Notoginsenoside R1 improves intestinal microvascular functioning in sepsis by targeting Drp1-mediated mitochondrial quality imbalance

References

• Abulwerdi FA, Xu W, Ageeli AA, Yonkunas MJ, Arun G, Nam H, Schneekloth JS, Dayie TK, Spector D, Baird N, et al. 2019. Selective small-molecule targeting of a triple helix encoded by the long noncoding RNA, MALAT1. ACS Chem Biol. 14(2):223–235. doi: 10.1021/acschembio.8b00807.
   PubMed Web of Science ®Google Scholar
• Armstrong SM, Mubareka S, Lee WL. 2013. The lung microvascular endothelium as a therapeutic target in severe influenza. Antiviral Res. 99(2):113–118. doi: 10.1016/j.antiviral.2013.05.003.
   PubMed Web of Science ®Google Scholar
• Baughman JM, Perocchi F, Girgis HS, Plovanich M, Belcher-Timme CA, Sancak Y, Bao XR, Strittmatter L, Goldberger O, Bogorad RL, et al. 2011. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature. 476(7360):341–345. doi: 10.1038/nature10234.
   PubMed Web of Science ®Google Scholar
• Bernardi P, Di Lisa F. 2015. The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection. J Mol Cell Cardiol. 78:100–106. doi: 10.1016/j.yjmcc.2014.09.023.
   PubMed Web of Science ®Google Scholar
• Biesalski HK, McGregor GP. 2007. Antioxidant therapy in critical care–is the microcirculation the primary target? Crit Care Med. 35(9 Suppl):S577–S583. doi: 10.1097/01.CCM.0000278598.95294.C5.
   PubMed Web of Science ®Google Scholar
• Calabrese DR, Zlotkowski K, Alden S, Hewitt WM, Connelly CM, Wilson RM, Gaikwad S, Chen L, Guha R, Thomas CJ, et al. 2018. Characterization of clinically used oral antiseptics as quadruplex-binding ligands. Nucleic Acids Res. 46(6):2722–2732. doi: 10.1093/nar/gky084.
   PubMed Web of Science ®Google Scholar
• Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ. 2009. Vitagenes, cellular stress response, and acetylcarnitine: relevance to hormesis. Biofactors. 35(2):146–160. doi: 10.1002/biof.22.
   PubMed Web of Science ®Google Scholar
• Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP. 2010. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal. 13(11):1763–1811. doi: 10.1089/ars.2009.3074.
   PubMed Web of Science ®Google Scholar
• Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM. 2007. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci. 8(10):766–775. doi: 10.1038/nrn2214.
   PubMed Web of Science ®Google Scholar
• Cao B, Xu Z, Liu C, Hu J, Zhu Z, Li J, Zhu G, Li F. 2021. Protective effects of notoginsenoside R1 on acute lung injury in rats with sepsis. Ann Transl Med. 9(12):996–996. doi: 10.21037/atm-21-2496.
   PubMed Web of Science ®Google Scholar
• Chan DC. 2020. Mitochondrial dynamics and its involvement in disease. Annu Rev Pathol. 15(1):235–259. doi: 10.1146/annurev-pathmechdis-012419-032711.
   PubMedGoogle Scholar
• Chopra M, Golden HB, Mullapudi S, Dowhan W, Dostal DE, Sharma AC. 2011. Modulation of myocardial mitochondrial mechanisms during severe polymicrobial sepsis in the rat. PLoS One. 6(6):e21285. doi: 10.1371/journal.pone.0021285.
   PubMed Web of Science ®Google Scholar
• Cloonan SM, Choi AMK. 2016. Mitochondria in lung disease. J Clin Invest. 126(3):809–820. doi: 10.1172/JCI81113.
   PubMed Web of Science ®Google Scholar
• De Stefani D, Raffaello A, Teardo E, Szabò I, Rizzuto R. 2011. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature. 476(7360):336–340. doi: 10.1038/nature10230.
