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. 2016 Jun 30;25(3):847–854. doi: 10.1007/s10068-016-0140-5

Anti-inflammatory activity of ethanolic extract from skipjack tuna (Katsuwonus pelamis) heart in LPS-induced RAW 264.7 cells and mouse ear edema model

Bo-Kyeong Kang 2, Min-Ji Kim 2, Koth-Bong-Woo-Ri Kim 1, Dong-Hyun Ahn 2,
PMCID: PMC6049154  PMID: 30263344

Abstract

This study investigated the anti-inflammatory activity of the ethanolic extract (THEE) obtained from the heart of skipjack tuna using lipopolysaccharide (LPS)-induced RAW 264.7 cells. THEE markedly suppressed the production of nitric oxide (NO), interleukin-6 (IL-6), tumor necrosis factor-α (TNF-α), and IL-1β in a dose-dependent manner. In addition, THEE decreased the expression of inducible NO synthase (iNOS), cyclooxygenase-2 (COX-2), nuclear factor-kappa B p65 (NF-κB p65), and mitogen-activated protein kinases (MAPKs) including phosphorylated c-Jun NH2-terminal kinase (p-JNK), phosphorylated extracellular signal-related kinase (p-ERK), and p-p38 proteins. Moreover, THEE orally treated at doses of 50, 100, and 250 mg/kg inhibited the croton oil-induced edema formation and the reduction of the epidermal/dermal thickness and the mast cell numbers was observed in histological analysis. There were no mortalities occurred in mice administered THEE at 5,000 mg/kg body weight. Taken together, these results indicate that THEE exerts the anti-inflammatory activities via inhibition of NF-κB and MAPKs activation.

Keywords: tuna heart, anti-inflammatory activity, NF-κB, MAPKs, croton oil-induced edema

