Exosomes derived from bone marrow mesenchymal stem cells regulate pyroptosis via the miR-143-3p/myeloid differentiation factor 88 axis to ameliorate intestinal ischemia-reperfusion injury

References

• Kalogeris T, Baines CP, Krenz M, et al. Ischemia/Reperfusion. Compr Physiol. 2016 Dec 6;7(1):113–20. doi: 10.1002/cphy.c160006
   PubMed Web of Science ®Google Scholar
• Golts E, Onaitis M. Commentary: Ischemia reperfusion-looking ahead. J Thorac Cardiovasc Surg. 2021 Feb;161(2):e124–e125. doi: 10.1016/j.jtcvs.2019.12.010
   PubMed Web of Science ®Google Scholar
• Mallick IH, Yang W, Winslet MC, et al. Ischemia-reperfusion injury of the intestine and protective strategies against injury. Dig Dis Sci. 2004 Sep;49(9):1359–1377. doi: 10.1023/B:DDAS.0000042232.98927.91
   PubMed Web of Science ®Google Scholar
• Leenarts CA, Grootjans J, Hundscheid IH, et al. Histopathology of human small intestinal and colonic ischemia-reperfusion: Experiences from human IR-models. Histol Histopathol. 2019 Jul;34(7):711–722. doi: 10.14670/HH-18-074
   PubMed Web of Science ®Google Scholar
• Barzegar M, Kaur G, Gavins FNE, et al. Potential therapeutic roles of stem cells in ischemia-reperfusion injury. Stem Cell Res. 2019 May;37:101421. doi: 10.1016/j.scr.2019.101421
   PubMed Web of Science ®Google Scholar
• Miceli V, Bulati M, Iannolo G, et al. Therapeutic properties of mesenchymal stromal/stem cells: The need of cell priming for cell-free therapies in regenerative medicine. Int J Mol Sci. 2021 Jan 14;22(2):763. doi: 10.3390/ijms22020763
   PubMed Web of Science ®Google Scholar
• Oliva J. Therapeutic properties of mesenchymal stem cell on organ ischemia-reperfusion injury. Int J Mol Sci. 2019 Nov 5;20(21):5511. doi: 10.3390/ijms20215511
   PubMed Web of Science ®Google Scholar
• Suh JH, Joo HS, Hong EB, et al. Therapeutic application of exosomes in inflammatory diseases. Int J Mol Sci. 2021 Jan 24;22(3):1144. doi: 10.3390/ijms22031144
   PubMed Web of Science ®Google Scholar
• Liu J, Chen T, Lei P, et al. Exosomes released by bone marrow mesenchymal stem cells attenuate lung injury induced by intestinal ischemia reperfusion via the TLR4/NF-κB pathway. Int J Med Sci. 2019;16(9):1238–1244. doi: 10.7150/ijms.35369
   PubMed Web of Science ®Google Scholar
• Kovacs SB, Miao EA. Gasdermins: Effectors of pyroptosis. Trends cell Biol 2017 Sep;27(9):673–684. doi: 10.1016/j.tcb.2017.05.005
   PubMed Web of Science ®Google Scholar
• Tsuchiya K. Switching from apoptosis to pyroptosis: Gasdermin-elicited inflammation and antitumor immunity. Int J Mol Sci. 2021 Jan 4;22(1):426. doi: 10.3390/ijms22010426
   PubMed Web of Science ®Google Scholar
• Wree A, Eguchi A, McGeough MD, et al. NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation, and fibrosis in mice. Hepatology. 2014 Mar;59(3):898–910. doi: 10.1002/hep.26592
   PubMed Web of Science ®Google Scholar
• Zhao Y, Shi J, Shao F. Inflammatory caspases: Activation and cleavage of gasdermin-D in vitro and during pyroptosis. Methods Mol Biol. 2018;1714:131–148. doi: 10.1007/978-1-4939-7519-8_9
