Morphine-induced delayed pre-conditioning against anoxia/reoxygenation injury in pulmonary artery endothelial cells: The role of mitochondrial KATP channels Retraction in /10.3892/mmr.2023.13030

Ding,Wengang; Guo,Yueping; Cui,Xiaoguang; Zhang,Bing; Li,Dongmei; Li,Wenzhi

doi:10.3892/mmr.2015.4629

Morphine-induced delayed pre-conditioning against anoxia/reoxygenation injury in pulmonary artery endothelial cells: The role of mitochondrial KATP channels

Retraction in: /10.3892/mmr.2023.13030

Authors:
- Wengang Ding
- Yueping Guo
- Xiaoguang Cui
- Bing Zhang
- Dongmei Li
- Wenzhi Li
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Affiliations: Department of Anesthesiology, The Second Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150086, P.R. China
Published online on: November 30, 2015 https://doi.org/10.3892/mmr.2015.4629
Pages: 1047-1053

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Abstract

Opioids produce delayed pre-conditioning (PC) in vivo and in vitro. Our previous research revealed that opioid‑induced delayed PC has an antiapoptotic effect on pulmonary artery endothelial cells (PAECs) suffering from anoxia/reoxygenation (A/R) injury. The present study hypothesized that activation of endothelial mitochondrial ATP‑sensitive potassium (KATP) channels may result in antiapoptotic effects and against dysfunction in PAECs. Cultured porcine PAECs underwent 16 h anoxia treatment, followed by 1 h reoxygenation, which occurred 24 h following pretreatment with saline (0.9% NaCl; w/v) or morphine (1 µM). To determine the underlying mechanism, a selective mitochondrial KATP inhibitor, 5‑hydroxydecanoic acid (5‑HD; 100 µM), and an opioid receptor antagonist, naloxone (Nal; 10 µM), were administered 30 min prior to the A/R load. The percentage of apoptotic cells was assessed by Annexin V‑fluorescein isothiocyanate staining, using a fluorescence‑activated cell sorter. The mRNA expression of intercellular cell adhesion molecule‑1 (ICAM‑1) was measured by reverse transcription‑quantitative polymerase chain reaction. The endothelin‑1 (ET‑1) content in the supernatant of PAECs cultures was estimated by radioimmunoassay. Compared with the control, A/R caused the apoptosis of PAECs, release of ET‑1 and increased mRNA expression of ICAM‑1. Morphine‑induced delayed PC significantly reduced PAEC apoptosis, increased the release of ET‑1 and reduced the mRNA expression of ICAM‑1 by ~1.7‑times, compared with A/R. The protective effect of morphine was abolished by pretreatment with 5‑HD and Nal, however, the two agents themselves failed to aggravate the A/R injury. These results suggested that morphine-induced delayed PC has a protective effect during A/R injury of PAECs. This effect may be mediated by mitochondrial KATP channels and is opioid receptor-dependent.

