Cornus iridoid glycoside alleviates sepsis-induced acute lung injury by regulating NF-κB and Nrf2/HO-1 pathways
Main Article Content
Keywords
acute lung injury, Cornus iridoid glycoside, NF-κB, Nrf2/HO-1, sepsis
Abstract
Background: Sepsis-induced acute lung injury (ALI) is a syndrome associated with inflammation. Cornus iridoid glycoside (CIG), a bioactive component isolated from Corni Fructus, exhibits anti-inflammatory activities. However, the function and underlying mechanisms of CIG in mice with sepsis-induced ALI remain elusive.
Methods: The sepsis-elicited ALI model of mice was established by the induction of cecal ligation and puncture (CLP). The wet/dry (W/D) ratio of lung tissues was examined, and the pathological alterations were determined by hematoxylin and eosin staining. The messenger RNA (mRNA) expressions and serum levels of Interleukin (IL)-1β, IL-6, and tumor necrosis factor-α (TNF-α) were measured by reverse transcription-quantitative polymerase chain reaction and enzyme-linked immunosorbent serologic assay, respectively. The concentrations of malondialdehyde (MDA), superoxide dismutase (SOD), and glutathione peroxidase (GSH-Px) were assessed by biochemical kits. In addition, the relative protein levels of p-p65, p65, phosphorylated- nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor, alpha (p-IκBα), IκBα, nuclear factor erythroid 2-related factor 2 (Nrf2), and heme oxygenase-1 (HO-1) gene were analyzed by Western blotting analysis.
Results: CLP enhanced W/D ratio and aggravated pathological changes and scores in mice, which were obviously alleviated by the two concentrations of CIG treatment. CIG treatment notably decreased the CLP-induced mRNA expressions and serum levels of IL-1β, IL-6, TNF-α, and MDA, but enhanced the decreased concentrations (caused by CLP) of SOD and GSH-Px. Moreover, CIG treatment significantly decreased the ratios of p65/p-p65 and IκBα/p-IκBα caused by CLP, but aggravated the CLP-induced relative protein levels of Nrf2 and HO-1.
Conclusions: CIG obviously ameliorated the sepsis-induced ALI in mice by suppressing inflammation and oxidative stress, which was closely associated with nuclear factor kappa B (NF-κB) and Nrf2–HO-1 signaling pathways.
References
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29. Chen Q, Shao X, He Y, Lu E, Zhu L, Tang W. Norisoboldine attenuates sepsis-induced acute lung injury by modulating macrophage polarization via PKM2/HIF-1α/PGC-1α pathway. Biol Pharm Bull. 2021;44(10):1536–47. 10.1248/bpb.b21-00457
30. Zhang J, Wang C, Wang H, Li X, Xu J, Yu K. Loganin alleviates sepsis-induced acute lung injury by regulating macrophage polarization and inhibiting NLRP3 inflammasome activation. Int Immunopharmacol. 2021;95:107529. 10.1016/j.intimp.2021.107529
31. Oliveira-Junior IS, Brunialti MK, Koh IH, Junqueira VB, Salomão R. Effect of pentoxifylline on lung inflammation and gas exchange in a sepsis-induced acute lung injury model. Braz J Med Biol Res. 2006;39(11):1455–63. 10.1590/S0100-879X2006001100009
32. Rahmati M, Keshvari M, Mirnasouri R, Chehelcheraghi F. Exercise and Urtica dioica extract ameliorate hippocampal insulin signaling, oxidative stress, neuroinflammation, and cognitive function in STZ-induced diabetic rats. Biomed Pharmacother. 2021;139:111577. 10.1016/j.biopha.2021.111577
33. Keshvari M, Rahmati M, Mirnasouri R, Chehelcheraghi F. Effects of endurance exercise and Urtica dioica on the functional, histological and molecular aspects of the hippocampus in STZ-induced diabetic rats. J Ethnopharmacol. 2020;256:112801. 10.1016/j.jep.2020.112801
