Specific microRNAs are involved in the reno‑protective effects of sevoflurane preconditioning and ischemic preconditioning against ischemia reperfusion injury in rats

Yamamoto,Makiko; Morita,Tomonori; Ishikawa,Masashi; Sakamoto,Atsuhiro

doi:10.3892/ijmm.2020.4477

Specific microRNAs are involved in the reno‑protective effects of sevoflurane preconditioning and ischemic preconditioning against ischemia reperfusion injury in rats

Authors:
- Makiko Yamamoto
- Tomonori Morita
- Masashi Ishikawa
- Atsuhiro Sakamoto
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Affiliations: Department of Anesthesiology and Pain Medicine, Graduate School of Medicine, Nippon Medical School, Tokyo 1138602, Japan
Published online on: January 27, 2020 https://doi.org/10.3892/ijmm.2020.4477
Pages: 1141-1149
Copyright: © Yamamoto et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The kidneys are prone to developing ischemia reperfusion injury (IRI) following certain renal surgeries and cardiovascular surgeries requiring cardiac arrest. Sevoflurane and ischemic preconditioning reportedly alleviate IRI, which is mediated via microRNAs. The present study compared anesthetic preconditioning (APC) and ischemic preconditioning (IPC) on microRNAs, which promote cell‑survival pathways in rats in a randomized controlled study. After undergoing right nephrectomy under general anesthesia, male Wistar rats (336±24 g) and were divided into four groups (IRI, APC, IPC and sham; n=7 each). The IRI group underwent 45 min clamping of the left renal vasculature, followed by 4 h of reperfusion. APC involved exposure to one minimum alveolar concentration sevoflurane for 15 min. IPC included three cycles of two‑min clamping and five‑min reperfusion. Blood and renal biopsy samples were assessed postoperatively to measure serum creatinine and to analyze renal microRNA (miR) expression using reverse transcription‑quantitative polymerase chain reaction (RT‑qPCR) testing and their target pathways with Ingenuity Pathway Analysis™. The present study found that serum creatinine values in APC (0.71±0.08 mg/dl) and IPC (0.73±0.1 mg/dl) groups were lower than in the IRI group (0.96±0.13 mg/dl; P<0.05), indicating amelioration of IRI by APC and IPC. RT‑qPCR followed by pathway analysis indicated that APC and IPC affect ‘protein kinase B (Akt)’. APC promoted miR‑17‑3p and suppressed miR‑27a. IPC promoted miR‑19a. All the miRs were predicted to regulate phosphorylated Akt, which promotes cell‑protection. Western blot analysis showed that expression of phosphorylated Akt increased and phosphatase and tensin homologue deleted from chromosome 10 (PTEN) decreased following APC and IPC. The present study concluded that APC and IPC affect different miRs, although they are estimated to similarly promote the PTEN/phosphoinositide 3‑kinase/Akt signaling pathway, resulting in reno‑protection.

