Suppressive Effect of Dietary Fucoidan on Proinflammatory Immune Response and MMP-1 Expression in UVB-Irradiated Mouse Skin

 

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Abstract

It is well known that ultraviolet B irradiation leads to dermal inflammation. In this study, we found that Mekabu fucoidan suppressed edema, decreased the thickness of the prickle cell layer, and decreased matrix metalloproteinase 1 in the skin of mice irradiated with ultraviolet B. Moreover, we found that the mean level of interferon gamma of Mekabu fucoidan-treated, ultraviolet B-irradiated mice (approximately 2.2 ng/mL) was not significantly different from that in normal mice (approximately 2.5 ng/mL). In contrast, a significant decrease in the mean level of interferon gamma (approximately 1.3 ng/mL) in ultraviolet B-irradiated control mice was observed compared with that in Mekabu fucoidan-treated, ultraviolet B-irradiated mice. The mean thickness of the prickle cell layer in the skin of Mekabu fucoidan-treated, ultraviolet B-irradiated mice was less than that in the ultraviolet B-irradiated control mice. Metalloproteinase 1 activity was significantly higher in the skin of ultraviolet B-irradiated mice than in the skin of untreated, nonirradiated normal mice. Metalloproteinase 1 in the skin of ultraviolet B-irradiated, Mekabu fucoidan- or L(+)-ascorbic acid (vitamin C)-treated mice was significantly lower than that in the ultraviolet B-irradiated control mice. Mitigation of the morphological changes in Mekabu fucoidan-treated mice was correlated with a decrease in metalloproteinase 1 levels. These data indicate that Mekabu fucoidan is an effective suppressor of inflammation in an ultraviolet B-irradiated mouse model.

