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A mechanism of low molecular weight fucoidans degraded by enzymatic and acidic hydrolysis for the prevention of UVB damage

Journal of Applied Phycology volume 29, pages 521–529 (2017)Cite this article

Abstract

Fucoidans have been long used as a food supplement due to their diverse pharmacological effects on human health. Low molecular weight fucoidan (LF) is a common form of fucoidans that has been shown to have enhanced biological activity. In the present study, fucoidans were extracted from the brown alga Sargassum hemiphyllum and enzyme-hydrolyzed into low and high molecular weight fucoidans (HF). The skin protective effects of LF, HF, and other fucoidans derivatives against ultraviolet B (UVB) damage were determined by measuring the expression levels of matrix metalloproteinase genes encoding collagenases (MMP-1, MMP-2, MMP-8, MMP-9, MMP-13), transforming growth factor β receptor II (TGFβRII), and type I procollagen. The results show that LF protects against UVB damage to the skin by inhibiting UVB-induced transcription factor activator protein-1 (AP-1)-stimulated transcription of MMP genes encoding collagenases (MMP-1, MMP-8, and MMP-13) and increasing TGFβRII mRNA levels to prevent the loss of TGFβRII that occurs during UVB-induced collagen degradation. Moreover, this study reveals that the biological properties of fucoidans are highly dependent on the fucose content, sulfate content, and molecular weight.

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References

  • Bergfeld WF (1997) The aging skin. Int J Fertil Womens Med 42:57–66

    CAS  PubMed  Google Scholar 

  • Bitzer M, von Gersdorff G, Liang D, Dominguez-Rosales A, Beg AA, Rojkind M, Bottinger EP (2000) A mechanism of suppression of TGF-β/SMAD signaling by NF-κB/RelA. Genes Dev 14:187–197

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen MC, Hsu WL, Hwang PA, Chou TC (2015) Low molecular weight fucoidan inhibits tumor angiogenesis through downregulation of HIF-1/VEGF signaling under hypoxia. Mar Drugs 13:4436–4451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiang HM, Lin TJ, Chiu CY, Chang CW, Hsu KC, Fan PC, Wen KC (2011) Coffea arabica extract and its constituents prevent photoaging by suppressing MMPs expression and MAP kinase pathway. Food Chem Toxicol 49:309–318

    Article  CAS  PubMed  Google Scholar 

  • Choi JI, Kim HJ (2013) Preparation of low molecular weight fucoidan by gamma-irradiation and its anticancer activity. Carbohydr Polym 97:358–362

    Article  CAS  PubMed  Google Scholar 

  • De Souza MCR, Marques CT, Dore CMG, da Silva FRF, Rocha HAO, Leite EL (2007) Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J Appl Phycol 19:153–160

    Article  Google Scholar 

  • Dodgson KS, Price RG (1963) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110

    Article  Google Scholar 

  • Fisher GJ, Datta S, Wang Z, Li XY, Quan T, Chung JH, Kang S, Voorhees JJ (2000) c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J Clin Invest 106:663–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitton JH (2011) Therapies from fucoidan; multifunctional marine polymers. Mar Drugs 9:1731–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furth JJ (1991) The steady-state levels of type I collagen mRNA are reduced in senescent fibroblasts. J Gerontol 46:B122–B124

    Article  CAS  PubMed  Google Scholar 

  • Ho JN, Lee YH, Park JS, Jun WJ, Kim HK, Hong BS, Shin DH, Cho HY (2005) Protective effects of aucubin isolated from Eucommia ulmoides against UVB-induced oxidative stress in human skin fibroblasts. Biol Pharm Bull 28:1244–1248

    Article  CAS  PubMed  Google Scholar 

  • Hsu H-Y, Lin T-Y, Hwang P-A, Tseng L-M, Chen R-H, Tsao S-M, Hsu J (2013) Fucoidan induces changes in the epithelial to mesenchymal transition and decreases metastasis by enhancing ubiquitin-dependent TGFβ receptor degradation in breast cancer. Carcinogenesis 34:874–884

    Article  CAS  PubMed  Google Scholar 

  • Hwang KA, Yi BR, Choi KC (2011) Molecular mechanisms and in vivo mouse models of skin aging associated with dermal matrix alterations. Lab Anim Res 27:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • Hwang P-A, Hung Y-L, Phan NN, Hieu B-T-N, Chang P-M, Li K-L, Lin Y-C (2016) The in vitro and in vivo effects of the low molecular weight fucoidan on the bone osteogenic differentiation properties. Cytotechnology 68:1349–1359