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1	Debout A, Foucher Y, Trébern-Launay K, Legendre C, Kreis H, Mourad G, Garrigue V, Morelon E, Buron F, Rostaing L, et al: Each additional hour of cold ischemia time significantly increases the risk of graft failure and mortality following renal transplantation. Kidney Int. 87:343–349. 2015. View Article : Google Scholar
2	Girerd S, Frimat L, Ducloux D, Le Meur Y, Mariat C, Moulin B, Mousson C, Reiu P, Dali-Youcef N, Merckle L, et al: EPURE transplant (eplerenone in patients undergoing renal transplant) study: Study protocol for a randomized controlled trial. Trials. 19:5952018. View Article : Google Scholar : PubMed/NCBI
3	Tonelli M, Wiebe N, Knoll G, Bello A, Browne S, Jadhav D, Klarenbach S and Gill J: Systematic review: Kidney transplantation compared with dialysis in clinically relevant outcomes. Am J Transplant. 11:2093–2109. 2011. View Article : Google Scholar : PubMed/NCBI
4	Lannemyr L, Bragadottir G, Hjärpe A, Redfors B and Ricksten SE: Impact of cardiopulmonary bypass flow on renal oxygenation in patients undergoing cardiac surgery. Ann Thorac Surg. 107:505–511. 2019. View Article : Google Scholar
5	Nadim MK, Forni LG, Bihorac A, Hobson C, Koyner JL, Shaw A, Arnaoutakis GJ, Ding X, Engelman DT, Gasparovic H, et al: Cardiac and vascular surgery-associated acute kidney injury: The 20th international consensus conference of the ADQI (acute disease quality initiative) group. J Am Heart Assoc. 7:e0088342018. View Article : Google Scholar : PubMed/NCBI
6	Eltzschig HK and Eckle T: Ischemia and reperfusion- from mechanism to translation. Nat Med. 17:1391–1401. 2011. View Article : Google Scholar : PubMed/NCBI
7	Eltzschig HK: Targeting hypoxia-induced inflammation. Anesthesiology. 114:239–242. 2011. View Article : Google Scholar : PubMed/NCBI
8	Choi HS, Hwang JK, Kim JG, Hwang HS, Lee SJ, Chang YK, Kim JI and Moon IS: The optimal duration of ischemic preconditioning for renal ischemia-reperfusion injury in mice. Ann Surg Treat Res. 93:209–216. 2017. View Article : Google Scholar : PubMed/NCBI
9	Jang HS, Kim J, Kim KY, Kim JI, Cho MH and Park KM: Previous ischemia and reperfusion injury results in resistance of the kidney against subsequent ischemia and reperfusion insult in mice; a role for the Akt signal pathway. Nephrol Dial Transplant. 27:3762–3770. 2012. View Article : Google Scholar : PubMed/NCBI
10	Liang Y, Li Z, Mo N, Li M, Zhuang Z, Wang J, Wang Y and Guo X: Isoflurane preconditioning ameliorates renal ischemia-reperfusion injury through antiinflammatory and anti-apoptotic actions in rats. Biol Pharm Bull. 37:1599–1605. 2014. View Article : Google Scholar
11	Su MW, Chang SS, Chen CH, Hung CC, Chang SW, Tsai YC and Lam CF: Preconditioning renoprotective effect of isoflurane in a rat model of virtual renal transplant. J Surg Res. 189:135–142. 2014. View Article : Google Scholar : PubMed/NCBI
12	Lempiäinen J, Finckenberg P, Mervaala EE, Storvik M, Lindstedt K, Levijoki J and Mervaala EM: Dexmedetomidine preconditioning ameliorates kidney ischemia-reperfusion injury. Pharmacol Res Perspect. 2:e000452014. View Article : Google Scholar : PubMed/NCBI
13	Lee HT, Chen SW, Doetschman TC, Deng C, D'Agati VD and Kim M: Sevoflurane protects against renal ischemia and reperfusion injury in mice via the transforming growth factor-beta1 pathway. Am J Physiol Renal Physiol. 295:F128–F136. 2008. View Article : Google Scholar : PubMed/NCBI
14	Julier K, da Silva R, Garcia C, Bestmann L, Frascarolo P, Zollinger A, Chassot PG, Schmid ER, Turina MI, von Segesser LK, et al: Preconditioning by sevoflurane decreases biochemical markers for myocardial and renal dysfunction in coronary artery bypass graft surgery: A double-blinded, placebo-controlled, multicenter study. Anesthesiology. 98:1315–1327. 2003. View Article : Google Scholar : PubMed/NCBI