   PubMedGoogle Scholar
• Popov SV, Maslov LN, Naryzhnaya NV, et al. The role of pyroptosis in ischemic and reperfusion injury of the heart. J Cardiovasc Pharmacol Ther. 2021 Nov;26(6):562–574. doi: 10.1177/10742484211027405
   PubMed Web of Science ®Google Scholar
• Xu XN, Jiang Y, Yan LY, et al. Aesculin suppresses the NLRP3 inflammasome-mediated pyroptosis via the Akt/GSK3β/NF-κB pathway to mitigate myocardial ischemia/reperfusion injury. Phytomedicine. 2021 Nov;92:153687. doi: 10.1006/j.phymed.2021.153687
   PubMed Web of Science ®Google Scholar
• Zeng Q, Zhou Y, Liang D, et al. Exosomes secreted from bone marrow mesenchymal stem cells attenuate oxygen-glucose deprivation/Reoxygenation-induced pyroptosis in PC12 cells by promoting AMPK-Dependent autophagic flux. Front Cell Neurosci. 2020;14:182. doi: 10.3389/fncel.2020.00182
   PubMed Web of Science ®Google Scholar
• Liu XL, Zhang MM, Liu HN, et al. Bone marrow mesenchymal stem cell-derived exosomes attenuate cerebral ischemia-reperfusion injury-induced neuroinflammation and pyroptosis by modulating microglia M1/M2 phenotypes. Exp Neurol. 2021 Jul;341:113700. doi: 10.1016/j.expneurol.2021.113700
   PubMed Web of Science ®Google Scholar
• Zhang G, Wan Z, Liu Z, et al. Exosomes derived from BMSCs ameliorate intestinal ischemia–reperfusion injury by regulating miR-144-3p-mediated oxidative stress. Dig Dis Sci. 2022 May 27;67(11):5090–5106. doi: 10.1007/s10620-022-07546-0
   PubMed Web of Science ®Google Scholar
• Coelho MJ, Fernandes MH. Human bone cell cultures in biocompatibility testing. Part II: effect of ascorbic acid, β-glycerophosphate and dexamethasone on osteoblastic differentiation. Biomaterials. 2000 2000 06 01;21(11):1095–1102. doi: 10.1016/S0142-9612(99)00192-1
   PubMed Web of Science ®Google Scholar
• Yao Y, Bi Z, Wu R, et al. METTL3 inhibits BMSC adipogenic differentiation by targeting the JAK1/STAT5/C/EBPβ pathway via an m(6)A-YTHDF2-dependent manner. FASEB J. 2019 Jun;33(6):7529–7544. doi: 10.1096/fj.201802644R
   PubMed Web of Science ®Google Scholar
• Gregory CA, Gunn WG, Peister A, et al. An alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem. 2004 Jun 1;329(1):77–84. doi: 10.1016/j.ab.2004.02.002
   PubMed Web of Science ®Google Scholar
• Deutsch MJ, Schriever SC, Roscher AA, et al. Digital image analysis approach for lipid droplet size quantitation of oil red O-stained cultured cells. Anal Biochem. 2014 Jan 15;445:87–89. doi: 10.1016/j.ab.2013.10.001
   PubMed Web of Science ®Google Scholar
• Weickert MT, Hecker JS, Buck MC, et al. Bone marrow stromal cells from MDS and AML patients show increased adipogenic potential with reduced Delta-like-1 expression. Sci Rep. 2021 Mar 15;11(1):5944. doi: 10.1038/s41598-021-85122-8
   PubMed Web of Science ®Google Scholar
• Wu XX, Showiheen SAA, Sun AR, et al. Exosomes Extraction and Identificatiom. Methods Mol Biol. 2019;2054:81–91. doi: 10.1007/978-1-4939-9767-5_4
   PubMedGoogle Scholar