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1	Tan J, Liu D, Lv X, Wang L, Zhao C, Che Y, Xie Q and Cui X: MAPK mediates inflammatory response and cell death in rat pulmonary microvascular endothelial cells in an ischemia-reperfusion model of lung transplantation. J Heart Lung Transplant. 32:823–831. 2013. View Article : Google Scholar : PubMed/NCBI
2	Davenpeck KL, Guo JP and Lefer AM: Pulmonary artery endothelial dysfunction following ischemia and reperfusion of the rabbit lung. J Vasc Res. 30:145–153. 1993. View Article : Google Scholar : PubMed/NCBI
3	Yaoita H, Ogawa K, Maehara K and Maruyama Y: Attenuation of ischemia/reperfusion injury in rats by a caspase inhibitor. Circulation. 97:276–281. 1998. View Article : Google Scholar : PubMed/NCBI
4	Qiu J, Li W, Feng S, Wang M and He Z: Transplantation of bone marrow-derived endothelial progenitor cells attenuates cerebral ischemia and reperfusion injury by inhibiting neuronal apoptosis, oxidative stress and nuclear factor-κB expression. Int J Mol Med. 31:91–98. 2013.
5	Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, Davis RJ, Choi AM and Lee PJ: Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem. 278:1248–1258. 2003. View Article : Google Scholar
6	Byrne CJ, McCafferty K, Kieswich J, Harwood S, Andrikopoulos P, Raftery M, Thiemermann C and Yaqoob MM: Ischemic conditioning protects the uremic heart in a rodent model of myocardial infarction. Circulation. 125:1256–1265. 2012. View Article : Google Scholar : PubMed/NCBI
7	Downey JM, Davis AM and Cohen MV: Signaling pathways in ischemic pre-conditioning. Heart Fail Rev. 12:181–188. 2007. View Article : Google Scholar : PubMed/NCBI
8	Dragasis S, Bassiakou E, Iacovidou N, Papadimitriou L, Andreas Steen P, Gulati A and Xanthos T: The role of opioid receptor agonists in ischemic pre-conditioning. Eur J Pharmacol. 720:401–408. 2013. View Article : Google Scholar : PubMed/NCBI
9	Barrère-Lemaire S, Combes N, Sportouch-Dukhan C, Richard S, Nargeot J and Piot C: Morphine mimics the antiapoptotic effect of pre-conditioning via an Ins (1,4,5) P3 signaling pathway in rat ventricular myocytes. Am J Physiol Heart Circ Physiol. 288:H83–H88. 2005. View Article : Google Scholar
10	Beheshtian A, Demehri S, Kiumehr S, Salmasi AH, Nezami BG, Rahimpour S, Amanpour S, Rabbani S, Mohagheghi MA and Dehpour AR: ATP-sensitive potassium channels mediate the anti-ischemic properties of ischemic and pharmacologic pre-conditioning in rat random-pattern skin flap. Ann Plast Surg. 57:94–99. 2006. View Article : Google Scholar : PubMed/NCBI
11	Nogueira MA, Coelho AM, Sampietre SN, Patzina RA, Pinheiro da Silva F, D'Albuquerque LA and Machado MC: Beneficial effects of adenosine triphosphate-sensitive K(+) channel opener on liver ischemia/reperfusion injury. World J Gastroenterol. 20:15319–15326. 2014. View Article : Google Scholar : PubMed/NCBI
12	Gaskin FS, Kamada K, Yusof M, Durante W, Gross G and Korthuis RJ: AICAR pre-conditioning prevents postischemic leukocyte rolling and adhesion: Role of K(ATP) channels and heme oxygenase. Microcirculation. 16:167–176. 2009. View Article : Google Scholar : PubMed/NCBI
13	Simerabet M, Robin E, Aristi I, Adamczyk S, Tavernier B, Vallet B, Bordet R and Lebuffe G: Preconditioning by an in situ administration of hydrogen peroxide: Involvement of reactive oxygen species and mitochondrial ATP-dependent potassium channel in a cerebral ischemia-reperfusion model. Brain Res. 1240:177–184. 2008. View Article : Google Scholar : PubMed/NCBI
14	Grossini E, Molinari C, Pollesello P, Bellomo G, Valente G, Mary D, Vacca G and Caimmi P: Levosimendan protection against kidney ischemia/reperfusion injuries in anesthetized pigs. J Pharmacol Exp Ther. 342:376–388. 2012. View Article : Google Scholar : PubMed/NCBI
15	Busija DW and Katakam PV: Mitochondrial mechanisms in cerebral vascular control: Shared signaling pathways with pre-conditioning. J Vasc Res. 51:175–189. 2014. View Article : Google Scholar :
16	Fryer RM, Hsu AK, Eells JT, Nagase H and Gross GJ: Opioid-induced second window of cardioprotection: Potential role of mitochondrial KATP channels. Circ Res. 84:846–851. 1999. View Article : Google Scholar : PubMed/NCBI
