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Cytotechnology

, Volume 68, Issue 5, pp 1737–1745 | Cite as

Immunostimulatory activity of snake fruit peel extract on murine macrophage-like J774.1 cells

  • Sri Wijanarti
  • Agus Budiawan Naro Putra
  • Kosuke Nishi
  • Eni Harmayani
  • Takuya SugaharaEmail author
Original Article

Abstract

Snake fruit (Salacca edulis Reinw.) is a tropical fruit produced in Indonesia. Snake fruit peel is normally discarded as waste. In the present study, it was revealed that snake fruit peel has high bioactivities on stimulation of the immune system. Snake fruit peel extract (SFPE) was prepared by extracting snake fruit peel powder in water for 15 h at 4 °C. SFPE enhanced phagocytotic activity of murine macrophage-like J774.1 cells. Production of cytokine such as tumour necrosis factor (TNF)-α and interleukin (IL)-6 was also stimulated by SFPE. The gene expression levels for these cytokines were elevated. Immunoblot analysis revealed that SFPE enhanced not only nuclear factor (NF)-κB but also mitogen-activated protein kinases signalling cascades such as JNK and p38 in macrophage. Overall findings suggested that SFPE has a potential beneficial effect to promote our body health through the stimulation of macrophage.

Keywords

J774.1 cells NF-κB Macrophage MAP kinase Phagocytosis Snake fruit 

References

  1. Aderem A, Ulevitch RJ (2000) Toll-like receptors in the induction of the innate immune response. Nature 406:782–787CrossRefGoogle Scholar
  2. Anand RJ, Kohler JW, Cavallo JA, Li J, Dubowski T, Hackam DJ (2007) Toll-like receptor 4 plays a role in macrophage phagocytosis during peritoneal sepsis. J Pediatr Surg 42:927–933CrossRefGoogle Scholar
  3. Bafna AR, Mishra SH (2006) Immunostimulatory effect of methanol extract of Curculigo orchioides on immunosuppressed mice. J Ethnopharmacol 104:1–4CrossRefGoogle Scholar
  4. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SYC, Gordon S (2002) Dectin-1 is a major β-glucan receptor on macrophages. J Exp Med 196:407–412CrossRefGoogle Scholar
  5. Daifuku M, Nishi K, Okamoto T, Nakano H, Nishimoto S, Sugahara T (2012) Immunostimulatory effects of water extract from bulbus arteriosus in tuna in vitro. J Funct Foods 4:263–270CrossRefGoogle Scholar
  6. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239–252CrossRefGoogle Scholar
  7. Deng GF, Shen C, Xu XR, Kuang RD, Guo YJ, Zeng LS, Gao LL, Lin X, Xie JF, Xia EQ, Li S, Wu S, Chen F, Ling WH, Li HB (2012) Potential of fruit wastes as natural resources of bioactive compounds. Int J Mol Sci 13:8308–8323CrossRefGoogle Scholar
  8. Feuerstein GZ, Liu T, Barone FC (1994) Cytokines, inflammation, and brain injury: role of tumor necrosis factor-α. Cerebrovasc Brain Metab Rev 6:341–360Google Scholar
  9. Gorina R, Font-Nieves M, Márquez-Kisinousky L, Santalucia T, Planas AM (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NF-κB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59:242–255CrossRefGoogle Scholar
  10. Guijarro-Muñoz I, Compte M, Álvarez-Cienfuegos A, Álvarez-Vallina L, Sanz L (2014) Lipopolysaccharide activates Toll-like receptor 4 (TLR4)-mediated NF-κB signaling pathway and proinflammatory response in human pericytes. J Biol Chem 289:2457–2468CrossRefGoogle Scholar
  11. Hayden MS, Ghosh S (2004) Signaling to NF-κB. Genes Dev 18:2195–2224CrossRefGoogle Scholar
  12. Herre J, Marshall ASJ, Caron E, Edwards AD, Williams DL, Schweighoffer E, Tybulewicz V, Reis e Sousa C, Gordon S, Brown GD (2004) Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104:4038–4045CrossRefGoogle Scholar
  13. Hume DA (2006) The mononuclear phagocyte system. Curr Opin Immunol 18:49–53CrossRefGoogle Scholar
  14. Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216CrossRefGoogle Scholar
  15. Katsiari CG, Liossis SNC, Sfikakis PP (2010) The pathophysiologic role of monocytes and macrophages in systemic lupus erythematosus: a reappraisal. Semin Arthritis Rheum 39:491–503CrossRefGoogle Scholar
  16. Kumalasari ID, Nishi K, Harmayani E, Raharjo S, Sugahara T (2013) Effect of bengkoang (Pachyrhizuserosus) fiber extract on murine macrophage-like J774.1 cells and mouse peritoneal macrophages. J Funct Foods 5:582–589CrossRefGoogle Scholar
  17. Kumalasari ID, Nishi K, Putra ABN, Sugahara T (2014) Activation of macrophages stimulated by the bengkoang fiber extract through toll-like receptor 4. Food Funct 5:1403–1408CrossRefGoogle Scholar
  18. Lee JS, Hong EK (2011) Immunostimulating activity of the polysaccharides isolated from Cordycepsmilitaris. Int Immunopharmacol 11:1226–1233CrossRefGoogle Scholar
