to the emergency department with severe sepsis. Shock. 2013; 40:375–381.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.