   PubMed Web of Science ®Google Scholar
• Duan C, Kuang L, Xiang X, Zhang J, Zhu Y, Wu Y, Yan Q, Liu L, Li T. 2020a. Activated Drp1-mediated mitochondrial ROS influence the gut microbiome and intestinal barrier after hemorrhagic shock. Aging (Albany NY). 12(2):1397–1416. doi: 10.18632/aging.102690.
   PubMedGoogle Scholar
• Duan C, Kuang L, Xiang X, Zhang J, Zhu Y, Wu Y, Yan Q, Liu L, Li T. 2020b. Drp1 regulates mitochondrial dysfunction and dysregulated metabolism in ischemic injury via Clec16a-, BAX-, and GSH- pathways. Cell Death Dis. 11(4):251. doi: 10.1038/s41419-020-2461-9.
   PubMed Web of Science ®Google Scholar
• Duan C, Ma R, Zeng X, Chen B, Hou D, Liu R, Li X, Liu L, Li T, Huang H. 2022. SARS-CoV-2 achieves immune escape by destroying mitochondrial quality: comprehensive analysis of the cellular landscapes of lung and blood specimens from patients with Covid-19. Front Immunol. 13:946731. doi: 10.3389/fimmu.2022.946731.
   PubMed Web of Science ®Google Scholar
• Duan C, Wang L, Zhang J, Xiang X, Wu Y, Zhang Z, Li Q, Tian K, Xue M, Liu L, et al. 2020c. Mdivi-1 attenuates oxidative stress and exerts vascular protection in ischemic/hypoxic injury by a mechanism independent of Drp1 gtpase activity. Redox Biol. 37:101706. doi: 10.1016/j.redox.2020.101706.
   PubMed Web of Science ®Google Scholar
• Duan CY, Kuang L, Hong C, Xiang X, Liu J, Li Q, Peng X, Zhou Y, Wang H, Liu L, et al. 2021. Mitochondrial Drp1 recognizes and induces excessive mptp opening after hypoxia through BAX-PiC and LRRK2-HK2. Cell Death Dis. 12(11):1050. doi: 10.1038/s41419-021-04343-x.
   PubMed Web of Science ®Google Scholar
• Exline MC, Crouser ED. 2008. Mitochondrial mechanisms of sepsis-induced organ failure. Front Biosci. 13:5030–5041. doi: 10.2741/3061.
   PubMed Web of Science ®Google Scholar
• Haak BW, Wiersinga WJ. 2017. The role of the gut microbiota in sepsis. Lancet Gastroenterol Hepatol. 2(2):135–143. doi: 10.1016/S2468-1253(16)30119-4.
   PubMed Web of Science ®Google Scholar
• Hao P, Jiang F, Cheng J, Ma L, Zhang Y, Zhao Y. 2017. Traditional Chinese medicine for cardiovascular disease: evidence and potential mechanisms. J Am Coll Cardiol. 69(24):2952–2966. doi: 10.1016/j.jacc.2017.04.041.
   PubMed Web of Science ®Google Scholar
• Huang K, Zhang P, Zhang Z, Youn JY, Wang C, Zhang H, Cai H. 2021. Traditional Chinese medicine (TCM) in the treatment of Covid-19 and other viral infections: efficacies and mechanisms. Pharmacol Ther. 225:107843. doi: 10.1016/j.pharmthera.2021.107843.
   PubMed Web of Science ®Google Scholar
• Ji WK, Chakrabarti R, Fan XT, Schoenfeld L, Strack S, Higgs HN. 2017. Receptor-mediated Drp1 oligomerization on endoplasmic reticulum. J Cell Biol. 216(12):4123–4139. doi: 10.1083/jcb.201610057.
   PubMed Web of Science ®Google Scholar
• Koh IHJ, Menchaca Diaz JL, Koh TH, Souza RL, Shu CM, Rogerio VE, Liberatore AMA. 2010. Microcirculatory evaluation in sepsis: a difficult task. Shock. 34 Suppl 1(7):27–33. doi: 10.1097/SHK.0b013e3181e7e80c.