  19. Leontowicz H, Leontowicz M, Drzewiecki J, Haruenkiy R, Poovarodom S, Park YS, Jung ST, Kang SG, Trakhtenberg S, Gorinstein S (2006) Bioactive properties of snake fruit (Salacca edulis Reinw.) and Mangosteen (Garcinia mangostana) and their influence on plasma lipid profile and antioxidant activity in rats fed cholesterol. Eur Food Res Technol 223:697–703CrossRefGoogle Scholar
  20. Li F, Li S, Li HB, Deng GF, Ling WH, Wu S, Xu XR, Chen F (2013) Antiproliferative activity of peels, pulps and seeds of 61 fruits. J Funct Foods 5:1298–1309CrossRefGoogle Scholar
  21. Logambal SM, Venkatalakshmi S, Michael RD (2000) Immunostimulatory effect of leaf extract of Ocimum sanctum Linn. in Oreochromis mossambicus (Peters). Hydrobiologia 430:113–120CrossRefGoogle Scholar
  22. Lu YC, Yeh WC, Ohashi PS (2008) LPS/TLR4 signal transduction pathway. Cytokine 42:145–151CrossRefGoogle Scholar
  23. Monobe M, Ema K, Kato F, Maeda-Yamamoto M (2008) Immunostimulating activity of a crude polysaccharide derived from green tea (Camellia sinensis) extract. J Agric Food Chem 56:1423–1427CrossRefGoogle Scholar
  24. Muraguchi A, Hirano T, Tang B, Matsuda T, Horii Y, Nakajima K, Kishimoto T (1988) The essential role of B cell stimulatory factor 2 (BSF-2/IL-6) for the terminal differentiation of B cells. J Exp Med 167:332–344CrossRefGoogle Scholar
  25. New L, Han J (1998) The p38 MAP kinase pathway and its biological function. Trends Cardiovasc Med 8:220–228CrossRefGoogle Scholar
  26. Nishi K, Kondo A, Okamoto T, Nakano H, Daifuku M, Nishimoto S, Sugahara T (2011) Immunostimulatory in vitro and in vivo effects of a water-soluble extract from kale. Biosci Biotechnol Biochem 75:40–46CrossRefGoogle Scholar
  27. Ono K, Han J (2000) The p38 signal transduction pathway: activation and function. Cell Signal 12:1–13CrossRefGoogle Scholar
  28. Pantic JM, Mechkarska M, Lukic ML, Conlon JM (2014) Effects of tigerinin peptides on cytokine production by mouse peritoneal macrophages and spleen cells and by human peripheral blood mononuclear cells. Biochimie 101:83–92CrossRefGoogle Scholar
  29. Putra ABN, Morishige H, Nishimoto S, Nishi K, Shiraishi R, Doi M, Sugahara T (2012) Effect of collagens from jellyfish and bovine Achilles tendon on the activity of J774.1 and mouse peritoneal macrophage cells. J Funct Foods 4:504–512CrossRefGoogle Scholar
  30. Putra ABN, Nishi K, Shiraishi R, Doi M, Sugahara T (2014) Jellyfish collagen stimulates production of TNF-α and IL-6 by J774.1 cells through activation of NF-κB and JNK via TLR4 signaling pathway. Mol Immunol 58:32–37CrossRefGoogle Scholar
  31. Putra ABN, Nishi K, Shiraishi R, Doi M, Sugahara T (2015) Jellyfish collagen stimulates maturation of mouse bone marrow-derived dendritic cells. J Funct Foods 14:308–317CrossRefGoogle Scholar
  32. Roberfroid MB (2002) Functional foods: concepts and application to inulin and oligo fructose. Br J Nutr 87:139–143CrossRefGoogle Scholar
  33. Schepetkin IA, Quinn MT (2006) Botanical polysaccharides: macrophage immunomodulation and therapeutic potential. Int Immunopharmacol 6:317–333CrossRefGoogle Scholar
  34. Sica A, Wang JM, Colotta F, Dejana E, Mantovani A, Oppenheim JJ, Larsen CG, Zachariae COC, Matsushima K (1990) Monocyte chemotactic and activating factor gene expression induced in endothelial cells by IL-1 and tumor necrosis factor. J Immunol 144:3034–3038Google Scholar
  35. Tosi MF (2005) Innate immune responses to infection. J Allergy Clin Immunol 116:241–249CrossRefGoogle Scholar
  36. Weston RW, Davis RJ (2002) The JNK signal transduction pathway. Curr Opin Genet Dev 12:14–21CrossRefGoogle Scholar
  37. Zaini NAM, Osman A, Hamid AA, Ebrahimpour A, Saari N (2013) Purification and characterization of membrane-bound polyphenoloxidase (mPPO) from snake fruit [Salacca zalacca (Gaertn.) Voss]. Food Chem 136:407–414CrossRefGoogle Scholar
  38. Zhang G, Ghosh S (2001) Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest 107:13–19CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Sri Wijanarti
    • 1
    • 2
  • Agus Budiawan Naro Putra
    • 1
    • 5
  • Kosuke Nishi
    • 1
  • Eni Harmayani
    • 2
  • Takuya Sugahara
    • 1
    • 3
    • 4
    Email author
  1. 1.Faculty of AgricultureEhime UniversityMatsuyamaJapan
  2. 2.Faculty of Agricultural TechnologyGadjah Mada UniversityYogyakartaIndonesia
  3. 3.Food and Health Sciences Research CenterEhime UniversityMatsuyamaJapan
  4. 4.South Ehime Fisheries Research CenterEhime UniversityAinanJapan
  5. 5.Indonesia International Institute for Life SciencesJakartaIndonesia

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