15	Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
16	Godwin JG, Ge X, Stephan K, Jurisch A, Tullius SG and Iacomini J: Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA. 107:14339–14344. 2010. View Article : Google Scholar : PubMed/NCBI
17	Morita T, Ishikawa M and Sakamoto A: Identical microRNAs regulate liver protection during anaesthetic and ischemic preconditioning in rats: An animal study. PLoS One. 10:e01258662015. View Article : Google Scholar : PubMed/NCBI
18	Takayama J, Takaoka M and Matsumura Y: Acute and chronic renal failure model in rats and mice. Nihon Yakurigaku Zasshi. 131:37–42. 2008.In Japanese. View Article : Google Scholar : PubMed/NCBI
19	Liu L, Pang XL, Shang WJ, Xie HC, Wang JX and Feng GW: Over-expressed microRNA-181a reduces glomerular sclerosis and renal tubular epithelial injury in rats with chronic kidney disease via down-regulation of the TLR/NF-κB pathway by binding to CRY1. Mol Med. 24:492018. View Article : Google Scholar
20	Ishikawa M, Tanaka S, Arai M, Genda Y and Sakamoto A: Differences in microRNA changes of healthy rat liver between sevoflurane and propofol anesthesia. Anesthesiology. 117:1245–1252. 2012. View Article : Google Scholar : PubMed/NCBI
21	Luan Y, Chen M and Zhou L: miR-17 targets PTEN and facilitates glial scar formation after spinal cord injuries via the PI3K/Akt/mTOR pathway. Brain Res Bull. 128:68–75. 2017. View Article : Google Scholar
22	Sun G, Lu Y, Li Y, Mao J, Zhang J, Jin Y, Sun Y, Liu L and Li L: miR-19a protects cardiomyocytes from hypoxia/reoxygenation-induced apoptosis via PTEN/PI3K/p-Akt pathway. Biosci Rep. 37:BSR201708992017. View Article : Google Scholar :
23	Liu G, Cao P, Chen H, Yuan W, Wang J and Tang X: miR-27a regulates apoptosis in nucleus pulposus cells by targeting PI3K. PLoS One. 8:e752512013. View Article : Google Scholar : PubMed/NCBI
24	Han J, Xuan JL, Hu HR and Chen ZW: Protective effect against myocardial ischemia reperfusion injuries induced by hyperoside preconditioning and its relationship with PI3K/Akt signaling pathway in rats. Zhongguo Zhong Yao Za Zhi. 40:118–123. 2015.In Chinese. PubMed/NCBI
25	Wu J, Yu J, Xie P, Maimaitili Y, Wang J, Yang L, Ma H, Zhang X, Yang Y and Zheng H: Sevoflurane postconditioning protects the myocardium against ischemia/reperfusion injury via activation of the JAK2-STAT3 pathway. PeerJ. 5:e31962017. View Article : Google Scholar : PubMed/NCBI
26	Liu C, Liu Y, Shen Z, Mial L, Zhang K, Wang F and Li Y: Sevoflurane preconditioning reduces intestinal ischemia-reper-fusion injury: Role of protein kinase C and mitochondrial ATP-sensitive potassium channel. PLoS One. 10:e01414262015. View Article : Google Scholar
27	Sun G, Zhou Y, Li H, Guo Y, Shan J, Xia M, Li Y, Li S, Long D and Feng L: Over-expression of microRNA-494 up-regulates hypoxia-inducible factor-1 alpha expression via PI3K/Akt pathway and protects against hypoxia-induced apop-tosis. J Biomed Sci. 20:1002013. View Article : Google Scholar
28	Nitulescu GM, Van De Venter M, Nitulescu G, Ungurianu A, Juzenas P, Peng Q, Olaru OT, Grădinaru D, Tsatsakis A, Tsoukalas D, et al: The Akt pathway in oncology therapy and beyond (review). Int J Oncol. 53:2319–2331. 2018.PubMed/NCBI
29	Satake A, Takaoka M, Nishikawa M, Yuba M, Shibata Y, Okumura K, Kitano K, Tsutsui H, Fujii K, Kobuchi S, et al: Protective effect of 17beta-estradiol on ischemic acute renal failure through the PI3K/Akt/eNOS pathway. Kidney Int. 73:308–317. 2008. View Article : Google Scholar
30	Song G, Ouyang G and Bao S: The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med. 9:59–71. 2005. View Article : Google Scholar : PubMed/NCBI
31	Zhang J, Liu XB, Cheng C, Xu DL, Lu QH and Ji XP: Rho-kinase inhibition is involved in the activation of PI3-kinase/Akt during ischemic-preconditioning-induced cardiomyocyte apoptosis. Int J Clin Exp Med. 7:4107–4114. 2014.
