Capsosiphon fulvescens suppresses LPS-stimulated inflammatory responses by suppressing TLR4/NF-κB activation in RAW264.7 murine macrophages

Seon Yeong Ji , EunJin Bang , Hyun Hwangbo , Min Yeong Kim , Da Hye Kim , Su Hyun Hong , Shin-Hyung Park , Chang-Young Kwon , Gi-Young Kim , You-Jin Jeon , Suengmok Cho , Yung Hyun Choi

Asian Pacific Journal of Tropical Biomedicine ›› 2024, Vol. 14 ›› Issue (3) : 115 -126.

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Asian Pacific Journal of Tropical Biomedicine ›› 2024, Vol. 14 ›› Issue (3) :115 -126. DOI: 10.4103/apjtb.apjtb_865_23
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Capsosiphon fulvescens suppresses LPS-stimulated inflammatory responses by suppressing TLR4/NF-κB activation in RAW264.7 murine macrophages
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Abstract

Objective: To evaluate the effects of Capsosiphon fulvescens (C. fulvescens) ethanolic extract on inflammation in lipopolysaccharide (LPS)-induced RAW296.7 macrophages. Methods: The protective effects of C. fulvescens ethanolic extract on LPS-induced inflammation in RAW264.7 macrophages were assessed using biochemical analysis, including enzyme-linked immunosorbent assay, quantitative reverse transcription-polymerase chain reaction, and Western blot analysis. To examine reactive oxygen species (ROS) production, flow cytometry analysis, and immunofluorescence staining were used. Furthermore, the modulatory effect of C. fulvescens ethanolic extract on NF-κB activation was investigated. Results: C. fulvescens ethanolic extract significantly attenuated LPS-induced levels of pro-inflammatory cytokines and notably reduced the secretion and mRNA levels of LPS-mediated matrix metalloproteinases. In addition, C. fulvescens ethanolic extract decreased ROS production and suppressed the TLR4/NF-κB signaling pathway. Conclusions: C. fulvescens ethanolic extract alleviates inflammation as well as oxidative stress by modulating the TLR4/NF-κB signaling in LPS-induced RAW264.7 macrophages. C. fulvescens can be used as a potential therapeutic agent to suppress inflammation and oxidative stress-associated diseases.

Keywords

Capsosiphon fulvescens / Inflammation / Oxidative stress / NF-κB / Nrf2 / TLR4

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Seon Yeong Ji, EunJin Bang, Hyun Hwangbo, Min Yeong Kim, Da Hye Kim, Su Hyun Hong, Shin-Hyung Park, Chang-Young Kwon, Gi-Young Kim, You-Jin Jeon, Suengmok Cho, Yung Hyun Choi. Capsosiphon fulvescens suppresses LPS-stimulated inflammatory responses by suppressing TLR4/NF-κB activation in RAW264.7 murine macrophages. Asian Pacific Journal of Tropical Biomedicine, 2024, 14 (3) : 115-126 DOI:10.4103/apjtb.apjtb_865_23

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Conflict of interest statement

The authors declare no potential conflicts of interest.

Funding

This research was funded by Korea Institute of Marine Science & Technology Promotion (KIMST) funded by the Ministry of Oceans and Fisheries, Korea (20220488).

Data availability statement

The data supporting the findings of this study are available from the corresponding authors upon request.

Authors’ contributions

SYJ, SHH, and YHC designed and conceptualized the study. SYJ planned and performed experiments and analyzed the data. EJB, HH, MYK, and SHP validated and reviewed the analysis. EJB reviewed and investigated the data. HH, MYK, DHK, SHP, CYK, GYK, YJJ, and SC provided resources for the experiment. EJB wrote the original draft. EJB and YHC reviewed and edited the manuscript. SHH visualized data in manuscript format. YHC supervised the study. CYK, GYK, YJJ, and SC administered the study project. YHC acquired the funding. All authors have read and agreed to the published version of the manuscript.

References

[1]

Lee E, Song CH, Bae SJ, Ha KT, Karki R. Regulated cell death pathways and their roles in homeostasis, infection, inflammation, and tumorigenesis. Exp Mol Med 2023; 55(8): 1632-1643.

[2]

Pang Y, Wu L, Tang C, Wang H, Wei Y. Autophagy-inflammation interplay during infection: Balancing pathogen clearance and host inflammation. Front Pharmacol 2022; 13: 832750.

[3]

Greten FR, Grivennikov SI. Inflammation and cancer: Triggers, mechanisms, and consequences. Immunity 2019; 51(1): 27-41.