References

  • 1.Tizard IR. An introduction inflammation. New York, NY, USA: Saunders College Publishing; 1986. Immunology; pp. 423–441. [Google Scholar]
  • 2.Nakashima H, Kido N, Kobayashi N, Motoki M, Neushul M, Yamamoto N. Purification and characterization of an avian myeloblastosis and human immunodeficiency virus reverse transcriptase inhibitor sulfated polysaccharide extracted from sea algae. Antimicrob. Agents Ch. 1987;31:1524–1528. doi: 10.1128/AAC.31.10.1524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Lawrence T, Willoughby DA, Gilroy DW. Anti-inflammatory lipid mediators and insights into theresolution of inflammation. Nat. Rev. Immunol. 2002;2:787–795. doi: 10.1038/nri915. [DOI] [PubMed] [Google Scholar]
  • 4.Fujiwara N, Kobayashi K. Macrophages in inflammation. Curr. Drug Targets. 2005;4:281–286. doi: 10.2174/1568010054022024. [DOI] [PubMed] [Google Scholar]
  • 5.Tak PP, Firestein GS. NF-ΚB: A key role in inflammatory diseases. J. Clin. Invest. 2001;107:7–11. doi: 10.1172/JCI11830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Oh HS, Kim JS, Heu MS. Preparation of functional seasoning sauce using enzymatic hydrolysates from skipjack tuna cooking drip. J. Korean Soc. Food Sci. Nutr. 2001;36:766–772. doi: 10.3746/jkfn.2007.36.6.766. [DOI] [Google Scholar]
  • 7.Rahman MS, Al-Saidi GS, Guizani N. Thermal characterization of gelatin extracted from yellowfin tuna skin and commercial mammalian gelatin. Food Chem. 2008;108:472–481. doi: 10.1016/j.foodchem.2007.10.079. [DOI] [PubMed] [Google Scholar]
  • 8.Lee HS, Kim HJ, Choi JI, Kim JH, Kim JG, Chun BS, Ahn DH, Chung YJ, Kim YJ, Byun MW, Lee JW. Antioxidant activity of the ethanol extract from cooking drips of Thunus thynnus by gamma irradiation. J. Korean Soc. Food Sci. Nutr. 2008;37:810–814. doi: 10.3746/jkfn.2008.37.6.810. [DOI] [Google Scholar]
  • 9.Jang JR, Kim KK, Mun SB, Lim SY. In vitro anticancer and antioxidant effect of solvent extracts from tuna dried at low temperature vacuum. J. Life Sci. 2009;19:633–638. doi: 10.5352/JLS.2009.19.5.633. [DOI] [Google Scholar]
  • 10.Seo DS, Kim YG, Hwang KH, Lee JK. Preparation of hydroxyapatite powder derived from tuna bone and its sintering property. J. Korean Ceram. Soc. 2008;45:594–599. doi: 10.4191/KCERS.2008.45.1.594. [DOI] [Google Scholar]
  • 11.Kim KS, Jeong BY, Bae TJ, Oh WS. Studies on the isolation, refining and utilization of lecithin from skipjack viscera oil. J. Korean Fish. Soc. 1998;31:895–900. [Google Scholar]
  • 12.Weisz A, Cicatiello L, Esumi H. Regulation of the mouse inducible-type nitric oxide synthase gene promoter by interferon-gamma, bacterial lipopolysaccharide and NG-monomethyl-L-arginine. Biochem. J. 1996;316:209–215. doi: 10.1042/bj3160209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Miyataka M, Rich KA, Ingram M, Yamamoto T, Bing RJ. Nitric oxide, antiinflammatory drugs on renal prostaglandins and cyclooxygenase-2. Hypertension. 2002;39:785–789. doi: 10.1161/hy0302.105689. [DOI] [PubMed] [Google Scholar]
  • 14.Han MH, Kim JW, Kim KY, Kim SG, Yu GJ, Cho YB, Hwang HJ, Kim BW, Kim BW, Kim CM, Choi YH. Single dose oral toxicity of Schisandraesemen essential oil in ICR mice. J. Life Sci. 2014;24:191–195. doi: 10.5352/JLS.2014.24.2.191. [DOI] [Google Scholar]
  • 15.Khair-El-Din T, Sicher SC, Vazquez MA, Chung GW, Stallworth KA, Kitamura K, Miller RT, Lu CY. Transcription of the murine iNOS gene is inhibited by docosahexaenoic acid, a major constituent of fetal and neonatal sera as well as fish oils. J. Exp. Med. 1996;183:1241–1246. doi: 10.1084/jem.183.3.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Erdmann K, Cheung BW, Schroder H. The possible roles of food-derived bioactive peptides in reducing the risk of cardiovascular disease. J. Nutr. Biochem. 2008;19:643–654. doi: 10.1016/j.jnutbio.2007.11.010. [DOI] [PubMed] [Google Scholar]
  • 17.Meisel H F, Gerald RJ. Biofunctional peptides from milk proteins: Mineral binding and cytomodulatory effects. Curr. Pharm. Design. 2003;9:1289–1295. doi: 10.2174/1381612033454847. [DOI] [PubMed] [Google Scholar]
  • 18.Cheong HS. Antioxidant effect of histidine containing low molecular weight peptide isolated from Skipjack boiled extract. Korean J. Food Cook. Sci. 2007;23:221–226. [Google Scholar]
