Journal of Veterinary Clinics (한국임상수의학회지)

The Korean Society of Veterinary Clinics (한국임상수의학회)
권호 표지
DOI QR코드

DOI QR Code

Fucoidan Upregulates Chemotactic Activity of Porcine Peripheral Blood Polymorphonuclear Cells to Interleukin-8 by PI3K Activation

  • Kang, Song-Ai (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Ahn, Changhwan (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Kang, Byeong-Teck (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Kang, Ji-Houn (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Jeung, Eui-Bae (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University) ;
  • Yang, Mhan-Pyo (Department of Veterinary Medicine, Veterinary Medical Center and College of Veterinary Medicine, Chungbuk National University)
  • Received : 2017.01.31
  • Accepted : 2017.02.16
  • Published : 2017.04.28
Download PDF
⟨ Previous Next ⟩

Abstract

Fucoidan increases the chemotactic activity of peripheral blood polymorphonuclear cells (PMNs) through interleukin (IL)-8 produced by peripheral blood mononuclear cells (PBMCs). It has been demonstrated that fucoidan can regulate the chemotaxis of PMNs by activating F-actin polymerization. The objectives of this study are to investigate the direct effect of fucoidan on the chemotaxis of porcine PMNs and to examine whether this effect is associated with changes in phosphoinositide 3-kinase (PI3K) activity. The chemotactic activity of porcine PMNs was evaluated by modified Boyden chamber assay. Akt phosphorylation activity, a main downstream of PI3K, was measured by Western blotting assay. Fucoidan itself has no chemoattractant effect for PMNs. However, direct treatment of PMNs with fucoidan showed higher chemotactic activity to porcine recombinant (pr) IL-8 than that of PMNs without fucoidan. The increased chemotactic activity of fucoidan-treated PMNs to pr IL-8 was suppressed by treatment of wortmannin, an inhibitor of PI3K. Treatment of PMNs with fucoidan also increased Akt phosphorylation level. This increase was also suppressed by wortmannin. These results suggested that fucoidan can upregulate chemotactic activity of porcine PMNs to IL-8, which is associated with PI3K activation.