• References

• 1 Maruyama H, Tamauchi H, Hashimoto M, Nakano T. Antitumor activity and immune response of Mekabu fucoidan extracted from sporophyll of Undaria pinnatifida . In Vivo 2003; 17: 245-250
  PubMedGoogle Scholar
• 2 Maruyama H, Tamauchi H, Hashimoto M, Nakano T. Suppression of Th2 immune responses by Mekabu fucoidan from Undaria pinnaifida sporophylls. Int Arch Allergy Immunol 2005; 137: 289-294
  CrossrefPubMedGoogle Scholar
• 3 Maruyama H, Tamauchi H, Iizuka M, Nakano T. The role of NK cells in antitumor activity of dietary fucoidan from Undaria pinnatifida sporophylls (Mekabu). Planta Med 2006; 72: 1415-1417
  Article in Thieme ConnectPubMedGoogle Scholar
• 4 Maruyama H, Suzuki K, Miyai S, Ohtsuki K. Characterization of meFucoidan as a selective inhibitor for secretory phospholipase A₂-IIA and the phosphorylation of meFucoidan-binding proteins by A-kinase in vitro . Biol Pharm Bull 2008; 31: 714-718
  CrossrefPubMedGoogle Scholar
• 5 Choi JI, Raghavendran HR, Sung NY, Kim JH, Chun BS, Ahn DH, Choi HS, Kang KW, Lee JW. Effect of fucoidan on aspirin-induced stomach ulceration in rats. Chem Biol Interact 2010; 183: 249-254
  CrossrefPubMedGoogle Scholar
• 6 Sinha S, Astani A, Ghosh T, Schnitzler P, Ray B. Polysaccharides from Sargassum tenerrimum: structural features, chemical modification and anti-viral activity. Phytochemistry 2010; 71: 235-242
  CrossrefPubMedGoogle Scholar
• 7 Lee JB, Hayashi K, Hashimoto M, Nakano T, Hayashi T. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharm Bull (Tokyo) 2010; 52: 1091-1094
  PubMedGoogle Scholar
• 8 Rana S, Byrne SN, MacDonald LJ, Chan CY, Halliday GM. Ultraviolet B suppresses immunity by inhibiting effector and memory T cells. Am J Pathol 2008; 172: 993-1004
  CrossrefPubMedGoogle Scholar
• 9 Bashir MM, Sharma MR, Werth VP. TNF-alpha production in the skin. Arch Dermatol Res 2009; 301: 87-91
  CrossrefPubMedGoogle Scholar
• 10 Gilmore TD. The Rel/NF-kappaB signal transduction pathway: introduction. Oncogene 1999; 18: 6842-6844
  CrossrefPubMedGoogle Scholar
• 11 Ali F, Sultana S. Repeated short-term stress synergizes the ROS signaling through up regulation of NFkB and iNOS expression induced due to combined exposure of trichloroethylene and UVB rays. Mol Cell Biochem 2012; 360: 133-145
  CrossrefPubMedGoogle Scholar
• 12 Tergaonkar V. NFkappaB pathway: a good signaling paradigm and therapeutic target. Int J Biochem Cell Biol 2006; 38: 1647-1653
  CrossrefPubMedGoogle Scholar
• 13 Shih MF, Cherng JY. Potential protective effect of fresh grown unicellular green algae component (resilient factor) against PMA- and UVB-induced MMP1 expression in skin fibroblasts. Eur J Dermatol 2008; 18: 303-307
  PubMedGoogle Scholar
• 14 Moon HJ, Lee SR, Shin SN, Jeong SH, Stonik VA, Rasskazov VA, Zvyagintseva T, Lee YH. Fucoidan inhibits UVB-Induced MMP-1 expression in human skin fibroblasts. Biol Pharm Bull 2008; 31: 284-289
  CrossrefPubMedGoogle Scholar
• 15 Panich U, Tangsupa-a-nan V, Onkoksoong T, Kongtaphan K, Kasetsinsombat K, Akarasereenont P, Wongkajornsilp A. Inhibition of UVA-mediated melanogenesis by ascorbic acid through modulation of antioxidant defense and nitric oxide system. Arch Pharm Res 2011; 34: 811-820
  CrossrefPubMedGoogle Scholar
• 16 Yoshimura M, Watanabe Y, Kasai K, Yamakoshi J, Koga T. Inhibitory effect of an ellagic acid-rich pomegranate extract on tyrosinase activity and ultraviolet-induced pigmentation. Biosci Biotechnol Biochem 2005; 69: 2368-2373
  CrossrefPubMedGoogle Scholar
• 17 Gensler HL. Reduction of immunosuppression in UV-irradiated mice by dietary retinyl palmitate plus canthaxanthin. Carcinogenesis 1989; 10: 203-207
  CrossrefPubMedGoogle Scholar
• 18 Wilgus TA, Ross MS, Parrett ML, Oberyszyn TM. Topical application of a selective cyclooxygenase inhibitor suppresses UVB mediated cutaneous inflammation. Prostaglandins Other Lipid Mediat 2000; 62: 367-384
  CrossrefPubMedGoogle Scholar
• 19 Paz ML, Ferrari A, Weill FS, Leoni J, Maglio DHG. Time-course evaluation and treatment of skin inflammatory immune response after ultraviolet B irradiation. Cytokine 2008; 44: 70-77
  CrossrefPubMedGoogle Scholar
• 20 Nishimura N, Tohyama C, Satoh M, Nishimura H, Reeve VE. Defective immune response and severe skin damage following UVB irradiation in interleukin-6-deficient mice. Immunology 1999; 97: 77-83
  CrossrefPubMedGoogle Scholar
• 21 Teunissen MB, Sylva-Steenland RM, Bos JD. Effect of low-dose ultraviolet-B radiation on the function of human T lymphocytes in vitro . Clin Exp Immunol 1993; 94: 208-213
  PubMedGoogle Scholar
• 22 Baeuerle PA, Baltimore D. NF-kappa B: ten years after. Cell 1996; 87: 13-20
  CrossrefPubMedGoogle Scholar
• 23 Van Loveren H, Boonstra A, Van Dijk M, Fluitman A, Savelkoul HF, Garssen J. UV exposure alters respiratory allergic responses in mice. Photochem Photobiol 2000; 72: 253-259
  CrossrefPubMedGoogle Scholar
• 24 Wang X, Bi Z, Chu W, Wan Y. IL-1 receptor antagonist attenuates MAP kinase/AP-1 activation and MMP1 expression in UVA-irradiated human fibroblasts induced by culture medium from UVB-irradiated human skin keratinocytes. Int J Mol Med 2005; 16: 1117-1124
  PubMedGoogle Scholar
• 25 Dong KK, Damaghi N, Picart SD, Markova NG, Obayashi K, Okano Y, Masaki H, Grether-Beck S, Krutmann J, Smiles KA, Yarosh DB. UV-induced DNA damage initiates release of MMP-1 in human skin. Exp Dermatol 2008; 17: 1037-1044
  CrossrefPubMedGoogle Scholar
• 26 Brenneisen P, Wenk J, Wlaschek M, Krieg T, Scharffetter-Kochanek K. Activation of p 70 ribosomal protein S6 kinase is an essential step in the DNA damage-dependent signaling pathway responsible for the ultraviolet B-mediated increase in interstitial collagenase (MMP-1) and stromelysin-1 (MMP-3) protein levels in human dermal fibroblasts. J Biol Chem 2000; 275: 4336-4344
  CrossrefPubMedGoogle Scholar
• 27 Yamamoto I, Maruyama H, Takahashi M, Komiyama K. The effect of dietary or intraperitoneally injected seaweed preparations on the growth of sarcoma-180 cells subcutaneously implanted into mice. Cancer Lett 1986; 30: 125-131
  CrossrefPubMedGoogle Scholar
• 28 Kajiya K, Sawane M, Huggenberger R, Detmar M. Activation of the VEGFR-3 pathway by VEGF-C attenuates UVB-induced edema formation and skin inflammation by promoting lymphangiogenesis. J Invest Dermatol 2009; 129: 1292-1298
  CrossrefPubMedGoogle Scholar