Nfluence of extracellular acidosis on the functional contribution of KATP and TASK-1 potassium channels to the regulation of vascular tone in early postnatal ontogenesis

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Abstract

The activity of many proteins and, as a result, of the mechanisms of vascular tone regulation depends on pH. A decrease of pH (uncompensated acidosis), usually causes relaxation of blood vessels, which has been studied in sufficient detail for an adult, matured organism. However, the effect of acidosis on the mechanisms of vascular tone regulation in the early postnatal period remains almost completely unexplored. The aim of this work was to study the effect of extracellular metabolic acidosis on the functional contribution of KATP and TASK-1 potassium channels to the regulation of vascular tone in early postnatal period. We modeled extracellular metabolic acidosis (pH 6.8, equimolar replacement of NaHCO3 with NaCl in solution) and studied isometric contractile responses of the saphenous artery in rats aged 3–4 months and rat pups aged 12–15 days. Arterial contraction to the α1-adrenergic agonist methoxamine at pH 6.8 was reduced compared to normal pH 7.4 in both 3–4-month-old and 12–15-day-old rats. The KATP channel blocker glibenclamide did not change the arterial responses to methoxamine, neither at pH 7.4 nor at pH 6.8 in any of the age groups. The TASK-1 channel blocker AVE1231 did not alter arterial contractile responses at any pH in 3–4-month-old rats. However, in 12–15-day-old rat pups, the increase in contractile responses to methoxamine under the influence of AVE1231 was less at pH 6.8 than at pH 7.4. Thus, the results of this work demonstrate that acidosis reduces the contractile activity of the arteries of 3–4-month-old animals and animals during early postnatal ontogenesis, while in the latter, the anticontractile role of TASK-1 channels decreases, and KATP channels do not affect the regulation of vascular tone, either under normal, or at acidic pH in any of the age groups.

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About the authors

A. A. Shvetsova

Lomonosov Moscow State University

Author for correspondence.
Email: Dina.Gaynullina@gmail.com
Russian Federation, Moscow

A. A. Borzykh

Institute of Biomedical Problems of the Russian Academy of Sciences; Lomonosov Moscow State University

