Advertisement

Adventitious root cultures of Oplopanax elatus inhibit LPS-induced inflammation via suppressing MAPK and NF-κB signaling pathways

  • Wen Tian
  • Xuan-Mei Piao
  • Cheng-Ri Yin
  • Xiao-Long Jiang
  • Hao-Ding Sun
  • Xiao-Li An
  • Jun JiangEmail author
  • Mei-Lan LianEmail author
Article
  • 134 Downloads

Abstract

Bioreactor-cultured adventitious roots (ARs) of the endangered medicinal plant Oplopanax elatus Nakai is a novel alternative plant material. To utilize ARs in the product production, the present study investigated the anti-inflammatory effect of O. elatus ARs. In the in vivo experiment, lipopolysaccharide (LPS)-induced acute lung injury disease model was established and several inflammatory indexes were determined. For the LPS-stimulated mice, after pretreatment of AR crude extract (200 mg/kg), cell infiltration in lungs was decreased, the production of proinflammatory mediators, including nitric oxide (NO), tumor necrosis factor (TNF)-α, and interleukin (IL)-6, and 1β in the bronchoalveolar lavage fluid was evidently reduced, which indicated that O. elatus ARs had an anti-inflammatory effect. In the in vitro experiment, ethyl acetate (EtOAc) fractions (12.5, 25, and 50 μg/mL) were used to treat LPS-induced peritoneal macrophages (PMs) of mice. The production of NO, prostaglandin E2, TNF-α, IL-6, and IL-1β in LPS-stimulated PMs was obviously inhibited (p < 0.05) after pretreatment with EtOAc fractions, and the expression of the inducible nitric oxide synthase and cyclooxygenase were also suppressed. To clarify the anti-inflammatory mechanism, effects of EtOAc fraction on changes of proteins related to the pathways of mitogen-activated protein kinases (MAPKs) and nuclear factor-kappa B (NF-κB) were investigated. The phosphorylation of extracellular regulated protein kinases, c-jun n-terminal kinase, and p38 MAPK in LPS-induced PMs was inhibited after pretreatment of EtOAc fractions. In addition, EtOAc fractions enhanced inhibitor of nuclear factor-kappa B-α expression and decreased nuclear translocation of p65 NF-κB. Thus, EtOAc from O. elatus ARs is involved in regulating MAKP and NF-κB signaling pathways to inhibit LPS-induced inflammation.

Keywords

Adventitious root Ethyl acetate fraction Proinflammatory mediator Mitogen-activated protein kinase Nuclear factor-kappa B 

