PDF herunterladen
CC BY-NC-ND 4.0 · Planta Medica International Open 2022; 9(01): e80-e89
DOI: 10.1055/a-1729-3654
Original Papers

Time-Dependent Anti-inflammatory Effects of a Lipid Extract from Macrocystis pyrifera on Toll-Like Receptor 2 Signaling in Human THP-1 Monocytes

Jamie Mei Lin Kok
1   Department of Pharmacology and Toxicology, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand
,
Georgina Dowd
2   The New Zealand Institute for Plant & Food Research Limited, Nelson, New Zealand
,
Jaydee Cabral
3   Department of Chemistry, University of Otago, Dunedin, New Zealand
,
Lyn Wise
1   Department of Pharmacology and Toxicology, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand
› Institutsangaben
› Weitere Informationen
   Lizenzen und Reprints

Abstract

Seaweeds reportedly contain anti-inflammatory compounds; however, little is known about the therapeutic potential of Macrocystis pyrifera. This study investigated the anti-inflammatory properties of a methanol:chloroform extract, chromatographic fractions, and fatty acids identified from M. pyrifera (Linnaeus) C. Agardh. In human THP-1 monocytes stimulated with the Toll-like receptor 2 agonist lipoteichoic acid, the extract decreased mRNA and protein levels of interleukin-1β, interleukin-8, and monocyte chemoattractant protein-1 to varied degrees at nontoxic concentrations. The greatest anti-inflammatory effects were elicited when the extract was applied between 6 h prior to, and 6 h after, the stimuli. Reduced levels of nuclear factor kappa-light-chain-enhancer of activated B cells signaling proteins were observed in extract-treated cells, with a significant decrease in the myeloid differentiation factor 88 protein abundance relative to stimulated THP-1 cells. Chromatographic fractionation of the extract yielded 40 fractions, of which fraction F25 exhibited the greatest inhibition of monocyte chemoattractant protein-1 production in activated THP-1 cells. Fatty acids abundant within the extract and F25 were identified then tested, individually and in combination, for their anti-inflammatory effects. Myristic acid, palmitoleic acid, and α-linolenic acid, but not the fatty acid combination, inhibited lipoteichoic acid-stimulated monocyte chemoattractant protein-1 production without compromising THP-1 cell viability. These findings indicate that the fatty acid-rich extract and fraction from M. pyrifera provide anti-inflammatory and cytoprotective effects that may be beneficial for use as a therapeutic.

Key words

Macrocystis pyrifera (Linnaeus) C. Agardh - Phaeophyta - Laminariaceae - fractionation - fatty acid - inflammation - Toll-like receptor - NFκΒ

