Propofol Causes Sustained Ca2+ Elevation in Endothelial Cells by Stimulating Ryanodine Receptor and Suppressing Plasmalemmal Ca2+ Pump.
Journal
Journal of cardiovascular pharmacology
ISSN: 1533-4023
Titre abrégé: J Cardiovasc Pharmacol
Pays: United States
ID NLM: 7902492
Informations de publication
Date de publication:
01 05 2022
01 05 2022
Historique:
received:
25
09
2021
accepted:
23
01
2022
pubmed:
4
3
2022
medline:
11
5
2022
entrez:
3
3
2022
Statut:
epublish
Résumé
Propofol, a general anesthetic administered intravenously, may cause pain at the injection site. The pain is in part due to irritation of vascular endothelial cells. We here investigated the effects of propofol on Ca2+ transport and pain mediator release in human umbilical vein endothelial cells (EA.hy926). Propofol mobilized Ca2+ from cyclopiazonic acid (CPA)-dischargeable pool but did not cause Ca2+ release from the lysosomal Ca2+ stores. Propofol-elicited Ca2+ release was suppressed by 100 μM ryanodine, suggesting the participation of ryanodine receptor channels. Propofol did not affect ATP-triggered Ca2+ release but abolished the Ca2+ influx triggered by ATP; in addition, propofol also suppressed store-operated Ca2+ entry elicited by CPA. Ca2+ clearance during CPA-induced Ca2+ discharge was unaffected by a low Na+ (50 mM) extracellular solution, but strongly suppressed by 5 mM La3+ (an inhibitor of plasmalemmal Ca2+ pump), suggesting Ca2+ extrusion was predominantly through the plasmalemmal Ca2+ pump. Propofol mimicked the effect of La3+ in suppressing Ca2+ clearance. Propofol also stimulated release of pain mediators, namely, reactive oxygen species and bradykinin. Our data suggest propofol elicited Ca2+ release and repressed Ca2+ clearance, causing a sustained cytosolic [Ca2+]i elevation. The latter may cause reactive oxygen species and bradykinin release, resulting in pain.
Identifiants
pubmed: 35239284
doi: 10.1097/FJC.0000000000001246
pii: 00005344-202205000-00019
doi:
Substances chimiques
Reactive Oxygen Species
0
Ryanodine Receptor Calcium Release Channel
0
Ryanodine
15662-33-6
Adenosine Triphosphate
8L70Q75FXE
Bradykinin
S8TIM42R2W
Calcium
SY7Q814VUP
Propofol
YI7VU623SF
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
749-757Informations de copyright
Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.
Déclaration de conflit d'intérêts
The authors report no conflicts of interest.
Références
Bali M, Akabas MH. Defining the propofol binding site location on the GABA A receptor. Mol Pharmacol. 2004;65:68–76.
Kobayashi M, Oi Y. Actions of propofol on neurons in the cerebral cortex. J Nippon Med Sch. 2017;84:165–169.
Wang Y, Yang E, Wells MM, et al. Propofol inhibits the voltage-gated sodium channel NaChBac at multiple sites. J Gen Physiol. 2018;150:1317–1331.
Ellermann C, Könemann H, Wolfes J, et al. Propofol abolishes torsade de pointes in different models of acquired long QT syndrome. Sci Rep. 2020;10:12133.
Deng F, Wang S, Zhang L, et al. Propofol through upregulating caveolin-3 attenuates post-hypoxic mitochondrial damage and cell death in H9C2 cardiomyocytes during hyperglycemia. Cell Physiol Biochem. 2017;44:279–292.
Zhang L, Wang J, Liang J, et al. Propofol prevents human umbilical vein endothelial cell injury from Ang II-induced apoptosis by activating the ACE2-(1-7)-Mas axis and eNOS phosphorylation. PLoS One. 2018;13:e0199373.
Zhu M, Chen J, Tan Z, et al. Propofol protects against high glucose-induced endothelial dysfunction in human umbilical vein endothelial cells. Anesth Analg. 2012;114:303–309.
Gragasin FS, Davidge ST. The effects of propofol on vascular function in mesenteric arteries of the aging rat. Am J Physiol Heart Circ Physiol. 2009;297:H466–H474.
Chang KS, Davis RF. Propofol produces endothelium-independent vasodilation and may act as a Ca2+ channel blocker. Anesth Analg. 1993;76:24–32.
Yamanoue T, Brum JM, Estafanous FG. Vasodilation and mechanism of action of propofol in porcine coronary artery. Anesthesiology. 1994;81:443–451.
Zhang G, Cui J, Chen Y, et al. The relaxant effect of propofol on isolated rat intrapulmonary arteries. Korean J Physiol Pharmacol. 2014;18:377–381.
Yu J, Kakutani T, Mizumoto K, et al. Propofol inhibits phorbol 12, 13-dibutyrate-induced, protein kinase C-mediated contraction of rat aortic smooth muscle. Acta Anaesthesiol Scand. 2006;50:1131–1138.
Wang Y, Zhou Q, Wu B, et al. Propofol induces excessive vasodilation of aortic rings by inhibiting protein kinase Cbeta2 and teta in spontaneously hypertensive rats. Br J Pharmacol. 2017;174:1984–2000.
Wang B, Luo T, Chen D, et al. Propofol reduces apoptosis and up-regulates endothelial nitric oxide synthase protein expression in hydrogen peroxide-stimulated human umbilical vein endothelial cells. Anesth Analg. 2007;105:1027–1033.
Wang L, Wu B, Sun Y, et al. Translocation of protein kinase C isoforms is involved in propofol-induced endothelial nitric oxide synthase activation. Br J Anaesth. 2010;104:606–612.
Scott RP, Saunders DA, Norman J. Propofol: clinical strategies for preventing the pain of injection. Anaesthesia. 1988;43:492–494.
