DOI QR코드

DOI QR Code

Structural Effects of Sulfated-Glycoproteins from Stichopus japonicus on the Nitric Oxide Secretion Ability of RAW 264.7 Cells

  • Cao, Rong-An (College of Food Science, Heilongjiang Bayi Agricultural University) ;
  • Lee, Su-Han (Department of Food Technology and Service, Eulji University) ;
  • You, SangGuan (Department of Marine Food Science and Technology, Gangneung-Wonju National University)
  • Received : 2014.11.11
  • Accepted : 2014.11.24
  • Published : 2014.12.31

Abstract

The effect of various levels of proteins, sulfates, and molecular weight ($M_w$) of a sulfated-glycoprotein ($NF_3$) from a sea cucumber, Stichopus japonicus, on nitric oxide (NO) releasing capacity from RAW 264.7 cells was investigated. The $NF_3$ derivatives had various amounts of proteins (4.8~11.2%) and sulfates (6.8~25.2%) as well as different $M_w$ ($640.3{\times}10^3{\sim}109.2{\times}10^3g/mol$). $NF_3$ was able to stimulate RAW 264.7 cells to release NO with lower protein contents, indicating that the protein moiety was not an important factor to stimulate macrophages. On the other hand, the NO inducing capacity was significantly reduced with decreased levels of sulfates and $M_w$, implying that sulfates and $M_w$ played a pivotal role in activating RAW 264.7 cells. It was not clear why sulfates and a certain range of $M_w$ were essential for stimulating macrophages. It appeared that certain levels of sulfates and $M_w$ of sulfated-glycoproteins were required to bind to the surface receptors on RAW 264.7 cells.