Supplementary Material



Publikationsverlauf

Eingereicht: 19. September 2021
Eingereicht: 13. Dezember 2021

Angenommen: 22. Dezember 2021

Artikel online veröffentlicht:
15. März 2022

© 2022. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

Georg Thieme Verlag
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Hernandez-Carmona G, Rodriguez E, Casas M, Sánchez I. Evaluation of the beds of Macrocystis pyrifera (Phaeophyta, Laminariales) in the Baja California Peninsula, Mexico. III. Summer 1986 and seasonal variation. Cienc Mar 1991; 17: 121-145
    CrossrefPubMedSuche in Google Scholar
  • 2 Buschmann AH, Camus C, Infante J, Neori A, Israel Á, Hernández-González MC. Pereda SV, Gomez-Pinchetti JL, Golberg A, Tadmor-Shalev N. Seaweed production: overview of the global state of exploitation, farming and emerging research activity. Eur J Phycol 2017; 52: 391-406
    CrossrefPubMedSuche in Google Scholar
  • 3 Purcell-Meyerink D, Packer MA, Wheeler TT, Hayes M. Aquaculture Production of the Brown Seaweeds Laminaria digitata and Macrocystis pyrifera: Applications in Food and Pharmaceuticals. Molecules 2021; 26: 1306
    CrossrefPubMedSuche in Google Scholar
  • 4 Fernando IP, Kim M, Son KT, Jeong Y, Jeon YJ. Antioxidant Activity of Marine Algal Polyphenolic Compounds: A Mechanistic Approach. J Med Food 2016; 19: 615-628
    CrossrefPubMedSuche in Google Scholar
  • 5 Netea MG, Balkwill F, Chonchol M, Cominelli F, Donath MY, Giamarellos-Bourboulis EJ. Golenbock D, Gresnigt MS, Heneka MT, Hoffman HM, Hotchkiss R, Joosten LAB, Kastner DL, Korte M, Latx E, Libby P, Mandrup-Poulsen T, Mantovani A, Mills KHG, Nowak KL, O'Neill LA, Pickkers P, van der Poll T, Ridker PM, Schalkwijk J, Schwartz DA, Siegmund B, Steer CJ, Tilg H, van der Meer JWM, van der Veerdonk FL, Dinarell CA. A guiding map for inflammation. Nat Immunol 2017; 18: 826-831
    CrossrefPubMedSuche in Google Scholar
  • 6 Kawai T, Akira S. Signaling to NF-κB by Toll-like receptors. Trends Mol Med 2007; 13: 460-469
    CrossrefPubMedSuche in Google Scholar
  • 7 Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 2009; 22: 240-273
    CrossrefPubMedSuche in Google Scholar
  • 8 Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T. Takeda K, Akira S. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999; 11: 443-451
    CrossrefPubMedSuche in Google Scholar
  • 9 Munford RS. Sensing gram-negative bacterial lipopolysaccharides: a human disease determinant?. Infect Immun 2008; 76: 454-465
    CrossrefPubMedSuche in Google Scholar
  • 10 Fournier B. The function of TLR2 during staphylococcal diseases. Front Cell Infect Microbiol 2013; 2: 167, 1–8
    CrossrefPubMedSuche in Google Scholar
  • 11 Aliprantis AO, Yang RB, Weiss DS, Godowski P, Zychlinsky A. The apoptotic signaling pathway activated by Toll-like receptor-2. EMBO J 2000; 19: 3325-3336
    CrossrefPubMedSuche in Google Scholar
  • 12 Lee J, Banu SK, Subbarao T, Starzinski-Powitz A, Arosh JA. Selective inhibition of prostaglandin E2 receptors EP2 and EP4 inhibits invasion of human immortalized endometriotic epithelial and stromal cells through suppression of metalloproteinases. Mol Cell Endocrinol 2011; 332: 306-313
    CrossrefPubMedSuche in Google Scholar
  • 13 Sostres C, Gargallo CJ, Arroyo MT, Lanas A. Adverse effects of non-steroidal anti-inflammatory drugs (NSAIDs, aspirin and coxibs) on upper gastrointestinal tract. Best Pract Res Clin Gastroentero 2010; 24: 121-132
    CrossrefPubMedSuche in Google Scholar
  • 14 Hörl WH. Nonsteroidal anti-inflammatory drugs and the kidney. Pharmaceuticals 2010; 3: 2291-2321
    CrossrefPubMedSuche in Google Scholar
  • 15 Wöhrl S. NSAID hypersensitivity – recommendations for diagnostic work up and patient management. Allgro J Int 2018; 27: 114-121
    PubMedSuche in Google Scholar
  • 16 Robertson RC, Guihéneuf F, Bahar B, Schmid M, Stengel DB, Fitzgerald GF. Ross RP, Stanton C. The anti-inflammatory effect of algae-derived lipid extracts on lipopolysaccharide (LPS)-stimulated human THP-1 macrophages. Mar Drugs 2015; 13: 5402-5424
    CrossrefPubMedSuche in Google Scholar
  • 17 Kim MM, Rajapakse N, Kim SK. Anti-inflammatory effect of Ishige okamurae ethanolic extract via inhibition of NF-kappaB transcription factor in RAW 264.7 cells. Phytother Res 2009; 23: 628-634
    CrossrefPubMedSuche in Google Scholar
  • 18 Heo SJ, Ko SC, Kang SM, Kang HS, Kim JP, Kim SH. Lee KW, Cho MG, Jeon YJ. Cytoprotective effect of fucoxanthin isolated from brown algae Sargassum siliquastrum against H2O2-induced cell damage. Eur Food Res Technol 2008; 228: 145-151
    CrossrefPubMedSuche in Google Scholar
