Volume 12, Issue 4 (Vol.12 No.4 Jan 2024)                   rbmb.net 2024, 12(4): 566-574 | Back to browse issues page

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Amin Mohedin J, Rezaiemanesh A, Asadi S, Haddadi M, Abdul Ahmed B, Gorgin Karaji A et al . Resolvin D1 (Rvd1) Attenuates In Vitro LPS-Stimulated Inflammation Through Downregulation of miR-155, miR -146, miR -148 and Krupple Like Factor 5. rbmb.net 2024; 12 (4) :566-574
URL: http://rbmb.net/article-1-1242-en.html
Department of immunology, school of medicine, Kermanshah University of Medical Science, Kermanshah, Iran.
Abstract:   (416 Views)
Background: Chronic inflammation is associated with many inflammatory diseases. Specialized pro-resolving mediators (SPMs) are well known for their crucial role in promoting the resolution phase of inflammation and restoring tissue homeostasis. Resolvin D1 (RvD1) is an endogenous omega-3-derived lipid mediator with pro-resolving activity. This study aimed to evaluate the effect of Resolvin D1 (RvD1) on some inflammatory miRNAs (mir-155-5p, miR146a-5p and miR148-3p) and Krüppel-like factors 5 (KLF5) in an LPS-stimulated THP-1 preclinical model of inflammation.

Methods: PMA-differentiated THP-1 cells (macrophages) were pre-incubated with or without various concentrations of RvD1 (10, 50, or 100 nM) for 2 h prior to stimulation by 1 μg/ml LPS. Un-stimulated PMA-differentiated THP-1 cells were as the control group. Then, the expression levels of target genes were evaluated by real-time PCR.

Results: Compared with untreated macrophages, stimulation with 1 µg/ml LPS increased mRNA expression levels of TNF-α, KLF5, miR-155-5p, miR-146-5p, and miR-148a-3p. When the cells were exposed to various concentrations (10, 50 and 100 nM) of RvD1 for 2 h prior to LPS stimulation, the TNF-α, KLF5, miR-155-5p, miR-146-5p, and miR-148a-3p mRNA expression levels were significantly downregulated in a dose-dependent manner, compared to the LPS group.

Conclusion: The results demonstrate that RvD1 can attenuate inflammatory response in LPS-stimulated macrophages. Our data also showed that RvD1 may exert anti-inflammatory effects by inhibiting miR-155-5p, miR-146a-5p, and miR-148-3p.
Full-Text [PDF 490 kb]   (79 Downloads)    
Type of Article: Original Article | Subject: Immunology
Received: 2023/09/9 | Accepted: 2023/11/15 | Published: 2024/07/2