34. Guo RF, Ward PA. Role of oxidants in lung injury during sepsis. Antioxid Redox Signal. 2007;9(11):1991–2002. 10.1089/ars.2007.1785
35. Alsharif KF, Almalki AA, Alsanie WF, Alzahrani KJ, Kabrah SM, Elshopakey GE, et al. Protocatechuic acid attenuates lipopolysaccharide-induced septic lung injury in mice: The possible role through suppressing oxidative stress, inflammation and apoptosis. J Food Biochem. 2021;45(10):e13915. 10.1111/jfbc.13915
36. Hu M, Yang J, Xu Y. Isoorientin suppresses sepsis-induced acute lung injury in mice by activating an EPCR-dependent JAK2/STAT3 pathway. J Mol Histol. 2022 Feb;53(1):97–109. 10.1007/s10735-021-10039-5
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39. Park CH, Noh JS, Kim JH, Tanaka T, Zhao Q, Matsumoto K, et al. Evaluation of morroniside, iridoid glycoside from corni fructus on diabetes-induced alterations such as oxidative stress, inflammation, and apoptosis in the liver of type 2 diabetic db/db mice. Biol Pharm Bull. 2011;34(10):1559–65. 10.1248/bpb.34.1559
40. Park CH, Tanaka T, Kim JH, Cho EJ, Park JC, Shibahara N, et al. Hepato-protective effects of loganin, iridoid glycoside from Corni Fructus, against hyperglycemia-activated signaling pathway in liver of type 2 diabetic db/db mice. Toxicology. 2011;290(1):14–21. 10.1016/j.tox.2011.08.004
41. Wang H, Zhou XM, Wu LY, Liu GJ, Xu WD, Zhang XS, et al. Aucubin alleviates oxidative stress and inflammation via Nrf2-mediated signaling activity in experimental traumatic brain injury. J Neuroinflamm. 2020;17(1):188. 10.1186/s12974-020-01863-9
42. Zhang Y, Han D, Yu S, An C, Liu X, Zhong H, et al. Protective effect of iridoid glycosides of the leaves of Syringa oblata Lindl. on dextran sulfate sodium-induced ulcerative colitis by inhibition of the TLR2/4/MyD88/NF-κB signaling pathway. Biomed Res Int. 2020;2020:7650123. 10.1155/2020/7650123
43. Zhao B, Gao W, Gao X, Leng Y, Liu M, Hou J, et al. Sulforaphane attenuates acute lung injury by inhibiting oxidative stress via Nrf2/HO-1 pathway in a rat sepsis model. Int J Clin Exp Pathol. 2017;10(8):9021–8. PMid: 31966772
44. Yuan J, Cheng W, Zhang G, Ma Q, Li X, Zhang B, et al. Protective effects of iridoid glycosides on acute colitis via inhibition of the inflammatory response mediated by the STAT3/NF-κB pathway. Int Immunopharmacol. 2020;81:106240. 10.1016/j.intimp.2020.106240
2. Biason L, Teixeira C, Haas JS, Cabral CDR, Friedman G. Effects of sepsis on morbidity and mortality in critically Ill patients 2 years after intensive care unit discharge. Am J Crit Care. 2019;28(6):424–32. 10.4037/ajcc2019638
3. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, et al. Incidence and outcomes of acute lung injury. N Engl J Med. 2005;353(16):1685–93. 10.1056/NEJMoa050333
4. Villar J, Sulemanji D, Kacmarek RM. The acute respiratory distress syndrome: Incidence and mortality, has it changed? Curr Opin Crit Care. 2014;20(1):3–9. 10.1097/MCC.0000000000000057
5. Matthay MA, Zemans RL, Zimmerman GA, Arabi YM, Beitler JR, Mercat A, et al. Acute respiratory distress syndrome. Nat Rev Dis Primers. 2019;5(1):18. 10.1038/s41572-019-0069-0
6. Zhang Y, Yu W, Han D, Meng J, Wang H, Cao G. L-lysine ameliorates sepsis-induced acute lung injury in a lipopolysaccharide-induced mouse model. Biomed Pharmacother. 2019;118:109307. 10.1016/j.biopha.2019.109307