32	Zhang SB, Liu TJ, Pu GH, Li BY, Gao XZ and Han XL: MicroRNA-374 exerts protective effects by inhibiting SP1 through activating the PI3K/Akt pathway in rat models of myocardial ischemia-reperfusion after sevoflurane preconditioning. Cell Physiol Biochem. 46:1455–1470. 2018. View Article : Google Scholar : PubMed/NCBI
33	Liu X, Hong Q, Wang Z, Yu Y, Zou X and Xu L: miR-21 inhibits autophagy by targeting Rab11a in renal ischemia/reperfusion. Exp Cell Res. 338:64–69. 2015. View Article : Google Scholar : PubMed/NCBI
34	Zhou M, Cai J, Tang Y and Zhao Q: miR-17-92 cluster is a novel regulatory gene of cardiac ischemic/reperfusion injury. Med Hypotheses. 81:108–110. 2013. View Article : Google Scholar : PubMed/NCBI
35	Hu Q, Luo W, Huang L, Huang R and Chen R: Apoptosis-related microRNA changes in the right atrium induced by remote ischemic perconditioning during valve replacement surgery. Sci Rep. 6:189592016. View Article : Google Scholar : PubMed/NCBI
36	Chen J, Huang ZP, Seok HY, Ding J, Kataoka M, Zhang Z, Hu X, Wang G, Lin Z, Wang S, et al: mir-17-92 cluster is required for and sufficient to induce cardiomyocyte proliferation in postnatal and adult hearts. Circ Res. 112:1557–1566. 2013. View Article : Google Scholar : PubMed/NCBI
37	Benhamou D, Labi V, Novak R, Dai I, Shafir-Alon S, Weiss A, Gaujoux R, Arnold R, Shen-Orr SS, Rajewsky K and Melamed D: A c-Myc/miR17-92/Pten axis controls PI3K-mediated positive and negative selection in B cell development and reconstitutes CD19 deficiency. Cell Rep. 16:419–431. 2016. View Article : Google Scholar : PubMed/NCBI
38	Ma Q, Peng Z, Wang L, Li Y, Wang K, Zheng J, Liang Z and Liu T: miR-19a correlates with poor prognosis of clear cell renal cell carcinoma patients via promoting cell proliferation and suppressing PTEN/SMAD4 expression. Int J Oncol. 49:2589–2599. 2016. View Article : Google Scholar : PubMed/NCBI
39	Liang Z, Pan Q, Zhang Z, Huang C, Yan Z, Zhang Y and Li J: MicroRNA-125a-5p controls the proliferation, apoptosis, migration and PTEN/MEK1/2/ERK1/2 signaling pathway in MCF-7 breast cancer cells. Mol Med Rep. 20:4507–4514. 2019.PubMed/NCBI
40	Zheng W, Matei N, Pang J, Luo X, Song Z, Tang J and Zhang JH: Delayed recanalization at 3 days after permanent MCAO attenuates neuronal apoptosis through FGF21/FGFR1/PI3K/Caspase-3 pathway in rats. Exp Neurol. 320:1130072019. View Article : Google Scholar : PubMed/NCBI
41	Yamamura S, Saini S, Majid S, Hirata H, Ueno K, Chang I, Tanaka Y, Gupta A and Dahiya R: MicroRNA-34a suppresses malignant transformation by targeting c-Myc transcriptional complexes in human renal cell carcinoma. Carcinogenesis. 33:294–300. 2012. View Article : Google Scholar :