17	Wang H, Long C, Duan Z, Shi C, Jia G and Zhang Y: A new ATP-sensitive potassium channel opener protects endothelial function in cultured aortic endothelial cells. Cardiovasc Res. 73:497–503. 2007. View Article : Google Scholar
18	Date T, Taniguchi I, Inada K, Matsuo S, Miyanaga S, Yamane T, Abe Y, Sugimoto K and Mochizuki S: Nicorandil inhibits serum starvation-induced apoptosis in vascular endothelial cells. J Cardiovasc Pharmacol. 46:721–726. 2005. View Article : Google Scholar : PubMed/NCBI
19	Block ER and Edwards D: Effect of plasma membrane fluidity on serotonin transport by endothelial cells. Am J Physiol. 253:C672–C678. 1987.PubMed/NCBI
20	Block ER, Patel JM, Angelides KJ, Sheridan NP and Garg LC: Hyperoxia reduces plasma membrane fluidity: A mechanism for endothelial cell dysfunction. J Appl Physiol (1985). 60:826–835. 1986.
21	Zhao P, Huang Y and Zuo Z: Opioid pre-conditioning induces opioid receptor-dependent delayed neuroprotection against ischemia in rats. J Neuropathol Exp Neurol. 65:945–952. 2006. View Article : Google Scholar : PubMed/NCBI
22	Ding WG, Zhou HC, Cui XG, Li WZ, Guo YP, Zhang B and Liu W: Anti-apoptotic effect of morphine-induced delayed pre-conditioning on pulmonary artery endothelial cells with anoxia/reoxygenation injury. Chin Med J (Engl). 121:1313–1318. 2008.
23	Kim SJ, Zhang X, Xu X, Chen A, Gonzalez JB, Koul S, Vijayan K, Crystal GJ, Vatner SF and Hintze TH: Evidence for enhanced eNOS function in coronary microvessels during the second window of protection. Am J Physiol Heart Circ Physiol. 292:H2152–H2158. 2007. View Article : Google Scholar : PubMed/NCBI
24	Frässdorf J, Weber NC, Obal D, Toma O, Müllenheim J, Kojda G, Preckel B and Schlack W: Morphine induces late cardioprotection in rat hearts in vivo: The involvement of opioid receptors and nuclear transcription factor kappaB. Anesth Analg. 101:934–941. 2005. View Article : Google Scholar : PubMed/NCBI
25	Serizawa K, Yogo K, Tashiro Y, Aizawa K and Ishizuka N: GATA-4 transcription factor regulates cardiac COX-2 expression induced by nicorandil in left ventricle of rats. Pharmacology. 93:129–136. 2014. View Article : Google Scholar : PubMed/NCBI
26	Swyers T, Redford D and Larson DF: Volatile anesthetic-induced pre-conditioning. Perfusion. 29:10–15. 2014. View Article : Google Scholar
27	Noma A: ATP-regulated K+ channels in cardiac muscle. Nature. 305:147–148. 1983. View Article : Google Scholar : PubMed/NCBI
28	Dos Santos P, Kowaltowski AJ, Laclau MN, Seetharaman S, Paucek P, Boudina S, Thambo JB, Tariosse L and Garlid KD: Mechanisms by which opening the mitochondrial ATP- sensitive K(+) channel protects the ischemic heart. Am J Physiol Heart Circ Physiol. 283:H284–H295. 2002. View Article : Google Scholar : PubMed/NCBI
29	Lai VK and Galiñanes M: Protection of human myocardium by bone marrow cells: Role of long-term administration of the mitochondrial K (ATP) channel opener nicorandil. J Surg Res. 171:66–70. 2011. View Article : Google Scholar
30	Teshima Y, Akao M, Baumgartner WA and Marbán E: Nicorandil prevents oxidative stress-induced apoptosis in neurons by activating mitochondrial ATP-sensitive potassium channels. Brain Res. 990:45–50. 2003. View Article : Google Scholar : PubMed/NCBI
31	Yu Y, Xiao Y, Wang H, Li J, Zuo X, Wang H and Xie W: Protective effect of nicorandil on hypoxia-induced apoptosis in HPAECs through inhibition of p38 MAPK phosphorylation. Mol Med Rep. 7:816–820. 2013.PubMed/NCBI
32	Duda M, Czarnowska E, Kurzelewski M, Konior A and Beresewicz A: Ischemic pre-conditioning prevents endothelial dysfunction, P-selectin expression and neutrophil adhesion by preventing endothelin and O₂-generation in the post-ischemic guinea-pig heart. J Physiol Pharmacol. 57:553–569. 2006.
33	Chen W, Zheng G, Yang S, Ping W, Fu X, Zhang N, Wang DW and Wang J: CYP2J2 and EETs Protect against Oxidative Stress and Apoptosis in Vivo and in Vitro Following Lung Ischemia/Reperfusion. Cell Physiol Biochem. 33:1663–1680. 2014. View Article : Google Scholar : PubMed/NCBI
34	Sato Y, Hogg JC, English D and van Eeden SF: Endothelin-1 changes polymorphonuclear leukocytes' deform-ability and CD11b expression and promotes their retention in the lung. Am J Respir Cell Mol Biol. 23:404–410. 2000. View Article : Google Scholar : PubMed/NCBI