Journal of Applied Biological Chemistry

  • 제62권1호
  • /
  • Pages.39-50
  • /
  • 2019
  • /
  • 1976-0442(pISSN)
  • /
  • 2234-7941(eISSN)
한국응용생명화학회 (The Korean Society for Applied Biological Chemistry)
권호 표지
DOI QR코드

DOI QR Code

Bioconversion of Gentiana scabra Bunge increases the anti-inflammatory effect in RAW 264.7 cells via MAP kinases and NF-κB pathway

  • Kim, Min-A (National Development Institute of Korean Medicine) ;
  • Lee, Han-Saem (National Development Institute of Korean Medicine) ;
  • Chon, So-Hyun (National Development Institute of Korean Medicine) ;
  • Park, Jeong-Eun (National Development Institute of Korean Medicine) ;
  • Lim, Yu-Mi (National Development Institute of Korean Medicine) ;
  • Kim, Eun-Jeong (National Development Institute of Korean Medicine) ;
  • Son, Eun-Kyung (National Development Institute of Korean Medicine) ;
  • Kim, Sang-Jun (Department of Natural Science, Republic of Korea Naval Academy) ;
  • So, Jai-Hyun (National Development Institute of Korean Medicine)
  • 투고 : 2018.12.03
  • 심사 : 2019.01.08
  • 발행 : 2019.03.31
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Mitogen-activated protein (MAP) kinases play an important role in cell growth and differentiation, as well as the modulation of proinflammatory cytokines. The objective of this study was to examine the increase in the anti-inflammatory effect of Gentiana scabra Bunge (GSB), due to bioconversion with the Aspergillus kawachii crude enzyme, via inhibition of the $NF-{\kappa}B$ signaling and MAP kinase pathways in RAW 264.7 cells. The expression of inducible nitric oxide synthase (iNOS) and cyclooxygenase-2 in RAW 264.7 cells treated with the GSB ethyl acetate fraction bioconverted with A. kawachii crude enzyme (GE-BA), was dramatically suppressed as compared to GSB ethyl acetate fraction non-bioconverted with the A. kawachii crude enzyme (GE-UA). The phosphorylation of p38, extracellular signal-regulated kinases, and inhibitory ${\kappa}B$ in RAW 264.7 cells treated with GE-BA was further suppressed, as compared to exposure to GE-UA. Moreover, the mRNA expression of interleukin 6, interleukin 1-beta, and tumor necrosis $factor-{\alpha}$ was further suppressed by GE-BA, compared to GE-UA. Similarly, anti-oxidant activities, such as 2,2-diphenyl-1-picrylhydrazyl hydrate and 2,2'-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) radical scavenging activity, of GE-BA were further increased compared to GE-UA. These observations demonstrate that the anti-oxidant and anti-inflammatory activities of GSB ethyl acetate fraction increases as a result from bioconversion with the A. kawachii crude enzyme.