Keywords

References

  1. Ali H, Haribabu B, Richardson RM, Snyderman R. Mechanisms of inflammation and leukocyte activation. Med Clin North Am 1997; 81: 1-28. https://doi.org/10.1016/S0025-7125(05)70503-4
  2. Arraes SM, Freitas MS, da Silva SV, de Paula Neto HA, Alves-Filho JC, Auxiliadora Martins M, Basile-Filho A, Tavares-Murta BM, Barja-Fidalgo C, Cunha FQ. Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood 2006; 108: 2906-2913. https://doi.org/10.1182/blood-2006-05-024638
  3. Backstrom L, Hoefling DC, Morkoc AC, Cowart RP. Effect of atrophic rhinitis on growth rate in Illinois swine herds. J Am Vet Med Assoc 1985; 187: 712-715.
  4. Blazquez S, Guigon G, Weber C, Syan S, Sismeiro O, Coppee JY, Labruyere E, Guillen N. Chemotaxis of Entamoeba histolytica towards the pro-inflammatory cytokine TNF is based on PI3K signalling, cytoskeleton reorganization and the galactose/N-acetylgalactosamine lectin activity. Cell Microbiol 2008; 10: 1676-1686. https://doi.org/10.1111/j.1462-5822.2008.01158.x
  5. Bourne HR, Weiner O. A chemical compass. Nature 2002;419: 21. https://doi.org/10.1038/419021a
  6. Cho TM, Kim WJ, Moon SK. Akt signaling is involved in fucoidan-induced inhibition of growth and migration of human bladder cancer cells. Food Chem Toxicol 2014; 64: 344-352. https://doi.org/10.1016/j.fct.2013.12.009
  7. Chodniewicz D, Zhelev DV. Chemoattractant receptorstimulated F-actin polymerization in the human neutrophil is signaled by 2 distinct pathways. Blood 2003; 101: 1181-1184. https://doi.org/10.1182/blood-2002-05-1435
  8. Chung CY, Funamoto S, Firtel RA. Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem Sci 2001; 26: 557-566. https://doi.org/10.1016/S0968-0004(01)01934-X
  9. Dharmawardhane S, Brownson D, Lennartz M, Bokoch GM. Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J Leukoc Biol 1999; 66: 521-527. https://doi.org/10.1002/jlb.66.3.521
  10. Ferguson GJ, Milne L, Kulkarni S, Sasaki T, Walker S, Andrews S, Crabbe T, Finan P, Jones G, Jackson S, Camps M, Rommel C, Wymann M, Hirsch E, Hawkins P, Stephens L. PI (3) $K{\gamma}$ has an important context-dependent role in neutrophil chemokinesis. Nat Cell Biol 2007; 9: 86-91. https://doi.org/10.1038/ncb1517
  11. Fry MJ. Phosphoinositide 3-kinase signalling in breast cancer: how big a role might it play?. Breast Cancer Res 2001; 3:304-312. https://doi.org/10.1186/bcr312
  12. Hayashi K, Nakano T, Hashimoto M, Kanekiyo K, Hayashi T. Defensive effects of a fucoidan from brown alga Undaria pinnatifida against herpes simplex virus infection. Int Immunopharmacol 2008; 8: 109-116. https://doi.org/10.1016/j.intimp.2007.10.017
  13. Hirsch E, Katanaev VL, Garlanda C, Azzolino O, Pirola L, Silengo L, Sozzani S, Mantovani A, Altruda F, Wymann MP. Central role for G protein-coupled phosphoinositide 3-kinase gamma in inflammation. Science 2000; 287: 1049-1053. https://doi.org/10.1126/science.287.5455.1049
  14. Jeon CJ, Kim SH, Kim SS, Kang JH, Yang MP. Fucoidan upregulates chemotactic activity of canine peripheral blood polymorphonuclear cells through interleukin-8 from peripheral blood mononuclear cells in vitro. J Vet Clin 2012; 29: 207-212.
  15. Katso R, Okkenhaug K, Ahmadi K, White S, Timms J, Waterfield MD. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu Rev Cell Dev Biol 2001; 17: 615-675. https://doi.org/10.1146/annurev.cellbio.17.1.615
  16. Kawashima T, Murakami K, Nishimura I, Nakano T, Obata A. A sulfated polysaccharide, fucoidan, enhances the immunomodulatory effects of lactic acid bacteria. Int J Mol Med 2012; 29: 447-453.
  17. Kim H, Lee A, Jung WK, Jeon TJ. Effects of fucoidan on cell morphology and migration in osteoblasts. Food Sci Biotechnol 2015; 24: 699-704. https://doi.org/10.1007/s10068-015-0091-2
  18. Kim SH, Kang JH, Yang MP. Fucoidan directly regulates the chemotaxis of canine peripheral blood polymorphonuclear cells by activating F-actin polymerization. Vet Immunol Immunopathol 2013; 151: 124-131. https://doi.org/10.1016/j.vetimm.2012.11.001