7. Ding X, Tong Y, Jin S, Chen Z, Li T, Billiar TR, et al. Mechanical ventilation enhances extrapulmonary sepsis-induced lung injury: role of WISP1-αvβ5 integrin pathway in TLR4-mediated inflammation and injury. Crit Care. 2018;22(1):302. 10.1186/s13054-018-2237-0
8. Sazonov V, Abylkassov R, Tobylbayeva Z, Saparov A, Mironova O, Poddighe D. Case series: Efficacy and safety of hemoadsorption with HA-330 adsorber in septic pediatric patients with cancer. Front Pediatr. 2021;9:672260. 10.3389/fped.2021.672260
9. Fu S, Yu S, Wang L, Ma X, Li X. Unfractionated heparin improves the clinical efficacy in adult sepsis patients: A systematic review and meta-analysis. BMC Anesthesiol. 2022;22(1):28. 10.1186/s12871-021-01545-w
10. Li HB, Feng QM, Zhang LX, Wang J, Chi J, Chen SQ, et al. Four new gallate derivatives from wine-processed corni fructus and their anti-inflammatory activities. Molecules. 2021;26(7):1851. 10.3390/molecules26071851
11. Wang X, Wu Y, Wang F, Yi J, Zhang Y. Optimization of polysaccharide process from Fructus corni with box-behnken design and antioxidant capacity. Pak J Pharm Sci. 2019;32(4):1537–44. PMid: 31608872
12. Bi H, Niu D, Guo C, Li J, Chen X, Zhang Y, et al. Comparative study of crude and wine-processing Corni Fructus on chemical composition and antidiabetic effects. Evid Based Complement Alternat Med. 2019;2019:3986964. 10.1155/2019/3986964
13. Wu Y, Wang X, Shen B, Kang L, Fan E. Extraction, structure and bioactivities of the polysaccharides from Fructus corni. Recent Pat Food Nutr Agric. 2013;5(1):57–61. 10.2174/2212798411305010009
14. Zhang XW, Sui Y, Liu XX, Fu CY, Qiao YH, Liu WJ, et al. Structures and anti-atherosclerotic effects of 1,6-α-glucans from Fructus corni. Int J Biol Macromol. 2020;161:1346–57. 10.1016/j.ijbiomac.2020.08.038
15. Mau J, Chen C, Hsieh P. Antimicrobial effect of extracts from Chinese chive, cinnamon, and corni fructus. J Agric Food Chem. 2001;49(1):183–8. 10.1021/jf000263c
16. Ya BL, Li CY, Zhang L, Wang W, Li L. Cornel iridoid glycoside inhibits inflammation and apoptosis in brains of rats with focal cerebral ischemia. Neurochem Res. 2010;35(5):773–81. 10.1007/s11064-010-0134-2
17. Silverman N, Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev. 2001;15(18):2321–42. 10.1101/gad.909001
18. Haddad JJ, Abdel-Karim NE. NF-κB cellular and molecular regulatory mechanisms and pathways: Therapeutic pattern or pseudo regulation? Cell Immunol. 2011;271(1):5–14. 10.1016/j.cellimm.2011.06.021
19. Ni YL, Shen HT, Su CH, Chen WY, Huang-Liu R, Chen CJ, et al. Nerolidol suppresses the inflammatory response during lipopolysaccharide-induced acute lung injury via the modulation of antioxidant enzymes and the AMPK/Nrf-2/HO-1 pathway. Oxid Med Cell Longev. 2019;2019:9605980. 10.1155/2019/9605980
20. Park C, Cha HJ, Lee H, Kim GY, Choi YH. The regulation of the TLR4/NF-κB and Nrf2/HO-1 signaling pathways is involved in the inhibition of lipopolysaccharide-induced inflammation and oxidative reactions by morroniside in RAW 264.7 macrophages. Arch Biochem Biophys. 2021;706:108926. 10.1016/j.abb.2021.108926
21. National Research Council (US) Committee for the Update of the Guide for the Care and Use of Laboratory Anumals. Guide for the care and use of laboratory animals. 8th ed. The National Academies collection: Reports funded by National Institutes of Health. Washington, DC: National Academies Press; 2011. PMid: 21595115 Copyright ©2011, National Academy of Sciences.