[4]

Facchin BM, Dos Reis GO, Vieira GN, Mohr ETB, da Rosa JS, Kretzer IF, et al. Inflammatory biomarkers on an LPS-induced RAW 264.7 cell model: A systematic review and meta-analysis. Inflamm Res 2022; 71(7-8): 741-758.

[5]

Ngkelo A, Meja K, Yeadon M, Adcock I, Kirkham PA. LPS induced inflammatory responses in human peripheral blood mononuclear cells is mediated through NOX4 and Giα dependent PI-3kinase signalling. J Inflamm (Lond) 2012; 9(1): 1. doi: 10.1186/1476-9255-9-1.

[6]

Coutinho-Wolino KS, Almeida PP, Mafra D, Stockler-Pinto MB. Bioactive compounds modulating Toll-like 4 receptor (TLR4)-mediated inflammation: Pathways involved and future perspectives. Nutr Res 2022; 107: 96-116.

[7]

Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine 2008; 42(2): 145-151.

[8]

Feghali CA, Wright TM. Cytokines in acute and chronic inflammation. Front Biosci 1997; 2: d12-d26.

[9]

Sies H, Jones DP. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat Rev Mol Cell Biol 2020; 21(7): 363-383.

[10]

Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antoxid Redox Signal 2014; 20(7): 1126-1167.

[11]

Capece D, Verzella D, Flati I, Arboretto P, Cornice J, Franzoso G. NF-κB: Blending metabolism, immunity, and inflammation. Trends Immunol 2022; 43(9): 757-775.

[12]

Lingappan K. NF-κB in oxidative stress. Curr Opin Toxicol 2018; 7: 81-86.

[13]

Sharif O, Bolshakov VN, Raines S, Newham P, Perkins ND. Transcriptional profiling of the LPS induced NF-kappaB response in macrophages. BMC Immunol 2007; 8. doi: 10.1186/1471-2172-8-1.

[14]

Wan J, Shan Y, Fan Y, Fan C, Chen S, Sun J, et al. NF-κB inhibition attenuates LPS-induced TLR4 activation in monocyte cells. Mol Med Rep 2016; 14(5): 4505-4510.

[15]

Chaudhary MR, Chaudhary S, Sharma Y, Singh TA, Mishra AK, Sharma S, et al. Aging, oxidative stress and degenerative diseases: Mechanisms, complications and emerging therapeutic strategies. Biogerontology 2023; 24(5): 609-662.

[16]

Ray PD, Huang BW, Tsuji Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 2012; 24(5): 981-990.

[17]

Synytsya A, Choi DJ, Pohl R, Na YS, Capek P, Lattová E, et al. Structural features and anti-coagulant activity of the sulphated polysaccharide SPS-CF from a green alga Capsosiphon fulvescens. Mar Biotechnol (NY) 2015; 17(6): 718-735.

[18]

Sun SM, Yang SH, Golokhvast KS, Le B, Chung G. Reconstructing the phylogeny of Capsosiphon fulvescens (Ulotrichales, Chlorophyta) from Korea based on rbcL and 18S rDNA sequences. Biomed Res Int 2016; 2016. doi: 10.1155/2016/1462916.

[19]

Mun YJ, Yoo HJ, Lee HE, Kim JH, Pyo HB, Woo WH. Inhibitory effect on the melanogenesis of Capsosiphon fulvescens. Yakhak Hoeji 2005; 49: 375-379.

[20]

Kwon MJ, Nam TJ. A polysaccharide of the marine alga Capsosiphon fulvescens induces apoptosis in AGS gastric cancer cells via an IGF-IR-mediated PI3K/Akt pathway. Cell Bio Int 2007; 31(8): 768-775.

[21]

Kwon MJ, Nam TJ. Effects of mesangi (Capsosiphon fulvescens) powder on lipid metabolism in high cholesterol fed rats. J Kor Soc Food Sci Nutr 2006; 35(5): 530-535.

[22]

Fang Z, Yang Jeong S, Ah Jung H, Sue Choi J, Sun Min B, Hee Woo M. Capsofulvesins A-C, cholinesterase inhibitors from Capsosiphon fulvescens. Chem Pharm Bull (Tokyo) 2012; 60(11): 1351-1358.

[23]

Oh JH, Choi YH, Nam TJ. Glycoproteins of Capsosiphon fulvescens modulate synaptic clustering of PSD95 and prevent social isolation-induced cognitive decline in aged male rats. J Nutr Biochem 2022; 107. doi: 10.1016/j.jnutbio.2022.109054.

[24]

Hong CO, Nam MH, Oh JS, Lee JW, Kim CT, Park KW, et al. Pheophorbide a from Capsosiphon fulvescens inhibits advanced glycation end products mediated endothelial dysfunction. Planta Med 2019; 82(1-2): 46-57.