Keywords

References

  1. Pomin VH, Pereira MS, Valente AP, Tollefsen DM, Pavao MS, Mourao 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. https://doi.org/10.1093/glycob/cwi021
  2. Mao WJ, Fang F, Li HY, Qi XH, Sun HH, Chen Y, Guo SD. 2008. Heparinoid-active two sulfated polysaccharides isolated from marine green algae Monostroma nitidum. Carbohydr Polym 74: 834-839. https://doi.org/10.1016/j.carbpol.2008.04.041
  3. Riou D, Colliec-Jouault S, Pinczon du Sel D, Bosch S, Siavoshian S, Le Bert V, Tomasoni C, Sinquin C, Durand P, Roussakis C. 1996. Antitumor and antiproliferative effects of a fucan extracted from Ascophyllum nodosum against a non-small-cell bronchopulmonary carcinoma line. Anticancer Res 16: 1213-1218.
  4. Yoo YC, Kim WJ, Kim SY, Kim SM, Chung MK, Park JW, Suh HH, Lee KB, Park YI. 2007. Immunomodulating activity of a fucoidan isolated from Korean Undaria pinnatifida sporophyll. Alage 22: 333-338. https://doi.org/10.4490/ALGAE.2007.22.4.333
  5. Soeda S, Kozako T, Iwata K, Shimeno H. 2000. Oversulfated fucoidan inhibits the basic fibroblast growth factor-induced tube formation by human umbilical vein endothelial cells: its possible mechanism of action. Biochim Biophys Acta 1497: 127-134. https://doi.org/10.1016/S0167-4889(00)00052-5
  6. Jiang Z, Ueno M, Nishiguchi T, Abu R, Isaka S, Okimura T, Yamaguchi K, Oda T. 2013. Importance of sulfate groups for the macrophage-stimulating activities of ascophyllan isolated from the brown alga Ascophyllum nodosum. Carbohydr Res 380: 124-129. https://doi.org/10.1016/j.carres.2013.05.018
  7. Kawashima T, Murakami K, Nishimura I, Nakano T, Obata A. 2012. A sulfated polysaccharide, fucoidan, enhances the immunomodulatory effects of lactic acid bacteria. Int J Mol Med 29: 447-453.
  8. Haroun-Bouhedja F, Ellouali M, Sinquin C, Boisson-Vidal C. 2000. Relationship between sulfate groups and biological activities of fucans. Thromb Res 100: 453-459. https://doi.org/10.1016/S0049-3848(00)00338-8
  9. Nishino T, Aizu Y, Nagumo T. 1991. The influence of sulfate content and molecular weight of a fucan sulfate from the brown seaweed Ecklonia kurome on its antithrombin activity. Thromb Res 64: 723-731. https://doi.org/10.1016/0049-3848(91)90072-5
  10. Bordbar S, Anwar F, Saari N. 2011. High-value components and bioactives from sea cucumbers for functional foods-a review. Mar Drugs 9: 1761-1805. https://doi.org/10.3390/md9101761
  11. Yu L, Ge L, Xue C, Chang Y, Zhang C, Xu X, Wang Y. 2014. Structural study of fucoidan from sea cucumber Acaudina molpadioides: a fucoidan containing novel tetrafucose repeating unit. Food Chem 142: 197-200. https://doi.org/10.1016/j.foodchem.2013.06.079
  12. Mourao PA, Pereira MS, Pavao MS, Mulloy B, Tollefsen DM, Mowinckel MC, Abildgaard U. 1996. Structure and anticoagulant activity of a fucosylated chondroitin sulfate from echinoderm sulfated fucose branches on the polysaccharide account for its high anticoagulant action. J Biol Chem 271: 23973-23984. https://doi.org/10.1074/jbc.271.39.23973
  13. Chen S, Xue C, Yin LA, Tang Q, Yu G, Chai W. 2011. Comparison of structures and anticoagulant activities of fucosylated chondroitin sulfates from different sea cucumbers. Carbohydr Polym 83: 688-696. https://doi.org/10.1016/j.carbpol.2010.08.040
  14. Guerard F, Decourcelle N, Sabourin C, Floch-Laizet C, Le Grel L, Le Floc'H PL, Gourlay F, Le Delezir RL, Jaouen P, Bourseau P. 2010. Recent developments of marine ingredients for food and nutraceutical applications: a review. J Sci Hal Aquat 2: 21-27.
  15. Liu X, Sun Z, Zhang M, Meng X, Xia X, Yuan W, Xue F, Liu C. 2012. Antioxidant and antihyperlipidemic activities of polysaccharides from sea cucumber Apostichopus japonicus. Carbohydr Polym 90: 1664-1670. https://doi.org/10.1016/j.carbpol.2012.07.047
  16. Jin JO, Shastina VV, Shin SW, Xu Q, Park JI, Rasskazov VA, Avilov SA, Fedorov SN, Stonik VA, Kwak JY. 2009. Differential effects of triterpene glycosides, frondoside A and cucumarioside $A_2$-2 isolated from sea cucumbers on caspase activation and apoptosis of human leukemia cells. FEBS Lett 583: 697-702. https://doi.org/10.1016/j.febslet.2009.01.010