키워드

참고문헌

  1. Dorward DA, Lucas CD, Rossi AG, Haslett C, Dhaliwal K (2012) Imaging inflammation: Molecular strategies to visualize key components of the inflammatory cascade, from initiation to resolution. Pharmacol Ther 135: 182-199 https://doi.org/10.1016/j.pharmthera.2012.05.006
  2. Li S, Wang Y, Zhao M, Wu J, Peng S (2015) BPIC: A novel anti-tumor lead capable of inhibiting inflammation and scavenging free radicals. Bioorg Med Chem Lett 25: 1146-1150 https://doi.org/10.1016/j.bmcl.2014.12.013
  3. Daabis RG, Rehem RNA, Hassan MM, Khalil GI (2016) Hypogonadism in patients with chronic obstructive pulmonary disease: relationship with airflow limitation, muscle weakness and systemic inflammation. Alexandria Univ Facul Med 52: 27-33 https://doi.org/10.1016/j.ajme.2015.01.002
  4. Westermann D, Van Linthout S, Dhayat S, Dhayat N, Schmidt A, Noutsias M, Song XY, Spillmann F, Riad A, Schultheiss HP, Tschope C (2007) Tumor necrosis factor-alpha antagonism protects from myocardial inflammation and fibrosis in experimental diabetic cardiomyopathy. Basic Res Cardiol 102: 500-507 https://doi.org/10.1007/s00395-007-0673-0
  5. Wang F, Ma J, Wang KS, Mi C, Lee JJ, Jin X (2015) Blockade of TNF-$\alpha$-induced NF-${\kappa}B$ signaling pathway and anti-cancer therapeutic response of dihydrotanshinone I. Int Immuno 25: 764-772
  6. Vannini F, Kashfi K, Nath N (2015) The dual role of iNOS in cancer. Redox Biol 6: 334-343 https://doi.org/10.1016/j.redox.2015.08.009
  7. Maskrey BH, Megson IL, Whitfield PD, Rossi AG (2011) Mechanisms of resolution of inflammation a focus on cardiovascular disease. Arterioscler Thromb Vasc Biol 31: 1001-1006 https://doi.org/10.1161/ATVBAHA.110.213850
  8. Lepetsos P, Papavassiliou AG (2016) ROS/oxidative stress signaling in osteoarthritis. Biochim Biophy Acta 1862: 576-591 https://doi.org/10.1016/j.bbadis.2016.01.003
  9. Yang RL, Shi YH, Hao G, Li W, Le GW (2008) Increasing oxidative stress with progressive hyperlipidemia in human. J clin Biochem Nutr 43: 154-158 https://doi.org/10.3164/jcbn.2008044
  10. Zhou J, Xu G, Bai Z, Li K, Yan J, Li F, Ma S, Xu H, Huang K (2015) Selenite exacerbates hepatic insulin resistance in mouse model of type 2 diabetes through oxidative stress-mediated JNK pathway. Toxicol Appl Pharm 289: 409-418 https://doi.org/10.1016/j.taap.2015.10.019
  11. Wang SW, Yang SG, Liu W, Zhang YX, Xu PX, Wang T, Liu RT (2016) Alpha-tocopherol quinine ameliorates spatial memory deficits by reducing beta-amyloid oligomers, neuroinflammation and oxidative stress in transgenic mice with Alzheimer's disease. Behav Brain Res 296: 109-117 https://doi.org/10.1016/j.bbr.2015.09.003
  12. Zo J, Feng D, Ling WH, Duan RD (2013) Lycopene suppresses proinflammatory response in lipopolysaccharide-stimulated macrophages by inhibiting ROS-induced trafficking of TLR4 to lipid raft-like domains. J Nutr Biochem 24: 1117-1122 https://doi.org/10.1016/j.jnutbio.2012.08.011
  13. Seo MJ, Lee YJ, Hwang JH, Kim KJ, Lee BY (2015) The inhibitory effects of quercetin on obesity and obesity-induced inflammation by regulation of MAPK signaling. J Nutr Biochem 26: 1308-1316 https://doi.org/10.1016/j.jnutbio.2015.06.005
  14. Liu D, Perkins JT, Hennig B (2016) EGCG prevents PCB-126-induced endothelial cell inflammation via epigenetic modifications of NF-${\kappa}B$ target genes in human endothelial cells. J Nutr Biochem 28: 164-170 https://doi.org/10.1016/j.jnutbio.2015.10.003
  15. Lee JY, Oh TH, Yune TY (2011) Ghrelin inhibits hydrogen peroxideinduced apoptotic cell death of oligodendrocytes via ERK and p38 MAPK signaling. Endoc 152: 2377-2386 https://doi.org/10.1210/en.2011-0090