Tan CH, Onsiong MK. Pain on injection of propofol. Anaesthesia. 1998;53:468–476.
Secor T, Safadi AO, Gunderson S. Propofol Toxicity. StatPearls Treasure Island, FL: StatPearls Publishing; 2020.
Leung YM, Huang CF, Chao CC, et al. Voltage-gated K+ channels play a role in cAMP-stimulated neuritogenesis in mouse neuroblastoma N2A cells. J Cel Physiol. 2011;226:1090–1098.
Atakpa P, Thillaiappan NB, Mataragka S, et al. IP3 receptors preferentially associate with ER-lysosome contact sites and selectively deliver Ca2+ to lysosomes. Cell Rep. 2018;25:3180–3193.
Patel S. Getting close. Lysosome-ER contact sites tailor Ca2+ signals. Cell Calcium. 2019;80:194–196.
Zuccolo E, Kheder DA, Lim D, et al. Glutamate triggers intracellular Ca2+ oscillations and nitric oxide release by inducing NAADP- and InsP3 -dependent Ca2+ release in mouse brain endothelial cells. J Cel Physiol. 2019;234:3538–3554.
Mantz J, Delumeau JC, Cordier J, et al. Differential effects of propofol and ketamine on cytosolic calcium concentrations of astrocytes in primary culture. Br J Anaesth. 1994;72:351–353.
Björnström K, Sjölander A, Schippert A, et al. A tyrosine kinase regulates propofol-induced modulation of the beta-subunit of the GABA(A) receptor and release of intracellular calcium in cortical rat neurones. Acta Physiol Scand. 2002;175:227–235.
Liang WZ, Jan CR, Lu CH. Investigation of 2,6-diisopropylphenol (propofol)-evoked Ca2+ movement and cell death in human glioblastoma cells. Toxicol Vitro. 2012;26:862–871.
Yang M, Wang Y, Liang G, et al. Alzheimer's disease presenilin-1 mutation sensitizes neurons to impaired autophagy flux and propofol neurotoxicity: role of calcium dysregulation. J Alzheimers Dis. 2019;67:137–147.
Urabe T, Yanase Y, Motoike S, et al. Propofol induces the elevation of intracellular calcium via morphological changes in intracellular organelles, including the endoplasmic reticulum and mitochondria. Eur J Pharmacol. 2020;884:173303.
Fruen BR, Mickelson JR, Roghair TJ, et al. Effects of propofol on Ca2+ regulation by malignant hyperthermia-susceptible muscle membranes. Anesthesiology. 1995;82:1274–1282.
Imura N, Shiraishi Y, Katsuya H, et al. Effect of propofol on norepinephrine-induced increases in [Ca2+]i and force in smooth muscle of the rabbit mesenteric resistance artery. Anesthesiology. 1998;88:1566–1578.
Tai YT, Wu CC, Wu GJ, et al. Study of propofol in bovine aortic endothelium: I. Inhibitory effect on bradykinin-induced intracellular calcium immobilization. Acta Anaesthesiol Sin. 2000;38:181–186.
Zhong H, Song R, Pang Q, et al. Propofol inhibits parthanatos via ROS-ER-calcium-mitochondria signal pathway in vivo and vitro. Cell Death Dis. 2018;9:932.
Ya Deau JT, Morelli CM, Desravines S. Inhibition by propofol of intracellular calcium mobilization in cultured mouse pituitary cells. Anesth Analg. 2003;97:1325–1330.
Nagase Y, Kaibara M, Uezono Y, et al. Propofol inhibits muscarinic acetylcholine receptor-mediated signal transduction in Xenopus Oocytes expressing the rat M1 receptor. Jpn J Pharmacol. 1999;79:319–325.
Samain E, Bouillier H, Marty J, et al. The effect of propofol on angiotensin II-induced Ca(2+) mobilization in aortic smooth muscle cells from normotensive and hypertensive rats. Anesth Analg. 2000;90:546–552.
Horibe M, Kondo I, Damron DS, et al. Propofol attenuates capacitative calcium entry in pulmonary artery smooth muscle cells. Anesthesiology. 2001;95:681–688.
Shimizu S, Ding X, Murray PA. Intravenous anesthetics inhibit capacitative calcium entry in pulmonary venous smooth muscle cells. Anesthesiology. 2006;104:791–797.
Grim KJ, Abcejo AJ, Barnes A, et al. Caveolae and propofol effects on airway smooth muscle. Br J Anaesth. 2012;109:444–453.
Lopez MM, Kosk-Kosicka D. Entropy-driven interactions of anesthetics with membrane proteins. Biochemistry. 1997;36:8864–8872.
Blaes N, Girolami JP. Targeting the “Janus face” of the B2-bradykinin receptor. Expert Opin Ther Targets. 2013;17:1145–1166.
Kallenborn-Gerhardt W, Schröder K, Geisslinger G, et al. NOXious signaling in pain processing. Pharmacol Ther. 2013;137:309–317.
Zhang X, Scicli GA, Xu X, et al. Role of endothelial kinins in control of coronary nitric oxide production. Hypertension. 1997;30:1105–1111.
Seyedi N, Nasjletti A, Xu X, et al. A23187 induced calcium influx is a co-factor for local kinin formation and not NO synthase in coronary microvessels. Circulation. 1994;90(suppl 1):1–105. Abstract.
Görlach A, Bertram K, Hudecova S, et al. Calcium and ROS: a mutual interplay. Redox Biol. 2015;6:260–271.
Wu KC, Wong KL, Shiao LR, et al. Perturbation of Ca 2+ stores and store-operated Ca 2+ influx by lidocaine in neuronal N2A and NG108-15 cells. Eur J Pharmacol. 2021;904:174115.