  17. Zhang Y, Song S, Song D, Liang H, Wang W, Ji A. 2010. Proliferative effects on neural stem/progenitor cells of a sulfated polysaccharide purified from the sea cucumber Stichopus japonicus. J Biosci Bioeng 109: 67-72. https://doi.org/10.1016/j.jbiosc.2009.07.010
  18. Kariya Y, Mulloy B, Imai K, Tominaga A, Kaneko T, Asari A, Suzuki K, Masuda H, Kyogashima M, Ishii T. 2004. Isolation and partial characterization of fucan sulfates from the body wall of sea cucumber Stichopus japonicus and their ability to inhibit osteoclastogenesis. Carbohydr Res 339: 1339-1346. https://doi.org/10.1016/j.carres.2004.02.025
  19. Chen S, Hu Y, Ye X, Li G, Yu G, Xue C, Chai W. 2012. Sequence determination and anticoagulant and antithrombotic activities of a novel sulfated fucan isolated from the sea cucumber Isostichopus badionotus. Biochim Biophys Acta 1820: 989-1000. https://doi.org/10.1016/j.bbagen.2012.03.002
  20. Sevag MG, Lackman DB, Smolens J. 1938. The isolation of the components of streptococcal nucleoproteins in serologically active form. J Biol Chem 124: 425-436.
  21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin-Phenol reagents. J Biol Chem 193: 265-275.
  22. Dodgson KS, Price RG. 1962. A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84: 106-110. https://doi.org/10.1042/bj0840106
  23. Bao HH, You SG. 2011. Molecular characteristics of watersoluble extracts from Hypsizigus marmoreus and their in vitro growth inhibition of various cancer cell lines and immunomodulatory function in RAW 264.7 cells. Biosci Biotechnol Biochem 75: 891-898. https://doi.org/10.1271/bbb.100825
  24. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. 1982. Analysis of nitrate, nitrite, and [$^{15}N$]nitrate in biological fluids. Anal Biochem 126: 131-136. https://doi.org/10.1016/0003-2697(82)90118-X
  25. Wada Y, Gu J, Okamoto N, Inui K. 1994. Diagnosis of carbohydrate-deficient glycoprotein syndrome by matrix-assisted laser desorption time-of-flight mass spectrometry. Biol Mass Spectrom 23: 108-109. https://doi.org/10.1002/bms.1200230211
  26. Jiao L, Li X, Li T, Jiang P, Zhang L, Wu M, Zhang L. 2009. Characterization and anti-tumor activity of alkali-extracted polysaccharide from Enteromorpha intestinalis. Int Immunopharmacol 9: 324-329. https://doi.org/10.1016/j.intimp.2008.12.010
  27. Chen Z, Soo MY, Srinivasan N, Tan BK, Chan SH. 2009. Activation of macrophages by polysaccharide-protein complex from Lycium barbarum L. Phytother Res 23: 1116-1122. https://doi.org/10.1002/ptr.2757
  28. Ji CF, Ji YB, Meng DY. 2013. Sulfated modification and anti-tumor activity of laminarin. Exp Ther Med 6: 1259-1264. https://doi.org/10.3892/etm.2013.1277
  29. Adhikari U, Mateu CG, Chattopadhyay K, Pujol CA, Damonte EB, Ray B. 2006. Structure and antiviral activity of sulfated fucans from Stoechospermum marginatum. Phytochemistry 67: 2474-2482. https://doi.org/10.1016/j.phytochem.2006.05.024
  30. Witvrouw M, De Clercq E. 1997. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen Pharmac 29: 497-511. https://doi.org/10.1016/S0306-3623(96)00563-0
  31. Pereira MS, Mulloy B, Mourao 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: 7656-7667. https://doi.org/10.1074/jbc.274.12.7656
  32. Yang C, Chung DH, Shin IS, Lee HY, Kim JC, Lee YJ, You SG. 2008. Effects of molecular weight and hydrolysis conditions on anticancer activity of fucoidans from sporophyll of Undaria pinnatifida. Int J Biol Macromol 43: 433-437. https://doi.org/10.1016/j.ijbiomac.2008.08.006

Cited by

  1. Effects of the molecular weight and protein and sulfate content of Chlorella ellipsoidea polysaccharides on their immunomodulatory activity 2018, https://doi.org/10.1016/j.ijbiomac.2017.08.144
  2. Immuno-enhancement effect of polysaccharide extracted from Stichopus japonicus on cyclophosphamide-induced immunosuppression mice vol.27, pp.2, 2014, https://doi.org/10.1007/s10068-017-0248-2
  3. Different Macrophage Type Triggering as Target of the Action of Biologically Active Substances from Marine Invertebrates vol.18, pp.1, 2020, https://doi.org/10.3390/md18010037