Ascophyllan purified from Ascophyllum nodosum induces Th1 and Tc1 immune responses by promoting dendritic cell maturation

Marine Drugs

Volumn 12, Issue 7, 2014, Pages 4148-4164

  Zhang, Wei ^a   Du, Jiang Yuan ^a   Jiang, Zedong ^b   Okimura, Takasi ^c   Oda, Tatsuya ^b   Yu, Qing ^d   Jin, Jun O ^a  

^a FUDAN UNIVERSITY   (China)

^b NAGASAKI UNIVERSITY   (Japan)

^c Research and Development Division   (Japan)

^d FORSYTH INSTITUTE   (United States)

Author keywords

Ascophyllan; DC maturation; Dendritic cells; Tc1 cells; Th1 cells

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD86 ANTIGEN; FUCOIDIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; POLYSACCHARIDE; POLYSACCHARIDE SULFATE; TUMOR NECROSIS FACTOR ALPHA; ASCOPHYLLIN; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ASCOPHYLLUM; ASCOPHYLLUM NODOSUM; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HELPER CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN PURIFICATION; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; UPREGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOTOXIC T LYMPHOCYTE; DRUG EFFECTS; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ASCOPHYLLUM; CYTOKINES; DENDRITIC CELLS; INTERLEUKIN-12; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; POLYSACCHARIDES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS;

EID: 84905836869     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12074148     Document Type: Article

References (33)

