Aquaculture International

, Volume 25, Issue 5, pp 1813–1819 | Cite as

Fucus vesiculosus extract inhibits the proteolytic activity and gene expression of matrix metalloproteinases in Atlantic salmon (Salmo salar L.)

  • Jonhard Eysturskarð
  • Sunnvør í Kongsstovu
  • Daisy Færø
  • Ása Jacobsen
  • Hóraldur Joensen


Fucoidans are sulfated fucose-rich polysaccharides found in macroalgae. Multiple biological functions have been attributed to fucoidans including inhibitory activity against matrix metalloproteinases (MMPs). A recent study showed that kidney and blood remains left in the abdominal cavity after gutting had a significant negative effect on gaping and fillet firmness in Atlantic salmon (Salmo salar L.). The authors hypothesized that one reason could be that MMPs from kidney and blood remains break down the connective tissue in Atlantic salmon fillets. The objectives of this study were to investigate the presence of MMPs in Atlantic salmon kidney and the inhibitory effect of a Fucus vesiculosus extract (FVE) on the proteolytic activity and gene expression of MMPs in Atlantic salmon. The inhibitory effect of FVE was compared to the inhibitory effect of the synthetic broad-spectrum MMP inhibitor marimastat. In this study, we found that FVE inhibits the proteolytic activity of MMP-1, MMP-2, MMP-9, and MMP-13 in Atlantic salmon kidney as well as MMP-2 gene expression in Atlantic salmon liver. Although the inhibitory effect of FVE on the proteolytic activity of MMPs is small compared to the inhibitory effect of marimastat, both FVE and marimastat inhibit 80% of the DQ-gelatin breakdown caused by Atlantic salmon kidney at a concentration of 0.1 mg mL−1. This indicates that FVE may also be capable of inhibiting other proteinases present in Atlantic salmon kidney. Overall, our findings suggest that FVE could be used in the fish processing industry to limit collagenase and gelatinase activity, thus reducing the connective tissue degradation in Atlantic salmon fillets.


Atlantic salmon (Salmo salar L.Fucus vesiculosus extract (FVE) Kidney Matrix metalloproteinases (MMPs) 