Email: Dina.Gaynullina@gmail.com
Russian Federation, Moscow; Moscow

D. K. Gaynullin

Lomonosov Moscow State University

Email: Dina.Gaynullina@gmail.com
Russian Federation, Moscow

References

  1. Berend K, de Vries APJ, Gans ROB (2014) Physiological Approach to Assessment of Acid–Base Disturbances. N Engl J Med 371: 1434–1445. https://doi.org/10.1056/NEJMRA1003327/SUPPL_FILE/NEJMRA1003327_DISCLOSURES.PDF
  2. Гайнуллина ДК, Швецова АА, Тарасова ОС (2022) Механизмы влияния ацидоза на тонус кровеносных сосудов. Авиакосмич экологич мед 56: 38–45. [Gainullina DK, Shvetso- va AA, Tarasova OS (2022) Mechanisms of the influence of acidosis on the tone of blood vessels. Aerospace Environment Med 56: 38–45. (In Russ)]. https://doi.org/10.21687/0233-528x-2022-56-5-38-45
  3. Gaynullina DK, Tarasova OS, Shvetsova AA, Borzykh AA, Schubert R (2022) The Effects of Acidosis on eNOS in the Systemic Vasculature: A Focus on Early Postnatal Ontogenesis. Int J Mol Sci 23: 5987. https://doi.org/10.3390/ijms23115987
  4. Boedtkjer E, Aalkjaer C (2012) Intracellular pH in the resistance vasculature: regulation and functional implications. J Vasc Res 49: 479–496. https://doi.org/10.1159/000341235
  5. Boedtkjer E (2018) Acid–base regulation and sensing: Accelerators and brakes in metabolic regulation of cerebrovascular tone. J Cereb Blood Flow Metab 38: 588–602. https://doi.org/10.1177/0271678X17733868
  6. Remzső G, Németh J, Varga V, Kovács V, Tóth-Szűki V, Kaila K, Voipio J, Domoki F (2020) Brain interstitial pH changes in the subacute phase of hypoxic-ischemic encephalopathy in newborn pigs. PLoS One 15: e0233851. https://doi.org/10.1371/journal.pone.0233851
  7. Shvetsova AA, Gaynullina DK, Tarasova OS, Schubert R (2019) Negative feedback regulation of vasocontraction by potassium channels in 10- to 15-day-old rats: Dominating role of Kv7 channels. Acta Physiol 225: e13176. https://doi.org/10.1111/apha.13176
  8. Wang X, Wu J, Li L, Chen F, Wang R, Jiang C (2003) Hypercapnic acidosis activates KATP channels in vascular smooth muscles. Circ Res 92: 1225–1232. https://doi.org/10.1161/01.RES.0000075601.95738.6D
  9. Celotto AC, Restini CBA, Capellini VK, Bendhack LM, Evora PRB (2011) Acidosis induces relaxation mediated by nitric oxide and potassium channels in rat thoracic aorta. Eur J Pharmacol 656: 88–93. https://doi.org/10.1016/j.ejphar.2011.01.053
  10. Lindauer U, Vogt J, Schuh-Hofer S, Dreier JP, Dirnagl U (2003) Cerebrovascular Vasodilation to Extraluminal Acidosis Occurs via Combined Activation of ATP-Sensitive and Ca 2+-Activated Potassium Channels. J Cereb Blood Flow Metab 23(10): 1227–1238. https://doi.org/10.1097/01.WCB.0000088764.02615.B7
  11. Rohra DK, Sharif HM, Zubairi HS, Sarfraz K, Ghayur MN, Gilani AH (2005) Acidosis-induced relaxation of human internal mammary artery is due to activation of ATP-sensitive potassium channels. Eur J Pharmacol 514: 175–181. https://doi.org/10.1016/j.ejphar.2005.02.041
  12. Phillis JW, Song D, O’Regan MH (2000) Mechanisms involved in coronary artery dilatation during respiratory acidosis in the isolated perfused rat heart. Basic Res Cardiol 95: 93–97. https://doi.org/10.1007/s003950050169
  13. Gurney A, Manoury B (2009) Two-pore potassium channels in the cardiovascular system. Eur Biophys J 38: 305–318. https://doi.org/10.1007/s00249-008-0326-8
  14. Goldstein SAN, Bockenhauer D, O’Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-p-domain subunits. Nat Rev Neurosci 23(2): 175–184. https://doi.org/10.1038/35058574
  15. Olschewski A, Li Y, Tang B, Hanze J, Eul B, Bohle RM, Wilhelm J, Morty RE, Brau ME, Weir EK, Kwapiszewska G, Klepetko W, Seeger W, Olschewski H (2006) Impact of TASK-1 in human pulmonary artery smooth muscle cells. Circ Res 98: 1072–1080. https://doi.org/10.1161/01.RES.0000219677.12988.e9
  16. Antigny F, Hautefort A, Meloche J, Belacel-Ouari M, Manoury B, Rucker-Martin C, Péchoux C, Potus F, Nadeau V, Tremblay E, Ruffenach G, Bourgeois A, Dorfmüller P, Breuils-Bonnet S, Fadel E, Ranchoux B, Jourdon P, Girerd B, Montani D, Provencher S, Bonnet S, Simonneau G, Humbert M, Perros F (2016) Potassium channel subfamily K member 3 (KCNK3) contributes to the development of pulmonary arterial hypertension. Circulation 133: 1371–1385. https://doi.org/10.1161/CIRCULATIONAHA.115.020951
  17. Gardener MJ, Johnson IT, Burnham MP, Edwards G, Heagerty AM, Weston AH (2004) Functional evidence of a role for two-pore domain potassium channels in rat mesenteric and pulmonary arteries. Br J Pharmacol 142: 192–202. https://doi.org/10.1038/sj.bjp.0705691
  18. Shvetsova AA, Gaynullina DK, Schmidt N, Bugert P, Lukoshkova E V, Tarasova OS, Schubert R (2020) TASK-1 channel blockade by AVE1231 increases vasocontractile responses and BP in 1- to 2-week-old but not adult rats. Br J Pharmacol 177: 5148–5162. https://doi.org/10.1111/bph.15249
  19. Stulcova B (1977) Postnatal development of cardiac output distribution measured by radioactive microspheres in rats. Neonatology 32: 119–124.
  20. Mulvany MJ, Halpern W (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41: 19–26. https://doi.org/10.1161/01.RES.41.1.19
  21. Yartsev VN, Karachentseva OV, Dvoretsky DP (2002) Effect of pH changes on reactivity of rat mesenteric artery segments at different magnitude of stretch. Acta Physiol Scand 174: 1–7. https://doi.org/10.1046/j.1365-201x.2002.00923.x
  22. Mohanty I, Suklabaidya S, Parija SC (2016) Acidosis reduces the function and expression of α1D-adrenoceptor in superior mesenteric artery of capra hircus. Int J Pharmacol 48: 399–406. https://doi.org/10.4103/0253-7613.186199
  23. Aoyama Y, Ueda K, Setogawa A, Kawai Y (1999) Effects of pH on contraction and Ca2+ mobilization in vascular smooth muscles of the rabbit basilar artery. Jpn J Physiol 49: 55–62.
  24. Akanji O, Weinzierl N, Schubert R, Schilling L (2019) Acid sensing ion channels in rat cerebral arteries: Probing the expression pattern and vasomotor activity. Life Sci 227: 193–200. https://doi.org/10.1016/j.lfs.2019.04.054
  25. Aleksandrowicz M, Kozniewska E (2020) Compromised regulation of the rat brain parenchymal arterioles in vasopressin-associated acute hyponatremia. Microcirculation 27: 1–7. https://doi.org/10.1111/micc.12644
  26. Hessellund A, Aalkjaer C, Bek T (2006) Effect of acidosis on isolated porcine retinal vessels. Curr Eye Res 31: 427–434. https://doi.org/10.1080/02713680600681236
  27. Ives SJ, Andtbacka RHI, Noyes RD, Morgan RG, Gifford JR, Park SY, Symons JD, Richard- son RS (2013) α1-Adrenergic responsiveness in human skeletal muscle feed arteries: The impact of reducing extracellular pH. Exp Physiol 98: 256–267. https://doi.org/10.1113/expphysiol.2012.066613
  28. Nakanishi T, Gu H, Momma K (1997) Developmental changes in the effect of acidosis on contraction, intracellular pH, and calcium in the rabbit mesenteric small artery. Pediatr Res 42: 750–757. https://doi.org/10.1203/00006450-199712000-00006
  29. Nakanishi T, Gu H, Momma K (1997) Effect of acidosis on contraction, intracellular pH, and calcium in the newborn and adult rabbit aorta. Heart Vessels 12: 207–215. https://doi.org/10.1007/BF02766785
  30. Lotshaw DP (2007) Biophysical, pharmacological, and functional characteristics of cloned and native mammalian two-pore domain K+ hannels. Cell Biochem Biophys 47(2): 209–256. https://doi.org/10.1007/s12013-007-0007-8
  31. Ma L, Zhang X, Zhou M, Chen H (2012) Acid-sensitive TWIK and TASK Two-pore Domain Potassium Channels Change Ion Selectivity and Become Permeable to Sodium in Extracellular Acidification. J Biol Chem 287(44): 37145–37153. https://doi.org/10.1074/jbc.M112.398164
  32. Mochalov SV, Tarasova NV, Kudryashova TV, Gaynullina DK, Kalenchuk VU, Borovik AS, Vorotnikov AV, Tarasova OS, Schubert R (2018) Higher Ca2+-sensitivity of arterial contraction in 1-week-old rats is due to a greater Rho-kinase activity. Acta Physiol 223: 1–15. https://doi.org/10.1111/apha.13044
  33. Akopov SE, Zhang L, Pearce WJ (1998) Regulation of Ca2+ sensitization by PKC and rho proteins in ovine cerebral arteries: Effects of artery size and age. Am J Physiol - Hear Circ Physiol 275: 930–939. https://doi.org/10.1152/ajpheart.1998.275.3.h930
  34. Boedtkjer E, Praetorius J, Matchkov VV, Stankevicius E, Mogensen S, Füchtbauer AC, Simon- sen U, Füchtbauer EM, Aalkjaer C (2011) Disruption of Na+, HCO2- cotransporter NBCn1 (slc4a7) Inhibits no-mediated vasorelaxation, smooth muscle Ca2+ Sensitivity, and hypertension development in mice. Circulation 124: 1819–1829. https://doi.org/10.1161/CIRCULATIONAHA.110.015974