1. Ramberg, J.E.; Nelson, E.D.; Sinnott, R.A. Immunomodulatory dietary polysaccharides: A systematic review of the literature. Nutr. J. 2010, 9, doi:10.1186/1475-2891-9-54.
2. Leung, M.Y.; Liu, C.; Koon, J.C.; Fung, K.P. Polysaccharide biological response modifiers. Immunol. Lett. 2006, 105, 101-114. (Pubitemid 43816084)
3. Nakayasu, S.; Soegima, R.; Yamaguchi, K.; Oda, T. Biological activities of fucose-containing polysaccharide ascophyllan isolated from the brown alga Ascophyllum nodosum. Biosci. Biotechnol. Biochem. 2009, 73, 961-964.
4. Larsen, B.; Haug, A.; Painter, T. Sulphated polysaccharides in brown algae. 3. The native state of dfucoidan in Ascophyllum nodosum and Fucus vesiculosus. Acta Chem. Scand. 1970, 24, 3339-3352.
5. Jiang, Z.; Okimura, T.; Yamaguchi, K.; Oda, T. The potent activity of sulfated polysaccharide, ascophyllan, isolated from Ascophyllum nodosum to induce nitric oxide and cytokine production from mouse macrophage RAW264.7 cells: Comparison between ascophyllan and fucoidan. Nitric Oxide 2011, 25, 407-415.
6. Nakano, K.; Kim, D.; Jiang, Z.; Ueno, M.; Okimura, T.; Yamaguchi, K.; Oda, T. Immunostimulatory activities of the sulfated polysaccharide ascophyllan from Ascophyllum nodosum in in vivo and in vitro systems. Biosci. Biotechnol. Biochem. 2012, 76, 1573-1576.
7. Banchereau, J.; Steinman, R.M. Dendritic cells and the control of immunity. Nature 1998, 392, 245-252. (Pubitemid 28155090)
8. Fujii, S.; Liu, K.; Smith, C.; Bonito, A.J.; Steinman, R.M. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J. Exp. Med. 2004, 199, 1607-1618. (Pubitemid 38821994)
9. Pooley, J.L.; Heath, W.R.; Shortman, K. Cutting edge: Intravenous soluble antigen is presented to CD4 T cells by CD8-dendritic cells, but cross-presented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 2001, 166, 5327-5330. (Pubitemid 32374150)
10. Schnorrer, P.; Behrens, G.M.; Wilson, N.S.; Pooley, J.L.; Smith, C.M.; El-Sukkari, D.; Davey, G.; Kupresanin, F.; Li, M.; Maraskovsky, E.; et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 2006, 103, 10729-10734.
11. Shortman, K.; Heath, W.R. The CD8+ dendritic cell subset. Immunol. Rev. 2010, 234, 18-31.
12. Villadangos, J.A.; Schnorrer, P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat. Rev. Immunol. 2007, 7, 543-555. (Pubitemid 46987783)
13. Watts, C. The exogenous pathway for antigen presentation on major histocompatibility complex class II and CD1 molecules. Nat. Immunol. 2004, 5, 685-692. (Pubitemid 39023297)
14. Moser, M.; Murphy, K.M. Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 2000, 1, 199-205.
15. Kurts, C.; Kosaka, H.; Carbone, F.R.; Miller, J.F.; Heath, W.R. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J. Exp. Med. 1997, 186, 239-245. (Pubitemid 27328024)
16. Tan, J.K.; O'Neill, H.C. Maturation requirements for dendritic cells in T cell stimulation leading to tolerance versus immunity. J. Leukoc. Biol. 2005, 78, 319-324. (Pubitemid 41061304)
17. Fitton, J.H. Therapies from fucoidan; multifunctional marine polymers. Mar. Drugs 2011, 9, 1731-1760.
18. Kwak, J.Y. Fucoidan as a marine anticancer agent in preclinical development. Mar. Drugs 2014, 12, 851-870.
19. Cumashi, A.; Ushakova, N.A.; Preobrazhenskaya, M.E.; D'Incecco, A.; Piccoli, A.; Totani, L.; Tinari, N.; Morozevich, G.E.; Berman, A.E.; Bilan, M.I.; et al. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 2007, 17, 541-552.
20. Kim, M.H.; Joo, H.G. Immunostimulatory effects of fucoidan on bone marrow-derived dendritic cells. Immunol. Lett. 2008, 115, 138-143.
21. Yang, M.; Ma, C.; Sun, J.; Shao, Q.; Gao, W.; Zhang, Y.; Li, Z.; Xie, Q.; Dong, Z.; Qu, X. Fucoidan stimulation induces a functional maturation of human monocyte-derived dendritic cells. Int. Immunopharmacol. 2008, 8, 1754-1760.
22. Jin, J.O.; Park, H.Y.; Xu, Q.; Park, J.I.; Zvyagintseva, T.; Stonik, V.A.; Kwak, J.Y. Ligand of scavenger receptor class A indirectly induces maturation of human blood dendritic cells via production of tumor necrosis factor-alpha. Blood 2009, 113, 5839-5847.
23. Jiang, Z.; Okimura, T.; Yokose, T.; Yamasaki, Y.; Yamaguchi, K.; Oda, T. Effects of sulfated fucan, ascophyllan, from the brown Alga Ascophyllum nodosum on various cell lines: A comparative study on ascophyllan and fucoidan. J. Biosci. Bioeng. 2010, 110, 113-117.
24. Vremec, D.; Pooley, J.; Hochrein, H.; Wu, L.; Shortman, K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 2000, 164, 2978-2986. (Pubitemid 30148956)
25. Takeda, K.; Akira, S. TLR signaling pathways. Semin. Immunol. 2004, 16, 3-9. (Pubitemid 38147427)
26. Gordon, S. Pattern recognition receptors: Doubling up for the innate immune response. Cell 2002, 111, 927-930. (Pubitemid 36044685)
27. Calzas, C.; Goyette-Desjardins, G.; Lemire, P.; Gagnon, F.; Lachance, C.; van Calsteren, M.R.; Segura, M. Group B Streptococcus and Streptococcus suis capsular polysaccharides induce chemokine production by dendritic cells via Toll-like receptor 2- and MyD88-dependent and -independent pathways. Infect. Immun. 2013, 81, 3106-3118.
28. Lin, C.Y.; Lu, M.C.; Su, J.H.; Chu, C.L.; Shiuan, D.; Weng, C.F.; Sung, P.J.; Huang, K.J. Immunomodulatory effect of marine cembrane-type diterpenoids on dendritic cells. Mar. Drugs 2013, 11, 1336-1350.
29. Wallner, S.; Lutz-Nicoladoni, C.; Tripp, C.H.; Gastl, G.; Baier, G.; Penninger, J.M.; Stoitzner, P.; Wolf, D. The role of the E3 ligase Cbl-B in murine dendritic cells. PLoS One 2013, 8, e65178.
30. Ochi, A.; Nguyen, A.H.; Bedrosian, A.S.; Mushlin, H.M.; Zarbakhsh, S.; Barilla, R.; Zambirinis, C.P.; Fallon, N.C.; Rehman, A.; Pylayeva-Gupta, Y.; et al. MyD88 inhibition amplifies dendritic cell capacity to promote pancreatic carcinogenesis via Th2 cells. J. Exp. Med. 2012, 209, 1671-1687.
31. Macedo, G.C.; Magnani, D.M.; Carvalho, N.B.; Bruna-Romero, O.; Gazzinelli, R.T.; Oliveira, S.C. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 2008, 180, 1080-1087.
32. Sathe, P.; Pooley, J.; Vremec, D.; Mintern, J.; Jin, J.O.; Wu, L.; Kwak, J.Y.; Villadangos, J.A.; Shortman, K. The acquisition of antigen cross-presentation function by newly formed dendritic cells. J. Immunol. 2011, 186, 5184-5192.
33. Vremec, D.; O'Keeffe, M.; Wilson, A.; Ferrero, I.; Koch, U.; Radtke, F.; Scott, B.; Hertzog, P.; Villadangos, J.; Shortman, K. Factors determining the spontaneous activation of splenic dendritic cells in culture. Innate Immun. 2011, 17, 338-352.