22. Liang W, Guo L, Liu T, Qin S. MEF2C alleviates acute lung injury in cecal ligation and puncture (CLP)-induced sepsis rats by up-regulating AQP1. Allergol Immunopathol (Madr). 2021;49(5):117–24. 10.15586/aei.v49i5.477
23. Wang ZF, Yang YM, Fan H. Protective effect of S-nitrosoglutathione pretreatment on acute lung injury in septic rats. Iran J Basic Med Sci. 2020;23(8):1059–64. 10.22038/ijbms.2020.43590.10240
24. Chen S, Chen X, Xiu Y-L, Sun K-X, Zong Z-H, Zhao Y. microRNA 490-3P enhances the drug-resistance of human ovarian cancer cells. J Ovarian Res. 2014;7:84. 10.1186/s13048-014-0084-4
25. Li S, Sun Y, Tang X, Wang L, Cheng X. miR-20a attenuates acute lung injury in septic rats via targeting TLR4. Signa Vitae. 2021;17(4):157–62.
26. da-Palma-Cruz M, da Silva RF, Monteiro D, Rehim H, Grabulosa CC, de Oliveira APL, et al. Photobiomodulation modulates the resolution of inflammation during acute lung injury induced by sepsis. Lasers Med Sci. 2019;34(1):191–9. 10.1007/s10103-018-2688-1
27. Wang Y, Xue L, Wu Y, Zhang J, Dai Y, Li F, et al. Ruscogenin attenuates sepsis-induced acute lung injury and pulmonary endothelial barrier dysfunction via TLR4/Src/p120-catenin/VE-cadherin signalling pathway. J Pharm Pharmacol. 2021;73(7):893–900. 10.1093/jpp/rgaa039
28. Zhang E, Wang J, Chen Q, Wang Z, Li D, Jiang N, et al. Artesunate ameliorates sepsis-induced acute lung injury by activating the mTOR/AKT/PI3K axis. Gene. 2020;759:144969. 10.1016/j.gene.2020.144969
29. Chen Q, Shao X, He Y, Lu E, Zhu L, Tang W. Norisoboldine attenuates sepsis-induced acute lung injury by modulating macrophage polarization via PKM2/HIF-1α/PGC-1α pathway. Biol Pharm Bull. 2021;44(10):1536–47. 10.1248/bpb.b21-00457
30. Zhang J, Wang C, Wang H, Li X, Xu J, Yu K. Loganin alleviates sepsis-induced acute lung injury by regulating macrophage polarization and inhibiting NLRP3 inflammasome activation. Int Immunopharmacol. 2021;95:107529. 10.1016/j.intimp.2021.107529
31. Oliveira-Junior IS, Brunialti MK, Koh IH, Junqueira VB, Salomão R. Effect of pentoxifylline on lung inflammation and gas exchange in a sepsis-induced acute lung injury model. Braz J Med Biol Res. 2006;39(11):1455–63. 10.1590/S0100-879X2006001100009
32. Rahmati M, Keshvari M, Mirnasouri R, Chehelcheraghi F. Exercise and Urtica dioica extract ameliorate hippocampal insulin signaling, oxidative stress, neuroinflammation, and cognitive function in STZ-induced diabetic rats. Biomed Pharmacother. 2021;139:111577. 10.1016/j.biopha.2021.111577
33. Keshvari M, Rahmati M, Mirnasouri R, Chehelcheraghi F. Effects of endurance exercise and Urtica dioica on the functional, histological and molecular aspects of the hippocampus in STZ-induced diabetic rats. J Ethnopharmacol. 2020;256:112801. 10.1016/j.jep.2020.112801
34. Guo RF, Ward PA. Role of oxidants in lung injury during sepsis. Antioxid Redox Signal. 2007;9(11):1991–2002. 10.1089/ars.2007.1785