  • 19 Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH. Affan A, Oh C, Jung WK, Jeon YJ. Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem Toxicol 2010; 48: 2045-2051
    CrossrefPubMedSuche in Google Scholar
  • 20 Kim KN, Heo SJ, Yoon WJ, Kang SM, Ahn G, Yi TH, Jeon YJ. Fucoxanthin inhibits the inflammatory response by suppressing the activation of NF-κB and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur J Pharmacol 2010; 649: 369-375
    CrossrefPubMedSuche in Google Scholar
  • 21 Zhang W, Oda T, Yu Q, Jin JO. Fucoidan from Macrocystis pyrifera has powerful immune-modulatory effects compared to three other fucoidans. Mar Drugs 2015; 13: 1084-1104
    CrossrefPubMedSuche in Google Scholar
  • 22 Ortiz J, Uquiche E, Robert P, Romero N, Quitral V, Llantén C. Functional and nutritional value of the Chilean seaweeds Codium fragile, Gracilaria chilensis and Macrocystis pyrifera. Eur J Lipid Sci Technol 2009; 111: 320-327
    CrossrefPubMedSuche in Google Scholar
  • 23 Nguyen S, Nguyen H, Truong K. Comparative cytotoxic effects of methanol, ethanol and DMSO on human cancer cell lines. Biomed Res Ther 2020; 7: 3855-3859
    CrossrefPubMedSuche in Google Scholar
  • 24 Iyer SS, Cheng G. Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease. Crit Rev Immunol 2012; 32: 23-63
    CrossrefPubMedSuche in Google Scholar
  • 25 Gil TY, Kang YM, Eom YJ, Hong CH, An HJ. Anti-Atopic Dermatitis Effect of Seaweed Fulvescens Extract via Inhibiting the STAT1 Pathway. Mediators Inflamm 2019; 2019: 3760934
    PubMedSuche in Google Scholar
  • 26 Khan MN, Cho JY, Lee MC, Kang JY, Park NG, Fujii H. Hong YK. Isolation of two anti-inflammatory and one pro-inflammatory polyunsaturated fatty acids from the brown seaweed Undaria pinnatifida. J Agric Food Chem 2007; 55: 6984-6988
    CrossrefPubMedSuche in Google Scholar
  • 27 Jayawardena TU, Kim HS, Sanjeewa KA, Kim SY, Rho JR, Jee Y. Ahn G, Jeon YJ. Sargassum horneri and isolated 6-hydroxy-4, 4, 7a-trimethyl-5, 6, 7, 7a-tetrahydrobenzofuran-2 (4H)-one (HTT); LPS-induced inflammation attenuation via suppressing NF-κB, MAPK and oxidative stress through Nrf2/HO-1 pathways in RAW 264.7 macrophages. Algal Res 2019; 40: 101513
    CrossrefPubMedSuche in Google Scholar
  • 28 Jayawardena TU, Sanjeewa K, Nagahawatta D, Lee HG, Lu YA, Vaas A. Abeytunga DTU, Nanayakkara CM, Lee DS, Jeon YJ. Anti-Inflammatory Effects of Sulfated Polysaccharide from Sargassum Swartzii in Macrophages via Blocking TLR/NF-Κβ Signal Transduction. Mar Drugs 2020; 18: 601
    CrossrefPubMedSuche in Google Scholar
  • 29 Xia S, Wang K, Wan L, Li A, Hu Q, Zhang C. Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Mar Drugs 2013; 11: 2667-2681
    CrossrefPubMedSuche in Google Scholar
  • 30 Souza CO, Teixeira AA, Biondo LA, Silveira LS, Calder PC, Rosa Neto JC. Palmitoleic acid reduces the inflammation in LPS-stimulated macrophages by inhibition of NFκB, independently of PPARs. Clin Exp Pharmacol Physiol 2017; 44: 566-575
    CrossrefPubMedSuche in Google Scholar
  • 31 Pauls SD, Rodway LA, Winter T, Taylor CG, Zahradka P, Aukema HM. Anti-inflammatory effects of α-linolenic acid in M1-like macrophages are associated with enhanced production of oxylipins from α-linolenic and linoleic acid. J Nutr Biochem 2018; 57: 121-129
    CrossrefPubMedSuche in Google Scholar
  • 32 Prasath KG, Alexpandi R, Parasuraman R, Pavithra M, Ravi AV, Pandian SK. Anti-inflammatory potential of myristic acid and palmitic acid synergism against systemic candidiasis in Danio rerio (Zebrafish). Biomed Pharmacother 2021; 133: 111043
    CrossrefPubMedSuche in Google Scholar
  • 33 Shen Z, Ma Y, Ji Z, Hao Y, Yan X, Zhong Y. Tan X, Ren W. Arachidonic acid induces macrophage cell cycle arrest through the JNK signaling pathway. Lipids Health Dis 2018; 17: 26, 1–9
    CrossrefPubMedSuche in Google Scholar
  • 34 Diakogiannaki E, Dhayal S, Childs CE, Calder PC, Welters HJ, Morgan NG. Mechanisms involved in the cytotoxic and cytoprotective actions of saturated versus monounsaturated long-chain fatty acids in pancreatic β-cells. J Endocrinol 2007; 194: 283-291
    CrossrefPubMedSuche in Google Scholar
  • 35 Wang X, Cui YJ, Qi J, Zhu MM, Zhang TL, Cheng M. Liu SM, Wang GC. Fucoxanthin Exerts Cytoprotective Effects against Hydrogen Peroxide-Induced Oxidative Damage in L02 Cells. Biomed Res Int 2018; 2018: 1085073
    CrossrefPubMedSuche in Google Scholar
  • 36 Chen SJ, Lin TB, Peng HY, Liu HJ, Lee AS, Lin CH. Tseng KW. Cytoprotective potential of fucoxanthin in oxidative stress-induced age-related macular degeneration and retinal pigment epithelial cell senescence in vivo and in vitro. Mar Drugs 2021; 19: 114, 1–15
    PubMedSuche in Google Scholar