References
1. Medzhitov R. Inflammation 2010: new adventures of an old flame. Cell. 2010;140(6):771-6. [DOI:10.1016/j.cell.2010.03.006] [PMID]
2. Nathan C, Ding A. Nonresolving inflammation. Cell. 2010;140(6):871-82. [DOI:10.1016/j.cell.2010.02.029] [PMID]
3. Chen S, Saeed A, Liu Q, Jiang Q, Xu H, Xiao GG, et al. Macrophages in immunoregulation and therapeutics. Signal Transduct Target Ther. 2023;8(1):207. [DOI:10.1038/s41392-023-01452-1] [PMID] []
4. Wang N, Liang H, Zen K. Molecular mechanisms that influence the macrophage m1-m2 polarization balance. Front Immunol. 2014;5:614. [DOI:10.3389/fimmu.2014.00614] [PMID] []
5. Das K, Rao LVM. The Role of microRNAs in Inflammation. Int J Mol Sci. 2022;23(24). [DOI:10.3390/ijms232415479] [PMID] []
6. Li H, Jiang T, Li MQ, Zheng XL, Zhao GJ. Transcriptional Regulation of Macrophages Polarization by MicroRNAs. Front Immunol. 2018;9:1175. [DOI:10.3389/fimmu.2018.01175] [PMID] []
7. Huang F, Zhao JL, Wang L, Gao CC, Liang SQ, An DJ, et al. miR-148a-3p Mediates Notch Signaling to Promote the Differentiation and M1 Activation of Macrophages. Front Immunol. 2017;8:1327. [DOI:10.3389/fimmu.2017.01327] [PMID] []
8. Ma Y, Shen N, Wicha MS, Luo M. The Roles of the Let-7 Family of MicroRNAs in the Regulation of Cancer Stemness. Cells. 2021;10(9). [DOI:10.3390/cells10092415] [PMID] []
9. Sheedy FJ. Turning 21: Induction of miR-21 as a Key Switch in the Inflammatory Response. Front Immunol. 2015;6:19. [DOI:10.3389/fimmu.2015.00019] [PMID] []
10. Sweet DR, Fan L, Hsieh PN, Jain MK. Kruppel-Like Factors in Vascular Inflammation: Mechanistic Insights and Therapeutic Potential. Front Cardiovasc Med. 2018;5:6. [DOI:10.3389/fcvm.2018.00006] [PMID] []
11. Sur I, Unden AB, Toftgard R. Human Kruppel-like factor5/KLF5: synergy with NF-kappaB/Rel factors and expression in human skin and hair follicles. Eur J Cell Biol. 2002;81(6):323-34. [DOI:10.1078/0171-9335-00257] [PMID]
12. Aizawa K, Suzuki T, Kada N, Ishihara A, Kawai-Kowase K, Matsumura T, et al. Regulation of platelet-derived growth factor-A chain by Kruppel-like factor 5: new pathway of cooperative activation with nuclear factor-kappaB. J Biol Chem. 2004;279(1):70-6. [DOI:10.1074/jbc.M306621200] [PMID]
13. Fujiu K, Manabe I, Nagai R. Renal collecting duct epithelial cells regulate inflammation in tubulointerstitial damage in mice. J Clin Invest. 2011;121(9):3425-41. [DOI:10.1172/JCI57582] [PMID] []
14. Zheng B, Yin WN, Suzuki T, Zhang XH, Zhang Y, Song LL, et al. Exosome-Mediated miR-155 Transfer from Smooth Muscle Cells to Endothelial Cells Induces Endothelial Injury and Promotes Atherosclerosis. Mol Ther. 2017;25(6):1279-94. [DOI:10.1016/j.ymthe.2017.03.031] [PMID] []
15. Lotfi R, Rezaiemanesh A, Mortazavi SH, Karaji AG, Salari F. Immunoresolvents in asthma and allergic diseases: Review and update. J Cell Physiol. 2019;234(6):8579-96. [DOI:10.1002/jcp.27836] [PMID]
16. Ozgul Ozdemir RB, Soysal Gunduz O, Ozdemir AT, Akgul O. Low levels of pro-resolving lipid mediators lipoxin-A4, resolvin-D1 and resolvin-E1 in patients with rheumatoid arthritis. Immunol Lett. 2020;227:34-40. [DOI:10.1016/j.imlet.2020.08.006] [PMID]
17. Yang A, Wu Y, Yu G, Wang H. Role of specialized pro-resolving lipid mediators in pulmonary inflammation diseases: mechanisms and development. Respir Res. 2021;22(1):204. [DOI:10.1186/s12931-021-01792-y] [PMID] []
18. Fredman G, Hellmann J, Proto JD, Kuriakose G, Colas RA, Dorweiler B, et al. An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques. Nature communications. 2016;7:12859. [DOI:10.1038/ncomms12859] [PMID] []
19. Recchiuti A, Serhan CN. Pro-Resolving Lipid Mediators (SPMs) and Their Actions in Regulating miRNA in Novel Resolution Circuits in Inflammation. Front Immunol. 2012;3:298. [DOI:10.3389/fimmu.2012.00298] [PMID] []
20. Cao D, Pi J, Shan Y, Tang Y, Zhou P. Anti-inflammatory effect of Resolvin D1 on LPS-treated MG-63 cells. Exp Ther Med. 2018;16(5):4283-8. [DOI:10.3892/etm.2018.6721] [PMID] []
21. Liao Z, Dong J, Wu W, Yang T, Wang T, Guo L, et al. Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARgamma/NF-kappaB pathway. Respir Res. 2012;13(1):110. [DOI:10.1186/1465-9921-13-110] [PMID] []
22. Liu Y, Zhou D, Long FW, Chen KL, Yang HW, Lv ZY, et al. Resolvin D1 protects against inflammation in experimental acute pancreatitis and associated lung injury. Am J Physiol Gastrointest Liver Physiol. 2016;310(5):G303-9. [DOI:10.1152/ajpgi.00355.2014] [PMID]
23. Bento AF, Claudino RF, Dutra RC, Marcon R, Calixto JB. Omega-3 fatty acid-derived mediators 17(R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J Immunol. 2011;187(4):1957-69. [DOI:10.4049/jimmunol.1101305] [PMID]
24. Murakami T, Suzuki K, Tamura H, Nagaoka I. Suppressive action of resolvin D1 on the production and release of septic mediators in D-galactosamine-sensitized endotoxin shock mice. Exp Ther Med. 2011;2(1):57-61. [DOI:10.3892/etm.2010.170] [PMID] []