35. Alsharif KF, Almalki AA, Alsanie WF, Alzahrani KJ, Kabrah SM, Elshopakey GE, et al. Protocatechuic acid attenuates lipopolysaccharide-induced septic lung injury in mice: The possible role through suppressing oxidative stress, inflammation and apoptosis. J Food Biochem. 2021;45(10):e13915. 10.1111/jfbc.13915
36. Hu M, Yang J, Xu Y. Isoorientin suppresses sepsis-induced acute lung injury in mice by activating an EPCR-dependent JAK2/STAT3 pathway. J Mol Histol. 2022 Feb;53(1):97–109. 10.1007/s10735-021-10039-5
37. Bora E-S, Erdoğan M-A, Özkul B, Sever İ-H, Söğüt İ, Hürdağ C, et al. Short-term protective effect of digitoxin in sepsis-induced acute lung injury. Biocell. 2022;46(2):433-9. 10.32604/biocell.2022.018510
38. Niu D, Chen X, Wang T, Wang F, Zhang Q, Xue X, et al. Protective effects of iridoid glycoside from corni fructus on type 2 diabetes with nonalcoholic fatty liver in mice. Biomed Res Int. 2021; 2021:3642463. 10.1155/2021/3642463
39. Park CH, Noh JS, Kim JH, Tanaka T, Zhao Q, Matsumoto K, et al. Evaluation of morroniside, iridoid glycoside from corni fructus on diabetes-induced alterations such as oxidative stress, inflammation, and apoptosis in the liver of type 2 diabetic db/db mice. Biol Pharm Bull. 2011;34(10):1559–65. 10.1248/bpb.34.1559
40. Park CH, Tanaka T, Kim JH, Cho EJ, Park JC, Shibahara N, et al. Hepato-protective effects of loganin, iridoid glycoside from Corni Fructus, against hyperglycemia-activated signaling pathway in liver of type 2 diabetic db/db mice. Toxicology. 2011;290(1):14–21. 10.1016/j.tox.2011.08.004
41. Wang H, Zhou XM, Wu LY, Liu GJ, Xu WD, Zhang XS, et al. Aucubin alleviates oxidative stress and inflammation via Nrf2-mediated signaling activity in experimental traumatic brain injury. J Neuroinflamm. 2020;17(1):188. 10.1186/s12974-020-01863-9
42. Zhang Y, Han D, Yu S, An C, Liu X, Zhong H, et al. Protective effect of iridoid glycosides of the leaves of Syringa oblata Lindl. on dextran sulfate sodium-induced ulcerative colitis by inhibition of the TLR2/4/MyD88/NF-κB signaling pathway. Biomed Res Int. 2020;2020:7650123. 10.1155/2020/7650123
43. Zhao B, Gao W, Gao X, Leng Y, Liu M, Hou J, et al. Sulforaphane attenuates acute lung injury by inhibiting oxidative stress via Nrf2/HO-1 pathway in a rat sepsis model. Int J Clin Exp Pathol. 2017;10(8):9021–8. PMid: 31966772
44. Yuan J, Cheng W, Zhang G, Ma Q, Li X, Zhang B, et al. Protective effects of iridoid glycosides on acute colitis via inhibition of the inflammatory response mediated by the STAT3/NF-κB pathway. Int Immunopharmacol. 2020;81:106240. 10.1016/j.intimp.2020.106240
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Tang, X., & Tang, H. (2022). Cornus iridoid glycoside alleviates sepsis-induced acute lung injury by regulating NF-κB and Nrf2/HO-1 pathways. Allergologia Et Immunopathologia, 50(5), 121-128. https://doi.org/10.15586/aei.v50i5.638
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How to Cite
Tang, X., & Tang, H. (2022). Cornus iridoid glycoside alleviates sepsis-induced acute lung injury by regulating NF-κB and Nrf2/HO-1 pathways. Allergologia Et Immunopathologia, 50(5), 121-128. https://doi.org/10.15586/aei.v50i5.638