  16. Hao Y, Liu C, Huang J, Gu Y, Li H, Yang Z, Li R (2016) Ghrelin protects against depleted uranium-induced apoptosis of MC3T3-E1 cells through oxidative stress-mediated p38-mitogen-activated protein kinase pathway. Toxicol appl pharm 290: 116-125 https://doi.org/10.1016/j.taap.2015.10.022
  17. Peng J, Lv YC, He PP, Tang YY, Xie W, Liu XY, Shi JF (2015) Betulinic acid down regulates expression of oxidative stress-induced lipoprotein lipase via the PKC/ERK/c-Fos pathway in RAW264. 7 macrophages. Bioch 119: 192-203 https://doi.org/10.1016/j.biochi.2015.10.020
  18. Fu J, Shi Q, Song X, Xia X, Su C, Liu Z, Song Y (2016) Tetrachlorobenzoquinone exhibits neurotoxicity by inducing inflammatory responses through ROS-mediated IKK/$I{\kappa}B$/NF-${\kappa}B$ signaling. Envir Toxicol Pharm 41: 241-250 https://doi.org/10.1016/j.etap.2015.12.012
  19. Wang Z, Wang C, Su T, Zhang J (2014) Antioxidant and immunological activities of polysaccharides from Gentiana scabra Bunge roots. Carbo Polym 112: 114-118 https://doi.org/10.1016/j.carbpol.2014.05.077
  20. Wang C, Wang Y, Zhang J, Wang Z (2014) Optimization for the extraction of polysaccharides from Gentiana scabra Bunge and their antioxidant in vitro and anti-tumor activity in vivo. J Tai Inst Chem Engineers 45: 1126-1132 https://doi.org/10.1016/j.jtice.2013.12.004
  21. Kakuda R, Iijima T, Yaoita Y, Machida K, Kikuchi M (2002) Triterpenoids from Gentiana scabra. Phytochem 59: 791-794 https://doi.org/10.1016/S0031-9422(02)00021-3
  22. Kim JA, Son NS, Son JK, Jahng Y, Chang HW, Jang TS, Lee SH (2009) Two new secoiridoid glycosides from the rhizomes of Gentiana scabra Bunge. Arch Pharm Res 32: 863-867 https://doi.org/10.1007/s12272-009-1608-0
  23. Cai W, Xu H, Xie L, Sun J, Sun T, Wu X, Fu Q (2016) Purification, characterization and in vitro anticoagulant activity of polysaccharides from Gentiana scabra Bunge roots. Carbo Polym 140: 308-313 https://doi.org/10.1016/j.carbpol.2015.12.054
  24. Palmerin-Carreno DM, Rutiaga-Quinones OM, Calvo JV, Prado-Barragan A, Huerta-Ochoa S (2015) Screening of microorganisms for bioconversion of (+)-valencene to (+)-nootkatone. LWT-Food Sci Tech 64: 788-793 https://doi.org/10.1016/j.lwt.2015.06.065
  25. Riou C, Salmon JM, Vallier MJ, Gunata Z, Barre P (1998) Purification, characterization, and substrate specificity of a novel highly glucosetolerant $\beta$-glucosidase from Aspergillus oryzae. Appl Environ Microbiol 64: 3607-3614 https://doi.org/10.1128/AEM.64.10.3607-3614.1998
  26. Kan SC, Zang CZ, Yeh CW, Chang WF, Lin CC, Hung TH, Liu YC (2015) Enhanced bioconversion rate and released substrate inhibition in (R)-phenylephrine whole-cell bioconversion via partial acetone treatment. Enzy Microb Technol 86: 34-38 https://doi.org/10.1016/j.enzmictec.2015.11.004
  27. Yang EJ, Kim SI, Park SY, Bang HY, Jeong JH, So JH, Song KS (2012). Fermentation enhances the in vitro antioxidative effect of onion (Allium cepa) via an increase in quercetin content. Food Chem Toxicol 50: 2042-2048 https://doi.org/10.1016/j.fct.2012.03.065
  28. Blois MS (1958) Antioxidant determination by the use of a stable free radical. Nature 26: 1198-1200
  29. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26: 1231-1237 https://doi.org/10.1016/S0891-5849(98)00315-3
  30. Hsu CL, Fang SC, Liu CW, Chen YF (2013) Inhibitory effects of new varieties of bitter melon on lipopolysaccharide-stimulated inflammatory response in RAW 264.7 cells. J Func Food 5: 1829-1837 https://doi.org/10.1016/j.jff.2013.09.002
  31. Kim H, Youn K, Yun EY, Hwang JS, Jeong WS, Ho CT, Jun M (2015) Oleic acid ameliorates $A{\beta}$-induced inflammation by downregulation of COX-2 and iNOS via $NF{\kappa}B$ signaling pathway. J Func Food 14: 1-11 https://doi.org/10.1016/j.jff.2015.01.027