[25]

Karima G, Shin K, Jeong, J, Choi D, Hwang KG, Hong JW. Stem cell oriented exosomes regulate cell proliferation in hepatoma carcinoma. Biotechnol Bioprocess Eng 2023; 28(2): 263-273.

[26]

Yang EJ, Yim EY, Song G, Kim GO, Hyun CG. Inhibition of nitric oxide production in lipopolysaccharide-activated RAW 264.7 macrophages by Jeju plant extracts. Interdiscip Toxicol 2009; 2(4): 245-249.

[27]

Kwon Y, Lee H, Park H, Lee B, Kwon TU, Kwon YJ, et al. YPEL3 expression induces cellular senescence via the Hippo signaling pathway in human breast cancer cells. Toxicol Res 2023; 39(4): 711-719.

[28]

Vo TT, Tran Q, Hong Y, Lee H, Cho H, Kim M, et al. AXL is required for hypoxia-mediated hypoxia-inducible factor-1 alpha function in glioblastoma. Toxicol Res 2023; 39(4): 669-679.

[29]

Gamal-Eldeen AM, Amer H, Helmy WA. Cancer chemopreventive and anti-inflammatory activities of chemically modified guar gum. Chem Biol Interact 2006; 161(3): 229-240.

[30]

Park C, Lee H, Kim SO, Lee EW, Lee HT, Kwon HJ, et al. The preventive effect of Mori ramulus on oxidative stress-induced cellular damage in skeletal L6 myoblasts through Nrf2-mediated activation of HO-1. Toxicol Res 2022; 39(1): 25-36.

[31]

Kim JJ, Lee NK, Ryu DE, Ko BH, Kim JH, Rhee JK, et al. Highly porous and rigid, full-thickness human skin model from the slime-webbed fiber scaffold. Biotechnol Bioprocess Eng 2023; 28(2): 246-254.

[32]

Lundberg JO, Weitzberg E. Nitric oxide signaling in health and disease. Cell 2022; 185(16): 2853-2878.

[33]

Choi BM, Pae HO, Jang SI, Kim YM, Chung HT. Nitric oxide as a pro-apoptotic as well as anti-apoptotic modulator. J Biochem Mol Biol 2002; 35(1): 116-126.

[34]

Sharma JN, Al-Omran A, Parvathy SS. Role of nitric oxide in inflammatory diseases. Inflammopharmacology 2007; 15(6): 252-259.

[35]

Nørregaard R, Kwon TH, Frøkiær J. Physiology and pathophysiology of cyclooxygenase-2 and prostaglandin E2 in the kidney . Kidney Res Clin Pract 2015; 34(4): 194-200.

[36]

Jin K. Qian C, Lin J, Liu B. Cyclooxygenase-2-prostaglandin E2 pathway: A key player in tumor-associated immune cells . Front Oncol 2023; 13. doi: 10.3389/fonc.2023.1099811.

[37]

Arango Duque G, Descoteaux A. Macrophage cytokines: Involvement in immunity and infectious diseases. Front Immunol 2014; 5. doi: 10.3389/fimmu.2014.00491.

[38]

Liu X, Yin S, Chen Y, Wu Y, Zheng W, Dong H, et al. LPS-induced proinflammatory cytokine expression in human airway epithelial cells and macrophages via NF-κB, STAT3 or AP-1 activation. Mol Med Rep 2018; 17(4): 5484-5491.

[39]

de Almeida LGN, Thode H, Eslambolchi Y, Chopra S, Young D, Gill S, et al. Matrix metalloproteinases: From molecular mechanisms to physiology, pathophysiology, and pharmacology. Pharmacol Rev 2022; 74(3): 712-768.

[40]

Ho HH, Antoniv TT, Ji JD, Ivashkiv LB. Lipopolysaccharide-induced expression of matrix metalloproteinases in human monocytes is suppressed by IFN-gamma via superinduction of ATF-3 and suppression of AP-1. J Immunol 2008; 181(7): 5089-5097.

[41]

Cabral-Pacheco GA, Garza-Veloz I, Castruita-De la Rosa C, Ramirez-Acuña JM, Perez-Romero BA, Guerrero-Rodriguez JF, et al. The roles of matrix metalloproteinases and their inhibitors in human diseases. Int J Mol Sci 2020; 21(24). doi: 10.3390/ijms21249739.

[42]

Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82(1): 47-95.

[43]

Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007; 47: 89-116.

[44]

Kansanen E, Kuosmanen SM, Leinonen H, Levonen AL. The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer. Redox Biol 2013; 1(1): 45-49.

[45]

Liu T, Zhang L, Joo D, Sun SC. NF-κB signaling in inflammation. Signal Transduct Target Ther 2017; 2: 17023.

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