• Yan X, Yu A, Zheng H, et al. Calycosin-7-O-β-D-glucoside attenuates OGD/R-Induced damage by preventing oxidative stress and neuronal apoptosis via the SIRT1/FOXO1/PGC-1α pathway in HT22 cells. Neural Plasticity. 2019;2019:8798069. doi: 10.1155/2019/8798069
   PubMed Web of Science ®Google Scholar
• Li Y, Feng D, Wang Z, et al. Ischemia-induced ACSL4 activation contributes to ferroptosis-mediated tissue injury in intestinal ischemia/reperfusion. Cell Death Diff. 2019 Nov;26(11):2284–2299. doi: 10.1038/s41418-019-0299-4
   PubMed Web of Science ®Google Scholar
• Chiu CJ, McArdle AH, Brown R, et al. Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal. Arch Surg (Chicago, Ill: 1960). 1970 Oct;101(4):478–483. doi: 10.1001/archsurg.1970.01340280030009
   PubMedGoogle Scholar
• Hirano S. Western blot analysis. Methods Mol Biol. 2012;926:87–97. doi: 10.1007/978-1-62703-002-1_6
   PubMedGoogle Scholar
• Gu S, Jin L, Zhang F, et al. Biological basis for restriction of microRNA targets to the 3’ untranslated region in mammalian mRnas. Nat Struct Mol Biol. 2009 Feb;16(2):144–150. doi: 10.1038/nsmb.1552
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001 Dec;25(4):402–408. doi: 10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Thomson JM, Parker JS, Hammond SM. Microarray analysis of miRNA gene expression. Methods Enzymol. 2007;427:107–122. doi: 10.1016/s0076-6879(07)27006-5
   PubMed Web of Science ®Google Scholar
• Chen F, Wang D, Li X, et al. Molecular mechanisms underlying intestinal ischemia/reperfusion injury: Bioinformatics analysis and in vivo validation. Med Sci Monit. 2020 Dec 8;26:e927476. doi: 10.12659/MSM.927476
   PubMed Web of Science ®Google Scholar
• Spees JL, Lee RH, Gregory CA. Mechanisms of mesenchymal stem/stromal cell function. Stem Cell Res Ther. 2016 Aug 31;7(1):125. doi: 10.1186/s13287-016-0363-7
   PubMedGoogle Scholar
• Qiu G, Zheng G, Ge M, et al. Functional proteins of mesenchymal stem cell-derived extracellular vesicles. Stem Cell Res Ther. 2019 Nov 28;10(1):359. doi: 10.1186/s13287-019-1484-6
   PubMed Web of Science ®Google Scholar
• McCulloh CJ, Olson JK, Wang Y, et al. Treatment of experimental necrotizing enterocolitis with stem cell-derived exosomes. J Pediatr Surg. 2018 Jun;53(6):1215–1220. doi: 10.1016/j.jpedsurg.2018.02.086
   PubMed Web of Science ®Google Scholar
• Chen H, Min XH, Wang QY, et al. Pre-activation of mesenchymal stem cells with TNF-α, IL-1β and nitric oxide enhances its paracrine effects on radiation-induced intestinal injury. Sci Rep. 2015 Mar 3;5(1):8718. doi: 10.1038/srep08718
   PubMedGoogle Scholar
• Gao Z, Zhang Q, Han Y, et al. Mesenchymal stromal cell-conditioned medium prevents radiation-induced small intestine injury in mice. Cytotherapy. 2012 Mar;14(3):267–273. doi: 10.3109/14653249.2011.616194
   PubMed Web of Science ®Google Scholar
• Yu B, Zhang X, Li X. Exosomes derived from mesenchymal stem cells. Int J Mol Sci. 2014 Mar 7;15(3):4142–4157. doi: 10.3390/ijms15034142
   PubMed Web of Science ®Google Scholar
• Phinney DG, Pittenger MF. Concise review: MSC-Derived exosomes for cell-free therapy. Stem Cells (Dayton, Ohio). 2017 Apr;35(4):851–858. doi: 10.1002/stem.2575