    Article  PubMed  Google Scholar 

  • Isnard N, Peterszegi G, Robert A, Robert L (2002) Regulation of elastase-type endopeptidase activity, MMP-2 and MMP-9 expression and activation in human dermal fibroblasts by fucose and a fucose-rich polysaccharide. Biomed Pharmacother 56:258–264

    Article  CAS  PubMed  Google Scholar 

  • Kim HH, Shin CM, Park CH, Kim KH, Cho KH, Eun HC, Chung JH (2005) Eicosapentaenoic acid inhibits UV-induced MMP-1 expression in human dermal fibroblasts. J Lipid Res 46:1712–1720

    Article  CAS  PubMed  Google Scholar 

  • Ku MJ, Jung JW, Lee MS, Cho BK, Lee SR, Lee HS, Vischuk OS, Zvyagintseva TN, Ermakova SP, Lee YH (2010) Effect of Fucus evanescens fucoidan on expression of matrix metalloproteinase-1 promoter, mRNA, protein and signal pathway. Life Sci 20:1603–1610

    Article  Google Scholar 

  • Kylin H (1913) Zur Biochemie der Meeresalgen. Hoppe Seylers Z Physiol Chem 83:171–197

    Article  CAS  Google Scholar 

  • Lee IH, Huang RL, Chen CT, Chen HC, Hsu WC, Lu MK (2002) Antrodia camphorata polysaccharides exhibit anti-hepatitis B virus effects. FEMS Microbiol Lett 209:63–67

    Article  CAS  PubMed  Google Scholar 

  • Lee NY, Ermakova SP, Choi HK, Kusaykin MI, Shevchenko NM, Zvyagintseva TN, Choi HS (2008) Fucoidan from Laminaria cichorioides inhibits AP-1 transactivation and cell transformation in the mouse epidermal JB6 cells. Mol Carcinog 47:629–637

    Article  CAS  PubMed  Google Scholar 

  • Luyt CE, Meddahi-Pelle A, Ho-Tin-Noe B, Colliec-Jouault S, Guezennec J, Louedec L, Prats H, Jacob MP, Osborne-Pellegrin M, Letourneur D, Michel JB (2003) Low-molecular-weight fucoidan promotes therapeutic revascularization in a rat model of critical hindlimb ischemia. J Pharmacol Exp Ther 305:24–30

    Article  CAS  PubMed  Google Scholar 

  • Moon HJ, Lee SR, Shim SN, Jeong SH, Stonik VA, Rasskazov VA, Zvyagintseva T, Lee YH (2008) Fucoidan inhibits UVB-induced MMP-1 expression in human skin fibroblasts. Biol Pharm Bull 31:284–289

    Article  CAS  PubMed  Google Scholar 

  • Moon HJ, Lee SH, Ku MJ, Yu BC, Jeon MJ, Jeong SH, Stonik VA, Zvyagintseva TN, Ermakova SP, Lee YH (2009a) Fucoidan inhibits UVB-induced MMP-1 promoter expression and down regulation of type I procollagen synthesis in human skin fibroblasts. Eur J Dermatol 19:129–134

    CAS  PubMed  Google Scholar 

  • Moon HJ, Park KS, Ku MJ, Lee MS, Jeong SH, Imbs TI, Zvyagintseva TN, Ermakova SP, Lee YH (2009b) Effect of Costaria costata fucoidan on expression of matrix metalloproteinase-1 promoter, mRNA, and protein. J Nat Prod 72:1731–1734

    Article  CAS  PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth 65:55–63

    Article  CAS  Google Scholar 

  • Nagasawa K, Inoue Y, Kamata T (1977) Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydr Res 58:47–55

    Article  CAS  PubMed  Google Scholar 

  • Park SB, Chun KR, Kim JK, Suk K, Jung YM, Lee WH (2010) The differential effect of high and low molecular weight fucoidans on the severity of collagen-induced arthritis in mice. Phytother Res 24:1384–1391

    Article  CAS  PubMed  Google Scholar 

  • Pfeifer GP, You YH, Besaratinia A (2005) Mutations induced by ultraviolet light. Mutat Res 571:19–31

    Article  CAS  PubMed  Google Scholar 

  • Philips N, Auler S, Hugo R, Gonzalez S (2011) Beneficial regulation of matrix metalloproteinases for skin health. Enzyme Res 2011:427285. doi:10.4061/2011/427285