  19. Kim SH, Kang JH, Yang MP. Fucoidan increases phagocytic capacity and oxidative burst activity of canine peripheral blood polymorphonuclear cells through TNF-${\alpha}$ from peripheral blood mononulear cells. J Vet Clin 2011; 28: 183-189.
  20. Kolsch V, Seher T, Fernandez-Ballester G. J, Serrano L, Leptin M. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 2007; 315: 384-386. https://doi.org/10.1126/science.1134833
  21. Lee H, Kim JS, Kim E. Fucoidan from seaweed Fucus vesiculosus inhibits migration and invasion of human lung cancer cell via PI3K-Akt-mTOR pathways. PLoS One 2012; 7: e50624. https://doi.org/10.1371/journal.pone.0050624
  22. Li W, Liu G, Chou IN, Kagan HM. Hydrogen peroxidemediated, lysyl oxidase-dependent chemotaxis of vascular smooth muscle cells. J Cell Biochem 2000; 78: 550-557. https://doi.org/10.1002/1097-4644(20000915)78:4<550::AID-JCB4>3.0.CO;2-8
  23. 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. https://doi.org/10.1055/s-2006-951703
  24. Matsubara K, Matsuura Y, Bacic A, Liao M, Hori K, Miyazawa K. Anticoagulant properties of a sulfated galactan preparation from a marine green alga, Codium cylindricum. Int J Biol Macromol 2001; 28: 395-399. https://doi.org/10.1016/S0141-8130(01)00137-4
  25. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006; 6: 173-182. https://doi.org/10.1038/nri1785
  26. Oudit GY, Penninger JM. Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc Res 2009; 82: 250-260
  27. Pereira MA, Sannomiya P, Leme JG. Inhibition of leukocyte chemotaxis by factor in alloxan-induced diabetic rat plasma. Diabetes 1987; 36: 1307-1314. https://doi.org/10.2337/diab.36.11.1307
  28. Postma M, Bosgraaf L, Loovers HM, Van Haastert PJ. Chemotaxis: signalling modules join hands at front and tail. EMBO Rep 2004; 5: 35-40. https://doi.org/10.1038/sj.embor.7400051
  29. Rameh LE, Cantley LC. The role of phosphoinositide 3-kinase lipid products in cell function. J Biol Chem 1999; 274: 8347-8350. https://doi.org/10.1074/jbc.274.13.8347
  30. Sadhu C, Masinovsky B, Dick K, Sowell CG, Staunton DE. Essential role of phosphoinositide 3-kinase delta in neutrophil directional movement. J Immunol 2003; 170: 2647-2654. https://doi.org/10.4049/jimmunol.170.5.2647
  31. Sasaki T, Irie-Sasaki J, Jones RG, Oliveira-dos-Santos AJ, Stanford WL, Bolon B, Wakeham A, Itie A, Bouchard D, Kozieradzki I, Joza N, Mak TW, Ohashi PS, Suzuki A, Penninger JM. Function of PI3Kgamma in thymocyte development, T cell activation, and neutrophil migration. Science 2000; 287: 1040-1046. https://doi.org/10.1126/science.287.5455.1040
  32. Son SM, Kang JH, Lee GS, Jeung EB, Yang MP. Induction of interleukin-8 expression in porcine peripheral blood mononuclear cells by trans10-cis12 conjugated linoleic acid. Vet Immunol Immunopathol 2006; 112: 284-289. https://doi.org/10.1016/j.vetimm.2006.02.005
  33. Stephens L, Ellson C, Hawkins P. Roles of PI3Ks in leukocyte chemotaxis and phagocytosis. Curr Opin Cell Biol 2002; 14: 203-213. https://doi.org/10.1016/S0955-0674(02)00311-3
  34. Vanhaesebroeck B, Jones GE, Allen WE, Zicha D, Hooshmand-Rad R, Sawyer C, Wells C, Waterfield MD, Ridley AJ. Distinct PI(3)Ks mediate mitogenic signalling and cell migration in macrophages. Nat Cell Biol 1999; 1: 69-71. https://doi.org/10.1038/9045
  35. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001; 70: 535-602. https://doi.org/10.1146/annurev.biochem.70.1.535
  36. Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, Bourne HR. A PtdInsP(3)- and Rho GTPasemediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 2002; 4: 509-513. https://doi.org/10.1038/ncb811
  37. Westphal M, Jungbluth A, Heidecker M, Muhlbauer B, Heizer C, Schwartz JM, Marriott G, Gerisch G. Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 1997; 7: 176-183. https://doi.org/10.1016/S0960-9822(97)70088-5
  38. Xu J, Wang F, Van Keymeulen A, Herzmark P, Straight A, Kelly K, Takuwa Y, Sugimoto N, Mitchison T, Bourne HR. Divergent signals and cytoskeletal assemblies regulate selforganizing polarity in neutrophils. Cell 2003; 114: 201-214. https://doi.org/10.1016/S0092-8674(03)00555-5