   PubMed Web of Science ®Google Scholar
• Li X, Zhang Y, Wang Y, et al. Exosomes derived from CXCR4-overexpressing BMSC Promoted activation of microvascular endothelial cells in cerebral ischemia/reperfusion injury. Neural Plasticity. 2020;2020:1–13. doi: 10.1155/2020/8814239
   Web of Science ®Google Scholar
• Chen Q, Liu Y, Ding X, et al. Bone marrow mesenchymal stem cell-secreted exosomes carrying microRNA-125b protect against myocardial ischemia reperfusion injury via targeting SIRT7. Mol Cell Biochem. 2020 Feb;465(1–2):103–114. doi: 10.1007/s11010-019-03671-z
   PubMed Web of Science ®Google Scholar
• Shi J, Gao W, Shao F. Pyroptosis: Gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci. 2017 Apr;42(4):245–254. doi: 10.1016/j.tibs.2016.10.004
   PubMed Web of Science ®Google Scholar
• Broz P. Immunology: Caspase target drives pyroptosis. Nature. 2015 Oct 29;526(7575):642–643. doi: 10.1038/nature15632
   PubMed Web of Science ®Google Scholar
• Jia C, Chen HW, Zhang J, et al. Role of pyroptosis in cardiovascular diseases. Int Immunopharmacol. 2019 Feb;67:311–318. doi: 10.1016/S0076-6879(07)27006-5
   PubMed Web of Science ®Google Scholar
• Zheng Z, Li G. Mechanisms and therapeutic regulation of pyroptosis in inflammatory diseases and cancer. Int J Mol Sci. 2020 Feb 20;21(4):1456. doi: 10.3390/ijms21041456
   PubMed Web of Science ®Google Scholar
• Qiu Z, Lei S, Zhao B, et al. NLRP3 inflammasome activation-mediated pyroptosis aggravates myocardial ischemia/reperfusion injury in diabetic rats. Oxid Med Cell Longevity. 2017;2017:9743280. doi: 10.1155/2017/9743280
   PubMed Web of Science ®Google Scholar
• Wu MY, Yiang GT, Liao WT, et al. Current mechanistic concepts in ischemia and reperfusion injury. Cell Physiol Biochem. 2018;46(4):1650–1667. doi: 10.1159/000489241
   PubMedGoogle Scholar
• Pegtel DM, Gould SJ. Exosomes. Annu Rev Biochem. 2019 Jun 20;88(1):487–514. doi: 10.1146/annurev-biochem-013118-111902
   PubMedGoogle Scholar
• Dexheimer PJ, Cochella L. MicroRNAs: From mechanism to organism. Front Cell Dev Biol. 2020;8:409. doi: 10.3389/fcell.2020.00409
   PubMed Web of Science ®Google Scholar
• Ghafouri-Fard S, Shoorei H, Taheri M. Non-coding RNAs participate in the ischemia-reperfusion injury. Biomedicine & Pharmacotherapy = Biomedecine & Pharmacotherapie. 2020 Sep;129:110419. doi: 10.1016/j.biopha.2020.110419
   PubMed Web of Science ®Google Scholar
• Chen G, Wang M, Ruan Z, et al. Mesenchymal stem cell-derived exosomal miR-143-3p suppresses myocardial ischemia-reperfusion injury by regulating autophagy. Life Sci. 2021 Sep 1;280:119742. doi: 10.1016/j.lfs.2021.119742
   PubMed Web of Science ®Google Scholar
• Deguine J, Barton GM. MyD88: a central player in innate immune signaling. F1000prime reports. F1000Prime Rep. 2014;6:97. doi: 10.12703/P6-97
   PubMedGoogle Scholar
• Subramanian S, Geng H, Tan XD. Cell death of intestinal epithelial cells in intestinal diseases. Sheng Li Xue Bao: [Acta Physiologica Sinica]. 2020 Jun 25;72(3):308–324.