   PubMedGoogle Scholar
• Lemasters JJ, Nieminen AL. 1997. Mitochondrial oxygen radical formation during reductive and oxidative stress to intact hepatocytes. Biosci Rep. 17(3):281–291. doi: 10.1023/a:1027332611839.
   PubMed Web of Science ®Google Scholar
• Li H, Zhu J, Xu Y, Mou F, Shan X, Wang Q, Liu B, Ning K, Liu J, Wang Y, et al. 2022. Notoginsenoside R1-loaded mesoporous silica nanoparticles targeting the site of injury through inflammatory cells improves heart repair after myocardial infarction. Redox Biol. 54:102384. doi: 10.1016/j.redox.2022.102384.
   PubMed Web of Science ®Google Scholar
• Liu B, Zhao T, Li Y, Han Y, Xu Y, Yang H, Wang S, Zhao Y, Li P, Wang Y. 2022. Notoginsenoside R1 ameliorates mitochondrial dysfunction to circumvent neuronal energy failure in acute phase of focal cerebral ischemia. Phytother Res. 36(5):2223–2235. doi: 10.1002/ptr.7450.
   PubMed Web of Science ®Google Scholar
• Liu C, Liu R, Cao Z, Guo Q, Huang H, Liu L, Xiao Y, Duan C, Ma R. 2022. Identification of MMP9 as a novel biomarker to mitochondrial metabolism disorder and oxidative stress in calcific aortic valve stenosis. Oxid Med Cell Longev. 2022:3858871–3858814. doi: 10.1155/2022/3858871.
   PubMed Web of Science ®Google Scholar
• Liu T, Ding Y, Wen A. 2018. Traditional Chinese medicine for ischaemic stroke. Lancet Neurol. 17(9):745. doi: 10.1016/S1474-4422(18)30290-4.
   PubMedGoogle Scholar
• Marsboom G, Toth PT, Ryan JJ, Hong Z, Wu X, Fang Y, Thenappan T, Piao L, Zhang HJ, Pogoriler J, et al. 2012. Dynamin-related protein 1-mediated mitochondrial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension. Circ Res. 110(11):1484–1497. doi: 10.1161/CIRCRESAHA.111.263848.
   PubMed Web of Science ®Google Scholar
• Martí-Renom MA, Stuart AC, Fiser A, Sánchez R, Melo F, Sali A. 2000. Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct. 29(1):291–325. doi: 10.1146/annurev.biophys.29.1.291.
   PubMedGoogle Scholar
• Parekh HS, Liu G, Wei MQ. 2009. A new dawn for the use of traditional Chinese medicine in cancer therapy. Mol Cancer. 8(1):21. doi: 10.1186/1476-4598-8-21.
   PubMedGoogle Scholar
• Pietrocola F, Galluzzi L, Bravo San Pedro JM, Madeo F, Kroemer G. 2015. Acetyl coenzyme a: a central metabolite and second messenger. Cell Metab. 21(6):805–821. doi: 10.1016/j.cmet.2015.05.014.
   PubMed Web of Science ®Google Scholar
• Prescott HC, Angus DC. 2018. Postsepsis morbidity. JAMA. 319(1):91. doi: 10.1001/jama.2017.19809.
   PubMedGoogle Scholar
• Raimundo N. 2014. Mitochondrial pathology: stress signals from the energy factory. Trends Mol Med. 20(5):282–292. doi: 10.1016/j.molmed.2014.01.005.
   PubMed Web of Science ®Google Scholar
• Reinhart K, Daniels R, Kissoon N, Machado FR, Schachter RD, Finfer S. 2017. Recognizing sepsis as a global health priority - a who resolution. N Engl J Med. 377(5):414–417. doi: 10.1056/NEJMp1707170.
   PubMed Web of Science ®Google Scholar
• Rittirsch D, Huber Lang MS, Flierl MA, Ward PA. 2009. Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc. 4(1):31–36. doi: 10.1038/nprot.2008.214.