  • 19.Lee SJ, Kim EK, Kim YS, Hwang JW, Lee KH, Choi DK, Kang H, Moon SH, Jeon BT, Park PJ. Purification and characterization of a nitric oxide inhibitory peptide from Ruditapes philippinarum. Food Chem. Toxicol. 2012;50:1660–1666. doi: 10.1016/j.fct.2012.02.021. [DOI] [PubMed] [Google Scholar]
  • 20.Hwang JW, Lee SJ, Kim YS, Kim EK, Ahn CB, Jeon YJ, Moon SH, Jeon BT, Park PJ. Purification and characterization of a novel peptide with inhibitory effects on colitis induced mice by dextran sulfate sodium from enzymatic hydrolysates of Crussostreagigas. Fish Shellfish Immun. 2012;33:993–999. doi: 10.1016/j.fsi.2012.08.017. [DOI] [PubMed] [Google Scholar]
  • 21.Hibi M, Nakajima T, Hirano T. IL-6 cytokine family and signal transduction: A model of the cytokine system. J. Mol. Med. 1996;74:1–12. doi: 10.1007/BF00202068. [DOI] [PubMed] [Google Scholar]
  • 22.Delgado AV, McManus AT, Chambers JP. Production of tumor necrosis factoralpha, interleukin 1-beta, interleukin 2 and interleukin 6 by rat leukocyte subpopulations after exposure to substance P. Neuropeptides. 2003;37:355–361. doi: 10.1016/j.npep.2003.09.005. [DOI] [PubMed] [Google Scholar]
  • 23.Moncada S, Higgs EA. Endogenous nitric oxide: Physiology, pathology and clinical relevance. Eur. J. Clin. Invest. 1991;21:361–374. doi: 10.1111/j.1365-2362.1991.tb01383.x. [DOI] [PubMed] [Google Scholar]
  • 24.Yun HY, Dawson VL, Dawson TM. Neurobiology of nitric oxide. Crit. Rev. Neurobiol. 1996;10:291–316. doi: 10.1615/CritRevNeurobiol.v10.i3-4.20. [DOI] [PubMed] [Google Scholar]
  • 25.Lin WJ, Yeh WC. Implication of toll-like receptor and tumor necrosis factor alpha signaling in septic shock. Shock. 2005;24:206–209. doi: 10.1097/01.shk.0000180074.69143.77. [DOI] [PubMed] [Google Scholar]
  • 26.Ghosh S, Hayden HS. New regulators of NF-ΚB in inflammation. Nat. Rev. Immunol. 2008;8:837–848. doi: 10.1038/nri2423. [DOI] [PubMed] [Google Scholar]
  • 27.Majdalawieh A, Ro HS. Regulation of I?Ba function and NF-ΚB signaling: AEBP1 is a novel proinflammatory mediator in macrophages. Mediat. Inflamm. 2010;2010:1–27. doi: 10.1155/2010/823821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Park HJ, Lee SH, Son DJ, Oh KW, Kim KH, Song HS, Kim GJ, Oh GT, Yoon DY, Hong JT. Antiarthritic effect of bee venom; Inhibition of inflammation mediator generation by suppression of NF-ΚB through interaction with the p50 subunit. Arthritis Rheum. 2004;50:3504–3515. doi: 10.1002/art.20626. [DOI] [PubMed] [Google Scholar]
  • 29.Ahn CB, Cho YS, Je YJ. Purification and anti-inflammatory action of tripeptide from salmon pectoral fin byproduct protein hydrolysate. Food Chem. 2015;168:151–156. doi: 10.1016/j.foodchem.2014.05.112. [DOI] [PubMed] [Google Scholar]
  • 30.Johnson GL, Lapadat R. Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science. 2002;298:1911–1912. doi: 10.1126/science.1072682. [DOI] [PubMed] [Google Scholar]
  • 31.Ryu IH, Cho HB, Kim SB, Seo YJ, Choi CM. The inhibitory effect of Picrasmae lignum on inflammatory responses. J. Orient. Obstet. Gynecol. 2011;24:1–14. [Google Scholar]
  • 32.Kim HR, Kim DW, Jo HS, Cho SB, Park JH, Lee CH, Choi YJ, Yeo EJ, Park SY, Kim ST, Yu YH, Kim DS, Kim HA, Cho SW, Han KH, Park J, Eum WS, Choi SY. Tatbiliveridin reductase A inhibits inflammatory response by regulation of MAPK and NF-ΚB pathways in RAW 264.7 cells and edema mouse model. Mol. Immunol. 2015;63:355–366. doi: 10.1016/j.molimm.2014.09.003. [DOI] [PubMed] [Google Scholar]
  • 33.Park SG, Jegal KH, Jung JY, Back YD, Byun SH, Kim YW, Cho IJ, Park SM, Kim SC. Leonuri fructus ameliorates acute inflammation via the inhibition of NF-ΚBmediated nitric oxide and pro-inflammatory cytokine production. Kor. J. Ori. Med. Physiol. Pathol. 2014;28:178–185. [Google Scholar]
  • 34.Towbin H, Pignat W, Wiesenberg I. Time-dependent cytokine production in the croton oil-induced mouse ear oedema and inhibition by prednisolone. Inflamm. Res. 1995;44:160–161. doi: 10.1007/BF01778311. [DOI] [PubMed] [Google Scholar]
  • 35.Dogne M, Hanson K, Supuran C, Pratico D. Coxibs and cardiovascular side-effects: From light to shadow. Curr. Pharm. Design. 2006;12:917–975. doi: 10.2174/138161206776055949. [DOI] [PubMed] [Google Scholar]

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