   PubMedGoogle Scholar
• Donovan C, Liu G, Shen S, et al. The role of the microbiome and the NLRP3 inflammasome in the gut and lung. J Leukoc Biol. 2020 Sep;108(3):925–935. doi: 10.1002/JLB.3MR0720-472RR
   PubMed Web of Science ®Google Scholar
• Nadatani Y, Watanabe T, Shimada S, et al. Microbiome and intestinal ischemia/reperfusion injury. J Clin Biochem Nutr. 2018 Jul;63(1):26–32. doi: 10.3164/jcbn.17-137
   PubMed Web of Science ®Google Scholar
• Li S, Luo L, He Y, et al. Dental pulp stem cell-derived exosomes alleviate cerebral ischaemia-reperfusion injury through suppressing inflammatory response. Cell Proliferation. 2021 Aug;54(8):e13093. doi: 10.1111/cpr.13093
   PubMed Web of Science ®Google Scholar
• Du Y, Qian B, Gao L, et al. Aloin preconditioning attenuates hepatic ischemia/reperfusion injury via inhibiting TLR4/MyD88/NF-κB signal pathway in vivo and in vitro. Oxid Med Cell Longevity. 2019;2019:3765898. doi: 10.1155/2019/3765898
   PubMed Web of Science ®Google Scholar
• Zhang W, Song J, Li W, et al. Salvianolic acid D alleviates cerebral ischemia-reperfusion injury by suppressing the cytoplasmic translocation and release of HMGB1-Triggered NF-κB activation to Inhibit inflammatory response. Mediators Inflamm. 2020;2020:9049614. doi: 10.1155/2020/9049614
   PubMed Web of Science ®Google Scholar
• Chawla M, Roy P, Basak S. Role of the NF-κB system in context-specific tuning of the inflammatory gene response. Curr Opin Immunol. 2021 Feb;68:21–27. doi: 10.1016/j.coi.2020.08.005
   PubMed Web of Science ®Google Scholar
• Chen X, Liu G, Yuan Y, et al. NEK7 interacts with NLRP3 to modulate the pyroptosis in inflammatory bowel disease via NF-κB signaling. Cell Death Dis. 2019 Dec 2;10(12):906. doi: 10.1038/s41419-019-2157-1
   PubMedGoogle Scholar
• Xu S, Chen HW, Ni H, et al. Targeting HDAC6 attenuates nicotine-induced macrophage pyroptosis via NF-κB/NLRP3 pathway. Atherosclerosis. 2021 Jan;317:1–9. doi: 10.1016/j.atherosclerosis.2021.11.021
   PubMed Web of Science ®Google Scholar
• Oeckinghaus A, Ghosh S. The NF-kappaB family of transcription factors and its regulation. Cold Spring Harbor Perspect Biol. 2009 Oct;1(4):a000034. doi: 10.1101/cshperspect.a000034
   PubMed Web of Science ®Google Scholar
• Scheidereit C. IkappaB kinase complexes: gateways to NF-kappaB activation and transcription. Oncogene. 2006 Oct 30;25(51):6685–6705. doi: 10.1038/sj.onc.1209934
   PubMed Web of Science ®Google Scholar
• He Y, Hara H, Núñez G. Mechanism and regulation of NLRP3 inflammasome activation. Trends Biochem Sci. 2016 Dec;41(12):1012–1021. doi: 10.1016/j.tibs.2016.09.002
   PubMed Web of Science ®Google Scholar
• Qiao Y, Wang P, Qi J, et al. TLR-induced NF-κB activation regulates NLRP3 expression in murine macrophages. FEBS Lett. 2012 Apr 5;586(7):1022–1026. doi: 10.1016/j.febslet.2012.02.045
   PubMed Web of Science ®Google Scholar
• Kelley N, Jeltema D, Duan Y, et al. The NLRP3 inflammasome: An overview of mechanisms of activation and regulation. Int J Mol Sci. 2019 Jul 6;20(13):3328. doi: 10.3390/ijms20133328
   PubMed Web of Science ®Google Scholar
• Huang Y, Xu W, Zhou R. NLRP3 inflammasome activation and cell death. Cell Mol Immunol. 2021 Sep;18(9):2114–2127. doi: 10.1038/s41423-021-00740-6
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhu X, Yuan S, et al. TLR4/NF-κB signaling induces GSDMD-Related pyroptosis in tubular cells in diabetic kidney disease. Front Endocrinol (Lausanne). 2019;10:603. doi: 10.3389/fendo.2019.00603
   PubMed Web of Science ®Google Scholar