    Article  PubMed  PubMed Central  Google Scholar 

  • Pomin VH, Pereira MS, Valente A-P, Tollefsen DM, Pavão MS, Mourão PA (2005) Selective cleavage and anticoagulant activity of a sulfated fucan: stereospecific removal of a 2-sulfate ester from the polysaccharide by mild acid hydrolysis, preparation of oligosaccharides, and heparin cofactor II–dependent anticoagulant activity. Glycobiology 15:369–381

  • Quan T, He T, Kang S, Voorhees JJ, Fisher GJ (2004) Solar ultraviolet irradiation reduces collagen in photoaged human skin by blocking transforming growth factor-β type II receptor/Smad signaling. Am J Pathol 165:741–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robert L, Fodil-Bourahla I, Bizbiz L, Robert AM (2004) Effect of L-fucose and fucose-rich polysaccharides on elastin biosynthesis, in vivo and in vitro. Biomed Pharmacother 58:123–128

    Article  CAS  PubMed  Google Scholar 

  • Senni K, Gueniche F, Foucault-Bertaud A, Igondjo-Tchen S, Fioretti F, Colliec-Jouault S, Durand P, Guezennec J, Godeau G, Letourneur D (2006) Fucoidan a sulfated polysaccharide from brown algae is a potent modulator of connective tissue proteolysis. Arch Biochem Biophys 445:56–64

    Article  CAS  PubMed  Google Scholar 

  • Sudel KM, Venzke K, Mielke H, Breitenbach U, Mundt C, Jaspers S, Koop U, Sauermann K, Knussman-Hartig E, Moll I, Gercken G, Young AR, Stab F, Wenck H, Gallinat S (2005) Novel aspects of intrinsic and extrinsic aging of human skin: beneficial effects of soy extract. Photochem Photobiol 81:581–587

    Article  PubMed  Google Scholar 

  • Sweeney EA, Lortat-Jacob H, Priestley GV, Nakamoto B, Papayannopoulou T (2002) Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood 99:44–51

    Article  CAS  PubMed  Google Scholar 

  • Turchin I, Bernatsky S, Clarke AE, St-Pierre Y, Pineau CA (2009) Cigarette smoking and cutaneous damage in systemic lupus erythematosus. J Rheumatol 36:2691–2693

    Article  PubMed  Google Scholar 

  • Varani J, Dame MK, Rittie L, Fligiel SE, Kang S, Fisher GJ, Voorhees JJ (2006) Decreased collagen production in chronologically aged skin: roles of age-dependent alteration in fibroblast function and defective mechanical stimulation. Am J Pathol 168:1861–1868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vittimberga FJ Jr, McDade TP, Perugini RA, Callery MP (1999) Sodium salicylate inhibits macrophage TNF-alpha production and alters MAPK activation. J Surg Res 84:143–149

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612–616

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Chung D, Shin I-S, Lee H, Kim J, Lee Y, You S (2008) Effects of molecular weight and hydrolysis conditions on anticancer activity of fucoidans from sporophyll of Undaria pinnatifida. Int J Biol Macromolec 43:433–437

  • Zhang Z, Teruya K, Eto H, Shirahata S (2011) Fucoidan extract induces apoptosis in MCF-7 cells via a mechanism involving the ROS-dependent JNK activation and mitochondria-mediated pathways. PLoS One 6(11):e27441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank the National Science Council of the Executive Yuan, Taiwan for the grant funding (NSC 104-2320-B-034-003, NSC 105-2320-B-034-001 to Yen-Chang Lin).

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Authors and Affiliations

  1. Department of Bioscience and Biotechnology, National Taiwan Ocean University, Keelung, Taiwan

    Pai-An Hwang

  2. Cancer Center, Taipei Municipal Wanfang Hospital, Taipei, Taiwan

    Ming-De Yan

  3. Seafood Technology Division, Fisheries Research Institute, Council of Agriculture, Keelung, Taiwan

    Ko-Liang Kuo

  4. Faculty of Applied Sciences, Ton Duc Thang University, Ho Chi Minh City, Vietnam

    Nam Nhut Phan

  5. Graduate Institute of Biotechnology, Chinese Culture University, 55 Hwa-Kang Rd., Yangmin Shan, Taipei, 1114, Taiwan

    Nam Nhut Phan & Yen-Chang Lin

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  1. Pai-An Hwang
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  2. Ming-De Yan
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Correspondence to Yen-Chang Lin.

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Hwang, PA., Yan, MD., Kuo, KL. et al. A mechanism of low molecular weight fucoidans degraded by enzymatic and acidic hydrolysis for the prevention of UVB damage. J Appl Phycol 29, 521–529 (2017). https://doi.org/10.1007/s10811-016-0929-x

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  • DOI: https://doi.org/10.1007/s10811-016-0929-x

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