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      Emodin Ameliorates Severe Acute Pancreatitis-Associated Acute Lung Injury in Rats by Modulating Exosome-Specific miRNA Expression Profiles

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          Abstract

          Background

          Numerous preclinical investigations have exhibited the beneficial impact of emodin (EMO) on the management of severe acute pancreatitis (SAP)-associated acute lung injury (ALI). However, the potential of EMO to mitigate organ damage through the modulation of exosome (Exo)-specific miRNA expression profiles remains unclear.

          Methods

          The SAP rat model was established by retrograde injection of 5% sodium taurocholate into the pancreatic bile duct. Rats received intragastric administration of EMO at 2 h and 12 h post-modeling. Plasma and bronchoalveolar lavage fluid (BALF)-derived exosomes were isolated and purified from SAP rats treated with EMO. The therapeutic effects of these Exos in SAP rats were assessed using hematoxylin-eosin staining and measurement of inflammatory factor levels. MicroRNA (miRNA) sequencing was conducted on plasma and BALF-derived Exos, and rescue experiments were performed to investigate the function of NOVEL miR-29a-3p in the treatment of SAP using EMO.

          Results

          EMO exhibits ameliorative effects on pancreatic and lung injury and inflammation in rats with SAP. Plasma/BALF-derived Exos from EMO-treated SAP rats also have therapeutic effects on SAP rats. The miRNA expression profile of plasma and BALF-derived Exos in SAP rats underwent significant changes upon exposure to EMO. In particular, 34 differentially expressed miRNAs (DEmiRNAs) were identified when comparing BALF-SAP+EMO-Exo and BALF-SAP-Exo. 39 DEmiRNAs were identified when comparing plasma-SAP+EMO-Exo to plasma-SAP-Exo. We found that SAP rats treated with Exos derived from BALF exhibited a more potent therapeutic response than those treated with Exos derived from plasma. EMO may rely on NOVEL-rno-miR-29a-3p expression to prevent pulmonary injury in SAP rats.

          Conclusion

          The mechanism of action of EMO is observed to have a significant impact on the miRNA expression profile of Exos derived from plasma and BALF in SAP rats. NOVEL-rno-miR-29a-3p, which is specific to Exos, and is derived from BALF, may play a crucial role in the therapeutic efficacy of EMO.

          Graphical Abstract

          Plain Language Summary

          • Exosomes extracted from plasma/BALF of EMO-treated SAP rats show a substantial therapeutic impact on SAP-Associated ALI, with BALF-derived exosomes having a higher therapeutic effect than plasma-derived exosomes.

          • EMO dramatically altered the miRNA expression patterns of plasma and BALF-derived exosomes in SAP rats.

          • The lung protective effect of EMO in SAP rats is somewhat reliant on Novel-rno-miR-29a-3p expression.

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          Most cited references43

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          Intestinal barrier damage, systemic inflammatory response syndrome, and acute lung injury: A troublesome trio for acute pancreatitis.

          Peng Ge, Yalan Luo, Chukwuemeka Okoye … (2020)
          Severe acute pancreatitis (SAP), a serious inflammatory disease of the pancreas, can easily lead to systemic inflammatory response syndrome (SIRS) and multiple organ dysfunction syndromes (MODS). Acute lung injury (ALI) is one of the most serious complications of SAP. However, the specific pathogenesis of SAP-associated ALI is not fully understood. Crosstalk and multi-mechanisms involving pancreatic necrosis, bacteremia, intestinal barrier failure, activation of inflammatory cascades and diffuse alveolar damage is the main reason for the unclear pathological mechanism of SAP-associated ALI. According to previous research on SAP-associated ALI in our laboratory and theories put forward by other scholars, we propose that the complex pattern of SAP-associated ALI is based on the "pancreas-intestine-inflammation/endotoxin-lung (P-I-I/E-L) pathway". In this review, we mainly concentrated on the specific details of the "P-I-I/E-L pathway" and the potential treatments or preventive measures for SAP-associated ALI.
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            Systematic review of extracellular vesicle-based treatments for lung injury: are EVs a potential therapy for COVID-19?