Extracellular matrix


Elongation factor 1-alpha


Fucus vesiculosus extract


Matrix metalloproteinases


Polymerase chain reaction


Relative fluorescence unit


Ribonucleic acid


Reverse transcriptase quantitative PCR


  1. Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for fucoidan bioactivity: a critical review of structure-function relations and extraction methods for fucose-containing sulfated polysaccharides from brown seaweeds. Marine Drugs 9:2106–2130CrossRefPubMedPubMedCentralGoogle Scholar
  2. Delbarre-Ladrat C, Chéret R, Taylor R, Verrez-Bagnis V (2006) Trends in postmortem aging in fish: understanding of proteolysis and disorganization of the myofibrillar structure. Crit Rev Food Sci Nutr 46:409–421CrossRefPubMedGoogle Scholar
  3. Fitton HJ, Dell’Acqua G, Gardiner VA, Karpiniec SS, Stringer DN, Davis E (2015a) Topical benefits of two fucoidan-rich extracts from marine macroalgae. Cosmetics 2:66–81CrossRefGoogle Scholar
  4. Fitton JH, Stringer DN, Karpiniec SS (2015b) Therapies from fucoidan: an update. Marine Drugs 13:5920–5946CrossRefPubMedPubMedCentralGoogle Scholar
  5. Gupta SP (2012) Matrix metalloproteinase inhibitors–specificity of binding and structure-activity relationships, vol 103. Springer Science & Business Media, DordrechGoogle Scholar
  6. Hlawaty H, Suffee N, Sutton A, Oudar O, Haddad O, Ollivier V, Laguillier-Morizot C, Gattegno L, Letourneur D, Charnaux N (2011) Low molecular weight fucoidan prevents intimal hyperplasia in rat injured thoracic aorta through the modulation of matrix metalloproteinase-2 expression. Biochem Pharmacol 81(2):233–243CrossRefPubMedGoogle Scholar
  7. Huang TH, Chiu YH, Chan YL, Chiu YH, Wang H, Huang KC, Li TL, Hsu KH, Wu CJ (2015) Prophylactic administration of fucoidan represses cancer metastasis by inhibiting vascular endothelial growth factor (VEGF) and matrix metalloproteinases (MMPs) in Lewis tumor-bearing mice. Marine Drugs 13:1882–1900CrossRefPubMedPubMedCentralGoogle Scholar
  8. Jacobsen Á, Joensen H, Eysturskarð J (2015) Gaping and loss of fillet firmness in farmed salmon (Salmo salar L.) closely correlated with post-slaughter cleaning of the abdominal cavity. Aquac Res 48(1):321–331CrossRefGoogle Scholar
  9. Kubota M, Kinoshita M, Kubota S, Yamashita M, Toyohara H, Sakaguchi M (2001) Possible implication of metalloproteinases in post-mortem tenderization of fish muscle. Fish Sci 67:965–968CrossRefGoogle Scholar
  10. Kubota M, Kinoshita M, Takeuchi K, Kubota S, Toyohara S, Sakaguchi M (2003) Solubilization of type I collagen from fish muscle connective tissue by matrix metalloproteinase-9 at chilled temperature. Fish Sci 69:1053–1059CrossRefGoogle Scholar
  11. Kwak JY (2014) Fucoidan as a marine anticancer agent in preclinical development. Marine Drugs 12:851–870CrossRefPubMedPubMedCentralGoogle Scholar
  12. Lafleur MA, Hollenberg MD, Atkinson SJ, Knauper V, Murphy G, Edwards DR (2001) Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membrane-type-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63 kDa active species. Biochem J 357:107–115CrossRefPubMedPubMedCentralGoogle Scholar
  13. Lee H, Kim JS, Kim E (2012) Fucoidan from seaweed Fucus vesiculosus inhibits migration and invasion of human lung cancer cell via PI3K-Akt-mTOR pathways. PLoS One 7(11):e50624CrossRefPubMedPubMedCentralGoogle Scholar
  14. Manello F (2008) Serum or plasma samples? The “Cinderella” role of blood collection procedures. Preanalytical methodological issues influence the release and activity of circulating matrix metalloproteinases and their tissue inhibitors, hampering diagnostic trueness and leading to misinterpretation. Arterioscler Thromb Vasc Biol 28:611–614CrossRefGoogle Scholar
  15. Min SK, Kwon OC, Lee S, Park KH, Kim JK (2012) An antithrombotic fucoidan, unlike heparin, does not prolong bleeding time in a murine arterial thrombosis model: a comparative study of Undaria pinnatifida sporophylls and Fucus vesiculosus. Phytother Res 26(5):752–757CrossRefPubMedGoogle Scholar
  16. Pedersen ME, Vuong TT, Rønning SB, Kolset SO (2015) Matrix metalloproteinases in fish biology and matrix turnover. Matrix Biol 44:86–93CrossRefPubMedGoogle Scholar
  17. Pereira MS, Mulloy B, Mourão PA (1999) Structure and anticoagulant activity of sulfated fucans comparison between the regular, repetitive, and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. J Biol Chem 274(12):7656–7667CrossRefPubMedGoogle Scholar
  18. Pomin VH (2012a) Fucanomics and galactanomics: current status in drug discovery, mechanisms of action and role of the well-defined structures. Biochim Biophys Acta 1820:1971–1979CrossRefPubMedGoogle Scholar
  19. Pomin VH (2012b) Fucanomics and galactanomics: marine distribution, medicinal impact, conception and challenges. Marine Drugs 10:793–811CrossRefPubMedPubMedCentralGoogle Scholar
  20. Puthiyachirakkal M, Lemerand K, Kumar D, Moore R, Philipson E, Mercer BM, Mansour JM, Hauguel-de Mouzon S, Moore JJ (2013) Thrombin weakens the amnion extracellular matrix (ECM) directly rather than through protease activated receptors. Placenta 34(10):924–931CrossRefPubMedGoogle Scholar
  21. Tang R, Dodd A, Lai D, McNabb WC, Love DR (2007) Validation of zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization. Acta Biochim Biophys Sin 39(5):384–390CrossRefPubMedGoogle Scholar
  22. Ustyuzhanina NE, Ushakova NA, Zyuzina KA, Bilan MI, Elizarova AL, Somonova OV, Madzhuga AV, Krylov VB, Preobrazhenskaya ME, Usov AI, Kiselevskiy MV (2013) Influence of fucoidans on hemostatic system. Marine drugs 11(7):2444–2458CrossRefPubMedPubMedCentralGoogle Scholar
  23. Vuong TT, Rønning SB, Kolset SO, Pedersen ME (2016) The enzyme profiles in the connective tissue attaching pin bones to the surrounding tissue is specific in farmed salmon (Salmo salar) and cod (Gadus morhua L.). Fish Physiol Biochem 1–7Google Scholar
  24. Xu C, Wang C, Cai QF, Zhang Q, Weng L, Liu GM, Su WJ, Cao MJ (2015) Matrix metalloproteinase 2 (MMP-2) plays a critical role in the softening of common carp muscle during chilled storage by degradation of type I and V collagens. J Agric Food Chem 63:10948–10956CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Aquaculture Research Station of the FaroesHvalvíkFaroe Islands
  2. 2.Department of Science and TechnologyUniversity of the Faroe IslandsFO-100 TórshavnFaroe Islands

Personalised recommendations