Notes

Funding information

This work was supported by the Jilin Scientific and Technological Development Program (Grant No. 20180101278JC) and the National Natural Science Foundation of China (Grant No. 21662038).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aïd S, Bosetti F (2011) Targeting cyclooxygenases-1 and -2 in neuroinflammation: therapeutic implications. Biochimie 93:46–51CrossRefPubMedGoogle Scholar
  2. Bachstetter AD, Xing B, Almeida LD, Dimayuga ER, Watterson DM, Eldik LJV (2011) Microglial p38α MAPK is a key regulator of proinflammatory cytokine up-regulation induced by toll-like receptor (TLR) ligands or beta-amyloid (Aβ). J Neuroinflamm 8:79–91CrossRefGoogle Scholar
  3. Chen H, Bai C, Wang X (2010) The value of the lipopolysaccharide-induced acute lung injury model in respiratory medicine. Expert Rev Resp Med 4:773–783CrossRefGoogle Scholar
  4. Chen X, Tang SA, Lee E, Qiu Y, Wang R, Duan HQ, Dan S, Jin M, Kong D (2015) IVSE, isolated from Inula japonica,suppresses LPS-induced NO production via NF-κB and MAPK inactivation in RAW264.7 cells. Life Sci 124:8–15CrossRefPubMedGoogle Scholar
  5. Dirsch V, Stuppner H, Vollmar A (1998) The Griess assay: suitable for a bioguided fractionation of anti-inflammatory plant extracts? Planta Med 64:423–426CrossRefPubMedGoogle Scholar
  6. Dubios M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  7. Eom SH, Lee JK, Kim H, Hyun TK (2017) De novo transcriptomic analysis to reveal functional genes involved in triterpenoid saponin biosynthesis in Oplopanax elatus Nakai. J Appl Bot Food Qual 90:18–27Google Scholar
  8. Han XZ, Ma R, Chen Q, Jin X, Jin Y, An RB, Piao XM, Lian ML, Quan L, Jiang J (2018) Anti-inflammatory action of Athyrium multidentatum extract suppresses the LPS-induced TLR4 signaling pathway. J Ethnopharmacol 217:220–227CrossRefPubMedGoogle Scholar
  9. Hunot S, Vila M, Teismann P, Davis RJ, Hirsch EC, Przedborski S, Rakic P, Flavell RA (2004) JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 101:665–670CrossRefPubMedPubMedCentralGoogle Scholar
  10. Itoh K, Udagawa N, Kobayashi K, Suda K, Li X, Takami M, Okahashi N, Nishihara T, Takahashi N (2003) Lipopolysaccharide promotes the survival of osteoclasts via Toll-like receptor 4, but cytokine production of osteoclasts in response to lipopolysaccharide is different from that of macrophages. J Immunol 170:3688–3695CrossRefPubMedGoogle Scholar
  11. Jiang XL, Piao XC, Gao R, Jin MY, Jiang J, Jin XH, Lian ML (2017) Improvement of bioactive compound accumulation in adventitious root cultures of an endangered plant species, Oplopanax elatus. Acta Physiol Plant 39:226–235Google Scholar
  12. Jiang YJ, Piao XC, Liu JS, Jiang J, Lian ZX, Kim MJ, Lian ML (2015) Bioactive compound production by adventitious root culture of Oplopanax elatus in balloon-type airlift bioreactor systems and bioactivity property. Plant Cell Tissue Organ Cult 123:413–425CrossRefGoogle Scholar
  13. Kang SM, More SV, Park JY, Kim BW, In PJ, Yoon SH, Choi DK (2014) A novel synthetic HTB derivative, BECT inhibits lipopolysaccharide-mediated inflammatory response by suppressing the p38 MAPK/JNK and NF-κB activation pathways. Pharmacol Rep 66:471–479CrossRefPubMedGoogle Scholar
  14. Kholina A, Nakonechnaya O, Koren O, Zhuravlev Y (2010) Genetic variation of Oplopanax elatus (Nakai) Nakai (Araliaceae). Russ J Gen 46:555–561CrossRefGoogle Scholar
  15. Kilbourn RG, Griffith OW (1992) Overproduction of nitric oxide in cytokine-mediated and septic shock. J Natl Cancer Inst 84:827–831CrossRefPubMedGoogle Scholar
  16. Martinon F, Burns K, Tschopp J (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of pro IL-beta. Mol Cell 10:417–426CrossRefPubMedGoogle Scholar
  17. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63CrossRefPubMedGoogle Scholar
  18. Ruimi N, Rwashdeh H, Wasser S, Konkimalla B, Efferth T, Borgatti M, Gambari R, Mahajna J (2010) Daedalea gibbosa substances inhibit LPS-induced expression of iNOS by suppression of NF-kappaB and MAPK activities in RAW 264.7 macrophage cells. Int J Mol Med 25:421–432PubMedGoogle Scholar
  19. Shikov AN, Pozharitskaya ON, Makarov VG, Makarov VG, Yang WZ, Guo DA (2014) Oplopanax elatus(Nakai) Nakai: chemistry, traditional use and pharmacology. Chin J Nat Med 10:721–729Google Scholar
  20. Shim DW, Han JW, Sun X, Jang CH, Koppula S, Kim TJ, Kang TB, Lee KH (2013) Lysimachia clethroides Duby extract attenuates inflammatory response in Raw 264.7 macrophages stimulated with lipopolysaccharide and in acute lung injury mouse model. J Ethnopharmacol 150:1007–1015CrossRefPubMedGoogle Scholar
  21. Singh D, Singh P, Gupta A, Solanki S, Sharma E, Nema R (2012) Qualitative estimation of bioactive compound present in Centella Asiatica: an important medicinal plant. Int J Life Sci Med Sci 2:5–7Google Scholar
  22. Tewari A, Bedi J, Singh B, Gill JPS (2018) S-adenosylmethionine attenuates the lipopolysaccharide-induced expression of the gene for tumour necrosis factor alpha. Environ Sci Pollut Res 25:15436–15448CrossRefGoogle Scholar
  23. Tianzhu Z, Shihai Y, Juan D (2014) The effects of morin on lipopolysaccharide-induced acute lung injury by suppressing the lung NLRP3 inflammasome. Inflammation 37:1976–1983CrossRefPubMedGoogle Scholar
  24. Uto T (2010) Eriobotryae folium extract suppresses LPS-induced iNOS and COX-2 expression by inhibition of NF-kappaB and MAPK activation in murine macrophages. Am J Chin Med 38:985–994CrossRefPubMedGoogle Scholar
  25. Wen CL, Chang CC, Huang SS, Kuo CL, Hsu SL, Deng JS, Huang GJ (2011) Anti-inflammatory effects of methanol extract of Antrodia cinnamomea mycelia both in vitro and in vivo. J Ethnopharmacol 137:575–584CrossRefPubMedGoogle Scholar
  26. Wu CH, An D, Sun LN, Wang M, Chang GN, Zhao CY, Lian ML (2017) A novel co-culture system of adventitious roots of Echinacea species in bioreactors for high production of bioactive compounds. Plant Cell Tissue Organ Cult 130:1–11Google Scholar
  27. Wu SQ, Lian ML, Gao R, Park SY, Xuan CP (2011) Bioreactor application on adventitious root culture of Astragalus membranaceus. In Vitro Cell Dev Bio-Plant 47:719–724CrossRefGoogle Scholar
  28. Yang M, Kwon HC, Kim YJ, Yang HO (2010) Oploxynes A and B, polyacetylenes from the stems of Oplopanax elatus. J Nat Prod 73:801–805CrossRefPubMedGoogle Scholar
  29. Yin SS, Gao WY, Liang YY, Wang J, Liu H, Wei CL, Zuo BM (2013) Influence of sucrose concentration and phosphate source on biomass and metabolite accumulation in adventitious roots of Pseudostellaria heterophylla. Acta Physiol Plant 35:1579–1585CrossRefGoogle Scholar
  30. Zhang SC, Wang GZ (1980) The effect of Echinopanax elatum Nakai on experimental arthritis and the neurohypophyseal-adrenal system. Acta Pharm Sin 15:81–85Google Scholar

Copyright information

© The Society for In Vitro Biology 2019

Authors and Affiliations

  1. 1.Key Laboratory of Natural Resource of Changbai Mountain and Functional Molecules, Ministry of EducationYanbian UniversityYanjiChina
  2. 2.Department of Urology, College of MedicineChungbuk National UniversityCheongjuRepublic of Korea

Personalised recommendations