   PubMed Web of Science ®Google Scholar
• Saijo H, Tatsumi N, Arihiro S, Kato T, Okabe M, Tajiri H, Hashimoto H. 2015. Microangiopathy triggers, and inducible nitric oxide synthase exacerbates dextran sulfate sodium-induced colitis. Lab Invest. 95(7):728–748. doi: 10.1038/labinvest.2015.60.
   PubMed Web of Science ®Google Scholar
• Schmidt K, Hernekamp JF, Philipsenburg C, Zivkovic AR, Brenner T, Hofer S. 2015. Time-dependent effect of clonidine on microvascular permeability during endotoxemia. Microvasc Res. 101:111–117. doi: 10.1016/j.mvr.2015.07.002.
   PubMed Web of Science ®Google Scholar
• Shou D, Yu Z, Meng J, Lai Z, Pang L, Dai M, Yang X, Tu Y. 2022. Panax notoginseng alleviates sepsis-induced acute kidney injury by reducing inflammation in rats. Evid Based Complement Alternat Med. 2022:9742169–9742169. doi: 10.1155/2022/9742169.
   PubMed Web of Science ®Google Scholar
• Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using clustal omega. Mol Syst Biol. 7:539.
   PubMed Web of Science ®Google Scholar
• Siracusa R, Scuto M, Fusco R, Trovato A, Ontario ML, Crea R, Di Paola R, Cuzzocrea S, Calabrese V. 2020. Anti-inflammatory and anti-oxidant activity of hidrox(®) in rotenone-induced parkinson’s disease in mice. Antioxidants (Basel). 9(9):824. doi: 10.3390/antiox9090824.
   PubMedGoogle Scholar
• Soreq L, Ben Shaul Y, Israel Z, Bergman H, Soreq H. 2012. Meta-analysis of genetic and environmental Parkinson’s disease models reveals a common role of mitochondrial protection pathways. Neurobiol Dis. 45(3):1018–1030. doi: 10.1016/j.nbd.2011.12.021.
   PubMed Web of Science ®Google Scholar
• Souza ACP, Yuen PST, Star RA. 2015. Microparticles: markers and mediators of sepsis-induced microvascular dysfunction, immunosuppression, and AKI. Kidney Int. 87(6):1100–1108. doi: 10.1038/ki.2015.26.
   PubMed Web of Science ®Google Scholar
• Sun B, Xiao J, Sun X, Wu Y. 2013. Notoginsenoside R1 attenuates cardiac dysfunction in endotoxemic mice: an insight into oestrogen receptor activation and PI3K/Akt signalling. Br J Pharmacol. 168(7):1758–1770. doi: 10.1111/bph.12063.
   PubMed Web of Science ®Google Scholar
• Thomas RR, Khan SM, Portell FR, Smigrodzki RM, Bennett JP. 2011. Recombinant human mitochondrial transcription factor a stimulates mitochondrial biogenesis and ATP synthesis, improves motor function after MPTP, reduces oxidative stress and increases survival after endotoxin. Mitochondrion. 11(1):108–118. doi: 10.1016/j.mito.2010.08.004.
   PubMed Web of Science ®Google Scholar
• Vincent JL, Opal SM, Marshall JC, Tracey KJ. 2013. Sepsis definitions: time for change. Lancet. 381(9868):774–775. doi: 10.1016/S0140-6736(12)61815-7.
   PubMed Web of Science ®Google Scholar
• Wu Q, Luo C, Tao L. 2017. Dynamin-related protein 1 (Drp1) mediating mitophagy contributes to the pathophysiology of nervous system diseases and brain injury. Histol Histopathol. 32:551–559.
   PubMed Web of Science ®Google Scholar
• Xu H, Zhang X, Shi Y, Yu K, Jiang Y. 2022. Notoginsenoside R1 relieves the myocardial infarction via activating the JAK2/STAT3 signaling pathway in vivo and in vitro. Bioengineered. 13(3):5653–5662. doi: 10.1080/21655979.2022.2037366.