            Kasra Khalaj, Rebeca Lopes Figueira, Lina Antounians … (2020)
            ABSTRACT Severe COVID-19 infection results in bilateral interstitial pneumonia, often leading to acute respiratory distress syndrome (ARDS) and pulmonary fibrosis in survivors. Most patients with severe COVID-19 infections who died had developed ARDS. Currently, ARDS is treated with supportive measures, but regenerative medicine approaches including extracellular vesicle (EV)-based therapies have shown promise. Herein, we aimed to analyse whether EV-based therapies could be effective in treating severe pulmonary conditions that affect COVID-19 patients and to understand their relevance for an eventual therapeutic application to human patients. Using a defined search strategy, we conducted a systematic review of the literature and found 39 articles (2014–2020) that reported effects of EVs, mainly derived from stem cells, in lung injury models (one large animal study, none in human). EV treatment resulted in: (1) attenuation of inflammation (reduction of pro-inflammatory cytokines and neutrophil infiltration, M2 macrophage polarization); (2) regeneration of alveolar epithelium (decreased apoptosis and stimulation of surfactant production); (3) repair of microvascular permeability (increased endothelial cell junction proteins); (4) prevention of fibrosis (reduced fibrin production). These effects were mediated by the release of EV cargo and identified factors including miRs-126, −30b-3p, −145, −27a-3p, syndecan-1, hepatocyte growth factor and angiopoietin-1. This review indicates that EV-based therapies hold great potential for COVID-19 related lung injuries as they target multiple pathways and enhance tissue regeneration. However, before translating EV therapies into human clinical trials, efforts should be directed at developing good manufacturing practice solutions for EVs and testing optimal dosage and administration route in large animal models.
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              Plasma-derived exosomes contribute to pancreatitis-associated lung injury by triggering NLRP3-dependent pyroptosis in alveolar macrophages

              Xiao-Bo Wu, Hong-Yu Sun, Zhu-Lin Luo … (2020)
              Article 0 comments Cited 39 times – based on 0 reviews     Review now
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                Author and article information

                Journal
                Journal ID (nlm-ta): Int J Nanomedicine
                Journal ID (iso-abbrev): Int J Nanomedicine
                Journal ID (publisher-id): ijn
                Title: International Journal of Nanomedicine
                Publisher: Dove
                ISSN (Print): 1176-9114
                ISSN (Electronic): 1178-2013
                Publication date (Electronic): 15 November 2023
                Publication date Collection: 2023
                Volume: 18
                Pages: 6743-6761
                Affiliations
                [1 ]Department of General Surgery, the First Affiliated Hospital of Dalian Medical University , Dalian, Liaoning, 116011, People’s Republic of China
                [2 ]Institute (College) of Integrative Medicine, Dalian Medical University , Dalian, Liaoning, 116011, People’s Republic of China
                [3 ]Laboratory of Integrative Medicine, the First Affiliated Hospital of Dalian Medical University , Dalian, Liaoning, 116011, People’s Republic of China
                [4 ]Department of Traditional Chinese Medicine, the Second Affiliated Hospital of Dalian Medical University , Dalian, 116023, People’s Republic of China
                [5 ]CAS Key Laboratory of Separation Science for Analytical Chemistry, National Chromatographic Research and Analysis Center, Dalian Institute of Chemical Physics, Chinese Academy of Science , Dalian, 116023, People’s Republic of China
                Author notes
                Correspondence: Hailong Chen, Email chenhailong@dmu.edu.cn
                Author information
                http://orcid.org/0000-0002-9619-5468
                Article
                Publisher ID: 428924
                DOI: 10.2147/IJN.S428924
                PMC ID: 10657551
                SO-VID: 5504bc8e-fd78-4854-ac63-eb75fce6ac76
                Copyright © © 2023 Yang et al.
                License:

                This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License ( http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms ( https://www.dovepress.com/terms.php).

                History
                Date received : 28 July 2023
                Date accepted : 20 October 2023
                Page count
                Figures: 8, References: 43, Pages: 19
                Funding
                Funded by: National Natural Science Foundation of China, open-funder-registry 10.13039/501100001809;
                Funded by: National Key R&D Program of China;
                Funded by: Applied Basic Research Program of Liaoning Province;
                This study was supported by National Natural Science Foundation of China (NO. 82074158 and 82274311), National Key R&D Program of China (NO. 2019YFE0119300), and Applied Basic Research Program of Liaoning Province (NO. 2023JH2/101300126).
                Categories
                Subject: Original Research

                ScienceOpen disciplines: Molecular medicine
                Keywords: severe acute pancreatitis,acute lung injury,emodin,exosome,microrna
                Data availability:
                ScienceOpen disciplines: Molecular medicine
                Keywords: severe acute pancreatitis, acute lung injury, emodin, exosome, microrna

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