Journal of Applied Biological Chemistry

The Korean Society for Applied Biological Chemistry (한국응용생명화학회)
권호 표지
DOI QR코드

DOI QR Code

Bioconversion enhances anti-oxidant and anti-inflammation activities of different parts of the Mulberry Tree (Morus alba L.), especially the leaf (Mori Folium)

  • Chon, So-Hyun (National Development Institute of Korean Medicine) ;
  • Kim, Min-A (National Development Institute of Korean Medicine) ;
  • Lee, Han-Saem (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)
  • Received : 2018.12.03
  • Accepted : 2019.01.09
  • Published : 2019.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

The mulberry tree (Morus alba L.) has been traditionally used in Chinese medicine to treat inflammatory diseases. We investigated the effects of bioconversion on different components of the mulberry tree, and determined changes in the physiological activities. Ethyl acetate-soluble fractions of five different segments (fruit, Mori Fructus; leaf, Mori Folium; twig, Mori Ramulus; root, Mori Cortex; and mistletoe, Loranthi Ramulus) of the mulberry tree show enhanced anti-oxidant effects in the 2,2-diphenyl-1-picrylhydrazyl, and 2,2'-azinobis-(3-ethylvenzothiazoline-6-sulfonic acid) assays, and enhanced anti-inflammatory effects of lipopolysaccharide (LPS)-stimulated nitric oxide (NO) production in RAW 264.7 macrophages, after being treated with a crude enzyme extract from Aspergillus kawachii, in the following order of activity: Mori Folium>Mori Cortex>Mori Ramulus>Mori Fructus>Loranthi Ramulus. Ethyl acetate- soluble fraction of mulberry leaves (Mori Folium) that underwent bioconversion was most effective, and was devoid of any cytotoxicity. The fraction was also effective against mRNA expression of LPS-induced pro-inflammatory cytokines, such as inducible nitric oxide synthase, cyclooxygenase-2, tumor necrosis $factor-{\alpha}$, $interleukin-1{\beta}$, and interleukin-6. In addition, the fraction was effective in LPS-induced phosphorylation of mitogen-activated protein kinases and IKK, and $I{\kappa}B$ degradation, followed by translocation of the nuclear $factor-{\kappa}B$ from the cytoplasm to the nucleus. Thus, bioconversion increased the anti-oxidative and anti-inflammatory activities of the mulberry leaf.