  32. Park EJ, Cheenpracha S, Chang LC, Pezzuto JM (2011) Suppression of cyclooxygenase-2 and inducible NOS expression by epimuqubilin A via IKK/$I{\kappa}B/NF$-${\kappa}B$ pathways in lipopolysaccharide-stimulated RAW 264.7 cells. Phytochem Lett 4: 426-431 https://doi.org/10.1016/j.phytol.2011.07.009
  33. Wann AKT, Chapple JP, Knight MM (2014) The primary cilium influences interleukin-$1{\beta}$-induced NF-${\kappa}B$ signalling by regulating IKK activity. Cellular Signal 26: 1735-1742 https://doi.org/10.1016/j.cellsig.2014.04.004
  34. Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH, Affan A, Oh C, Jung WK, Jeon YJ (2010) Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharidestimulated RAW 264.7 macrophages. Food and Chem Toxi 48: 2045-2051 https://doi.org/10.1016/j.fct.2010.05.003
  35. Floegel A, Kim DO, Chung SJ, Koo SI, Chun OK (2011) Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J Food Comp Analy 24: 1043-1048 https://doi.org/10.1016/j.jfca.2011.01.008
  36. Lafferty EI, Qureshi ST, Schnare M (2010) The role of toll-like receptors in acute and chronic lung inflammation. J Inflam 7: 1-14 https://doi.org/10.1186/1476-9255-7-1
  37. Wu KL, Chan SH, Chan JY (2012) Neuroinflammation and oxidative stress in rostral ventrolateral medulla contribute to neurogenic hypertension induced by systemic inflammation. J Neuroinfla 9: 1-15 https://doi.org/10.1186/1742-2094-9-1
  38. Chesnokova V, Pechnick RN, Wawrowsky K (2016) Chronic peripheral inflammation, hippocampal neurogenesis, and behavior. Brain Behav Immun 58: 1-8 https://doi.org/10.1016/j.bbi.2016.01.017
  39. Karuppagounder V, Arumugam S, Thandavarayan RA, Pitchaimani V, Sreedhar R, Afrin R, Ueno K (2015) Naringenin ameliorates daunorubicin induced nephrotoxicity by mitigating AT1R, ERK1/2-$NF{\kappa}B$ p65 mediated inflammation. Int Immuno 28: 154-159 https://doi.org/10.1016/j.intimp.2015.05.050
  40. Henrissat B, Bairoch A (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 293: 781-788 https://doi.org/10.1042/bj2930781
  41. Singh A (2008) Phytochemicals of Gentianaceae: a review of pharmacological properties. Int J Pharma Sci Nanotec 1: 33-36
  42. Zeng W, Han H, Tao Y, Yang L, Wang Z, Chen K (2013) Identification of bio-active metabolites of gentiopicroside by UPLC/Q-TOF MS and NMR. Biomed Chroma 27: 1129-1136 https://doi.org/10.1002/bmc.2917
  43. Koseki T, Mese Y, Fushinobu S, Masaki K, Fujii T, Ito K, Iefuji H (2008) Biochemical characterization of a glycoside hydrolase family 61 endoglucanase from Aspergillus kawachii. Appl Micro Biotec 77: 1279-1285 https://doi.org/10.1007/s00253-007-1274-4
  44. Wojtunik-Kulesza KA, Oniszczuk A, Oniszczuk T, Waksmundzka-Hajnos M (2016) The influence of common free radicals and antioxidants on development of Alzheimer's Disease. Biomed Pharm 78: 39-49 https://doi.org/10.1016/j.biopha.2015.12.024
  45. Jabbari M, Jabbari A (2016) Antioxidant potential and DPPH radical scavenging kinetics of water-insoluble flavonoid naringenin in aqueous solution of micelles. Colloid Surf A: Physical Engineer Aspects 489: 392-399 https://doi.org/10.1016/j.colsurfa.2015.11.022
  46. Lou H, Hu Y, Zhang L, Sun P, Lu H (2012) Nondestructive evaluation of the changes of total flavonoid, total phenols, ABTS and DPPH radical scavenging activities, and sugars during mulberry (Morus alba L.) fruits development by chlorophyll fluorescence and RGB intensity values. LWT-Food Sci Techno 47: 19-24 https://doi.org/10.1016/j.lwt.2012.01.008