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2. Fig. 1. Effect of extracellular acidosis (pH 6.8) on contractile responses of the saphenous artery to methoxamine in rats aged 3–4 months (a) and 12–15 days (b). The numbers in brackets indicate the number of animals in the group. * p < 0.05 (two-way ANOVA for repeated measures).

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3. Fig. 2. Effect of the KATP channel blocker glibenclamide on the contractile responses of the saphenous artery to methoxamine in rats aged 3–4 months at pH 7.4 (a) and pH 6.8 (b). The numbers in brackets indicate the number of animals in the group.

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4. Fig. 3. Effect of the KATP channel blocker glibenclamide on the contractile responses of the saphenous artery to methoxamine in 12–15-day-old rat pups at pH 7.4 (a) and pH 6.8 (b). The numbers in brackets indicate the number of animals in the group.

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5. Fig. 4. Effect of the TASK-1 channel blocker AVE1231 on the contractile responses of the saphenous artery to methoxamine in rats aged 3–4 months at pH.

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6. Fig. 5. Effect of the TASK-1 channel blocker AVE1231 on the contractile responses of the saphenous artery to methoxamine in 12–15-day-old rat pups at pH 7.4 (a) and pH 6.8 (b). The numbers in brackets indicate the number of animals in the group. * p < 0.05 (two-way ANOVA for repeated measures). 7.4 (a) and pH 6.8 (b). The numbers in brackets indicate the number of animals in the group.

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