   PubMed Web of Science ®Google Scholar
• Yan Y, Zhang D, Zhou P, Li B, Huang SY. 2017. Hdock: a web server for protein-protein and protein-DNA/RNA docking based on a hybrid strategy. Nucleic Acids Res. 45(W1):W365–W373. doi: 10.1093/nar/gkx407.
   PubMed Web of Science ®Google Scholar
• Zeng X, Zhang Y, Ma R, Chen Y, Xiang X, Hou D, Li X, Huang H, Li T, Duan C. 2022. Activated Drp1 regulates p62-mediated autophagic flux and aggravates inflammation in cerebral ischemia-reperfusion via the ROS-RIP1/RIP3-exosome axis. Mil Med Res. 9:25.
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang J, Zhang C, Zhang X, Ye J, Kuang S, Sun G, Sun X. 2018. Notoginsenoside R1 protects against diabetic cardiomyopathy through activating estrogen receptor α and its downstream signaling. Front Pharmacol. 9:1227. doi: 10.3389/fphar.2018.01227.
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang X, Zhang C, Shen Q, Sun G, Sun X. 2019. Notoginsenoside R1 protects db/db mice against diabetic nephropathy via upregulation of Nrf2-mediated HO-1 expression. Molecules. 24(2):247. doi: 10.3390/molecules24020247.
   PubMed Web of Science ®Google Scholar
• Zhang H, Feng Y, Yao Y. 2018. Potential therapy strategy: targeting mitochondrial dysfunction in sepsis. Mil Med Res. 5:41.
   PubMed Web of Science ®Google Scholar
• Zhang T, Hou D, He J, Zeng X, Liu R, Liu L, Li T, Xiao Y, Ma R, Huang H, et al. 2022. Oxidative-damaged mitochondria activate GABARAPL1-induced NLRP3 inflammasomes in an autophagic-exosome manner after acute myocardial ischemia. Oxid Med Cell Longev. 2022:7958542–7958519. doi: 10.1155/2022/7958542.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Cai W, Han G, Zhou S, Li J, Chen M, Li H. 2020. Panax notoginseng saponins prevent senescence and inhibit apoptosis by regulating the PI3K‑AKT‑mTOR pathway in osteoarthritic chondrocytes. Int J Mol Med. 45(4):1225–1236. doi: 10.3892/ijmm.2020.4491.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Song Y, Wang C, Jiang J, Liu S, Bai Q, Li L, Jin H, Jin Y, Yan G. 2022. Panax notoginseng saponin R1 attenuates allergic rhinitis through AMPK/Drp1 mediated mitochondrial fission. Biochem Pharmacol. 202:115106. doi: 10.1016/j.bcp.2022.115106.
   PubMed Web of Science ®Google Scholar
• Zhong L, Zhou X, Liu Y, Wang Y, Ma F, Guo B, Yan Z, Zhang Q. 2015. Estrogen receptor α mediates the effects of notoginsenoside R1 on endotoxin-induced inflammatory and apoptotic responses in H9c2 cardiomyocytes. Mol Med Rep. 12(1):119–126. doi: 10.3892/mmr.2015.3394.
   PubMed Web of Science ®Google Scholar
• Zhou P, Xie W, Meng X, Zhai Y, Dong X, Zhang X, Sun G, Sun X. 2019. Notoginsenoside R1 ameliorates diabetic retinopathy through PINK1-dependent activation of mitophagy. Cells. 8(3):213. doi: 10.3390/cells8030213.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Kuang L, Wu Y, Deng H, She H, Zhou Y, Zhang J, Liu L, Li T. 2021. Protective effects of inhibition of mitochondrial fission on organ function after sepsis. Front Pharmacol. 12:712489. doi: 10.3389/fphar.2021.712489.
   PubMed Web of Science ®Google Scholar
• Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med. 192(7):1001–1014. doi: 10.1084/jem.192.7.1001.
   PubMed Web of Science ®Google Scholar