Keywords

References

  1. Kim SI, Kim JE, So JH, Rhee IK, Chung SK, Lee KB, Yoo YC (2004) Changes in chemical composition and biological activities Oriental crude drugs by food processing techniques (I)-Changes in liquiritigenin contents in licorice extract treated by the crude enzyme extract from Aspergillus kawachii. Kor J Pharmacogn 35: 309-314
  2. Yang EJ, Kim SI, Park SY, Bang HY, Jeong JH, So JH, Rhee IK, Song KS (2012) Fermentation enhances the in vitro antioxidative effect of onion (Allium cepa) via an increase in quercetin content. Food Chem Toxico 50: 2042-2048 https://doi.org/10.1016/j.fct.2012.03.065
  3. Jeon KS, Hwang IK, Ji GE (2002) Assay of b-glucosidase activity of Bifidobacteria and the hydrolysis of isoflavone glucosides by Bifidobacterium sp. Int-57 insoymilk fermentation. J Microbiol Biotechnol 12: 8-13
  4. Balsano C, Alisi A (2009) Antioxidant Effects of Natural Bioactive Compounds. Current Pharmaceutical Design 11: 3063-3073 https://doi.org/10.2174/138161209789058084
  5. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agri Food Chem 53: 1841-1856 https://doi.org/10.1021/jf030723c
  6. Naik E, Dixit VM (2011) Mitochondrial reactive oxygen species drive proinflammatory cytokine production. J Exp Med 208: 417-420 https://doi.org/10.1084/jem.20110367
  7. Conese M, Assael BM (2001) Bacterial infections and inammation in the lungs of cystic brosis patients. Pediatric Infectious Disease Journal 20: 207-213 https://doi.org/10.1097/00006454-200102000-00018
  8. Atabai K, Matthay MA (2002) The pulmonary physician in critical care. 5: Acute lung injury and the acute respiratory distress syndrome: Denitions and epidemiology. Thorax 57: 452-458 https://doi.org/10.1136/thorax.57.5.452
  9. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD (2005) Incidence and outcomes of acute lung injury. New Eng J Med 353: 1685-1693 https://doi.org/10.1056/NEJMoa050333
  10. Ulevitch RJ, Tobias PS (1999) Recognition of Gram-negative bacteria and endotoxin by the innate immune system. Curr Opin Immunol 11: 19-22 https://doi.org/10.1016/S0952-7915(99)80004-1
  11. Boje KM (2004) Nitric oxide neurotoxicity in neurodegenerative diseases. Frontiers in Bioscience 9: 763-776 https://doi.org/10.2741/1268
  12. Hartlage-Rubsamen M, Lemke R, Schliebs R (1999) Interleukin-1beta, inducible nitric oxide synthase, and nuclear factor-kappaB are induced in morphologically distinct microglia after rat hippocampal lipopolysaccharide/interferon-gamma injection. J Neuroscience Research 57: 388-398 https://doi.org/10.1002/(SICI)1097-4547(19990801)57:3<388::AID-JNR11>3.0.CO;2-2
  13. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, Sonobe Y, Mizuno T, Suzumura A (2006) Tumor necrosis factor-alpha induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J Biol Chem 281: 21362-21368 https://doi.org/10.1074/jbc.M600504200
  14. Katsube T, Imawaka N, Kawano Y, Yamazaki Y, Shiwaku K, Yamane Y (2006) Antioxidant avonol glycosides in mulberry (Morus alba L.) leaves isolated based on LDL antioxidant activity. Food Chem 97: 25-31 https://doi.org/10.1016/j.foodchem.2005.03.019
  15. Zhang W, Han F, He J, Duan C (2008) HPLC-DAD-ESI-MS/MS analysis and antioxidant activities of nonanthocyanin phenolics in mulberry (Morus alba L.). J Food Sci 73: 512-518 https://doi.org/10.1111/j.1750-3841.2008.00854.x
  16. Huang HP, Shih YW, Chang YC, Hung CN, Wang CJ (2008) Chemoinhibitory effect of mulberry anthocyanins on melanoma metastasis involved in the Ras/PI3K pathway. J Agric Food Chem 56: 9286-9293 https://doi.org/10.1021/jf8013102
  17. Chen CC, Liu LK, Hsu JD, Huang HP, Yang MY (2005) Mulberry extract inhibits the development of atherosclerosis in cholesterol-fed rabbits. Food Chem 91: 601-607 https://doi.org/10.1016/j.foodchem.2004.06.039
  18. Liu LK, Chou FP, Chen YC, Chyau CC, Ho HH (2009) Effects of Mulberry (Morus alba L.) Extracts on Lipid Homeostasis in Vitro and in Vivo. J Agric Food Chem 57: 7605-7611 https://doi.org/10.1021/jf9014697
  19. Kim SB, Chang BY, Jo YH, Lee SH, Han SB (2013) Macrophage activating activity of pyrrole alkaloids from Morus alba fruits. J Ethnopharmacol 145: 393-396 https://doi.org/10.1016/j.jep.2012.11.007
  20. Kang TH, Hur JY, Kim HB, Ryu JH, Kim SY (2006) Neuroprotective effects of the cyanidin-3-O-beta-D-glucopyranoside isolated from mulberry fruit against cerebral ischemia. Neurosci Lett 391: 122-126 https://doi.org/10.1016/j.neulet.2005.08.053
  21. Nidome T, Takahashi K, Goto Y, Goh S, Tanaka N, Kamei K, Ichida M, Hara S, Akaike A, Kihara T (2007) Mulberry leaf extract prevents amyloid beta-peptide bril formation and neurotoxicity. Neuro report 18: 813-816
  22. Blois MS (1958) Antioxidant determination by the use of a stable free radical. Nature 181: 1199-1200 https://doi.org/10.1038/1811199a0
  23. 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
  24. Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH, Affan Abu, Oh CH, Jung WK, Jeon YJ (2010) Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharidestimulated RAW 264.7 macrophages. Food Chem Toxico 48: 2045-2051 https://doi.org/10.1016/j.fct.2010.05.003
  25. Łochynska M, Oleszak G (2011) Multi-use of the white mulberry (Morus alba L.). Ecological questions 15.1: 91-95 https://doi.org/10.12775/v10090-011-0040-5
  26. Georgetti SR (2009) Enhanced in vitro and in vivo antioxidant activity and mobilization of free phenolic compounds of soybean flour fermented with different [beta]-glucosidase-producing fungi. J Applied Microbiology 106: 1364-5072 https://doi.org/10.1111/j.1365-2672.2008.03978.x
  27. Reddy BD, Reddanna P (2009) Chebulagic acid (CA) attenuates LPSinduced inflammation by suppressing $NF-{\kappa}B$ and MAPK activation in RAW 264.7 macrophages. Biochem Biophys Res Commun 381: 112-117 https://doi.org/10.1016/j.bbrc.2009.02.022
  28. Kawai T, Akira S (2006) TLR signaling. Cell Death Differ 13: 816-825 https://doi.org/10.1038/sj.cdd.4401850
  29. Kim KN, Heo SJ, Yoon WJ, Kang SM, Ahn G, Yi TH, Jeon YJ (2010) Fucoxanthin inhibits the inflammatory response by suppressing the activation of $NF-{\kappa}B$ and MAPKs in lipopolysaccharide-induced RAW 264.7 macrophages. Eur J Pharmacol 649: 369-375 https://doi.org/10.1016/j.ejphar.2010.09.032
  30. Jung YJ, Jung JI, Cho HJ, Choi MS, Sung MK, Yu R, Kang YH, Park JH (2014) Berteroin present in cruciferous vegetables exerts potent antiinflammatory properties in murine macrophages and mouse skin. Int J Mol Sci 15: 20686-20705 https://doi.org/10.3390/ijms151120686