25. Eickmeier O, Seki H, Haworth O, Hilberath JN, Gao F, Uddin M, et al. Aspirin-triggered resolvin D1 reduces mucosal inflammation and promotes resolution in a murine model of acute lung injury. Mucosal Immunol. 2013;6(2):256-66. [DOI:10.1038/mi.2012.66] [PMID] []
26. Sakurai H, Suzuki S, Kawasaki N, Nakano H, Okazaki T, Chino A, et al. Tumor necrosis factor-alpha-induced IKK phosphorylation of NF-kappaB p65 on serine 536 is mediated through the TRAF2, TRAF5, and TAK1 signaling pathway. J Biol Chem. 2003;278(38):36916-23. [DOI:10.1074/jbc.M301598200] [PMID]
27. Lee IT, Yang CM. Inflammatory signalings involved in airway and pulmonary diseases. Mediators Inflamm. 2013;2013:791231. [DOI:10.1155/2013/791231] [PMID] []
28. Wang B, Gong X, Wan JY, Zhang L, Zhang Z, Li HZ, Min S. Resolvin D1 protects mice from LPS-induced acute lung injury. Pulm Pharmacol Ther. 2011;24(4):434-41. [DOI:10.1016/j.pupt.2011.04.001] [PMID]
29. Duffield JS, Hong S, Vaidya VS, Lu Y, Fredman G, Serhan CN, Bonventre JV. Resolvin D series and protectin D1 mitigate acute kidney injury. J Immunol. 2006;177(9):5902-11. [DOI:10.4049/jimmunol.177.9.5902] [PMID]
30. Yin Y, Chen F, Wang W, Wang H, Zhang X. Resolvin D1 inhibits inflammatory response in STZ-induced diabetic retinopathy rats: Possible involvement of NLRP3 inflammasome and NF-kappaB signaling pathway. Mol Vis. 2017;23:242-50.
31. Paul P, Chakraborty A, Sarkar D, Langthasa M, Rahman M, Bari M, et al. Interplay between miRNAs and human diseases. J Cell Physiol. 2018;233(3):2007-18. [DOI:10.1002/jcp.25854] [PMID]
32. Graff JW, Dickson AM, Clay G, McCaffrey AP, Wilson ME. Identifying functional microRNAs in macrophages with polarized phenotypes. J Biol Chem. 2012;287(26):21816-25. [DOI:10.1074/jbc.M111.327031] [PMID] []
33. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A. 2006;103(33):12481-6. [DOI:10.1073/pnas.0605298103] [PMID] []
34. Cai X, Yin Y, Li N, Zhu D, Zhang J, Zhang CY, Zen K. Re-polarization of tumor-associated macrophages to pro-inflammatory M1 macrophages by microRNA-155. J Mol Cell Biol. 2012;4(5):341-3. [DOI:10.1093/jmcb/mjs044] [PMID]
35. Bala S, Marcos M, Kodys K, Csak T, Catalano D, Mandrekar P, Szabo G. Up-regulation of microRNA-155 in macrophages contributes to increased tumor necrosis factor alpha (TNFalpha) production via increased mRNA half-life in alcoholic liver disease. J Biol Chem. 2011;286(2):1436-44. [DOI:10.1074/jbc.M110.145870] [PMID] []
36. Tili E, Michaille JJ, Cimino A, Costinean S, Dumitru CD, Adair B, et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol. 2007;179(8):5082-9. [DOI:10.4049/jimmunol.179.8.5082] [PMID]
37. Teng C, Lin C, Huang F, Xing X, Chen S, Ye L, et al. Intracellular codelivery of anti-inflammatory drug and anti-miR 155 to treat inflammatory disease. Acta Pharm Sin B. 2020;10(8):1521-33. [DOI:10.1016/j.apsb.2020.06.005] [PMID] []
38. Sun Y, Cai J, Ma F, Lu P, Huang H, Zhou J. miR-155 mediates suppressive effect of progesterone on TLR3, TLR4-triggered immune response. Immunol Lett. 2012;146(1-2):25-30. [DOI:10.1016/j.imlet.2012.04.007] [PMID]
39. Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, et al. Expression of MicroRNA-146a in osteoarthritis cartilage. Arthritis Rheum. 2009;60(4):1035-41. [DOI:10.1002/art.24404] [PMID] []
40. Wang S, Yang Y, Suen A, Zhu J, Williams B, Hu J, et al. Role of extracellular microRNA-146a-5p in host innate immunity and bacterial sepsis. iScience. 2021;24(12):103441. [DOI:10.1016/j.isci.2021.103441] [PMID] []
41. Rotllan N, Zhang X, Canfran-Duque A, Goedeke L, Grinan R, Ramirez CM, et al. Antagonism of miR-148a attenuates atherosclerosis progression in APOB(TG)Apobec(-/-)Ldlr(+/-) mice: A brief report. Biomed Pharmacother. 2022;153:113419. [DOI:10.1016/j.biopha.2022.113419] [PMID] []
42. Kumekawa M, Fukuda G, Shimizu S, Konno K, Odawara M. Inhibition of monocyte chemoattractant protein-1 by Kruppel-like factor 5 small interfering RNA in the tumor necrosis factor- alpha-activated human umbilical vein endothelial cells. Biol Pharm Bull. 2008;31(8):1609-13. [DOI:10.1248/bpb.31.1609] [PMID]
43. Chen HL, Chong IW, Lee YC, Tsai JR, Yuan SS, Wang HM, et al. Kruppel-like factor 5 mediates proinflammatory cytokine expression in lipopolysaccharide-induced acute lung injury through upregulation of nuclear factor-kappaB phosphorylation in vitro and in vivo. Mediators Inflamm. 2014;2014:281984. [DOI:10.1155/2014/281984] [PMID] []
44. Huang HL, Yang WY, Pu HF, Tsai TH, Lin CH, Chen NJ, Tarng DC. Kruppel-like factor 5 associates with melamine-cyanurate crystal-induced nephritis in rats. Nephrol Dial Transplant. 2013;28(10):2477-83. [DOI:10.1093/ndt/gft308] [PMID]

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