  47. Kwaw E, Ma Y, Tchabo W, Apaliya MT, Wu M, Sacle Sackey A, Xiao L, Tahir HE (2018) Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic -acid-fermented mulberry juice. Food Chem 250: 148-154 https://doi.org/10.1016/j.foodchem.2018.01.009
  48. Lai CS, Lee JH, Ho CT, Liu CB, Wang JM, Wang YJ, Pan MH (2009) Rosmanol potently inhibits lipopolysaccharide-induced iNOS and COX- 2 expression through down regulating MAPK, NF-${\kappa}B$, STAT3 and C/EBP signaling pathways. J Agri Food Chem 57: 10990-10998 https://doi.org/10.1021/jf9025713
  49. Dannenberg AJ, Lippman SM, Mann JR, Subbaramaiah K, DuBois RN (2005) Cyclooxygenase-2 and epidermal growth factor receptor: pharmacologic targets for chemoprevention. J Clin Oncol 23: 254-266 https://doi.org/10.1200/JCO.2005.09.112
  50. Nahar PP, Driscoll MV, Li L, Slitt AL, Seeram NP (2014) Phenolic mediated anti-inflammatory properties of a maple syrup extract in RAW 264.7 murine macrophages. J Func Foods 6: 126-136 https://doi.org/10.1016/j.jff.2013.09.026
  51. Xiong H, Cheng Y, Zhang X, Zhang X (2014) Effects of taraxasterol on iNOS and COX-2 expression in LPS-induced RAW 264.7 macrophages. J Ethnopharm 155: 753-757 https://doi.org/10.1016/j.jep.2014.06.023
  52. Lee J, Tae N, Lee JJ, Kim T, Lee JH (2010) Eupatolide inhibits lipopolysaccharide-induced COX-2 and iNOS expression in RAW264. 7 cells by inducing proteasomal degradation of TRAF6. Eur J Pharm 636: 173-180 https://doi.org/10.1016/j.ejphar.2010.03.021
  53. Yokota T, Wang Y (2016) p38 MAP kinases in the heart. Gene 575: 369-376 https://doi.org/10.1016/j.gene.2015.09.030
  54. Park EJ, Shen L, Sun D, Pezzuto JM (2013) Inhibitory effect of a callophycin A derivative on iNOS expression via inhibition of Akt in lipopolysaccharide-stimulated RAW 264.7 cells. J Nat Prod 77: 527-535 https://doi.org/10.1021/np400800h
  55. Pasquali MAB, Gelain DP, Zeidan-Chuli F, Pires AS, Gasparotto J, Terra SR, Moreira JCF (2013) Vitamin A (retinol) down regulates the receptor for advanced glycation endproducts (RAGE) by oxidant-dependent activation of p38 MAPK and NF-${\kappa}B$ in human lung cancer A549 cells. Cell Signal. 25: 939-954 https://doi.org/10.1016/j.cellsig.2013.01.013
  56. Zhang TZ, Yang SH, Yao JF, Du J, Yan TH (2015) Sangxingtang inhibits the inflammation of LPS-induced acute lung injury in mice by downregulating the MAPK/NF-${\kappa}B$ pathway. Chin J Nat Med 13: 889-895 https://doi.org/10.1016/S1875-5364(15)30094-7
  57. Ma JQ, Li Z, Xie WR, Liu CM, Liu SS (1998) Quercetin protects mouse liver against CCl 4-induced inflammation by the TLR2/4 and MAPK/NF-${\kappa}B$ pathway. Int Immun 28: 531-539 https://doi.org/10.1016/j.intimp.2015.06.036
  58. Lee JI, Burckart GJ (1998) Nuclear factor kappa B: important transcription factor and therapeutic target. J Clin Pharm 38: 981-993 https://doi.org/10.1177/009127009803801101
  59. Zeng KW, Yu Q, Song FJ, Liao LX, Zhao MB, Dong X, Tu PF (2015) Deoxysappanone B, a homo isoflavone from the Chinese medicinal plant Caesalpinia sappan L., protects neurons from microglia-mediated inflammatory injuries via inhibition of IeB kinase (IKK)-NF-${\kappa}B$ and p38/ERK MAPK pathways. Eur J Pharm 748: 18-29 https://doi.org/10.1016/j.ejphar.2014.12.013
  60. Hu TY, Ju JM, Mo LH, Ma L, Hu WH, You RR, Chen XQ, Chen YY, Liu ZQ, Qiu LZ, Qiu SQ, Fan JT, Cheng BH (2019) Anti-inflammation action of xanthones from Swertia chirayita by regulating COX-2/NF-${\kappa}B$/MAPKs/AKt signaling pathways in RAW 264.7 macrophage cells. Phytomed 55: 214-221 https://doi.org/10.1016/j.phymed.2018.08.001

피인용 문헌

  1. Systems pharmacology to reveal multi-scale mechanisms of traditional Chinese medicine for gastric cancer vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-01535-5