The Korean Journal of Mycology (한국균학회지)

The Korean Society of Mycology (한국균학회)
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Hexane and Chloroform Fractions of Laetiporus sulphrueus var. miniatus Inhibit Thrombin-treated Matrix Metalloproteinase-2/9 Expression in Human Oral Squamous Carcinoma YD-10B Cells

  • Kim, Eun-Jung (Department of Biomedical Laboratory Science, Sangji University) ;
  • Yoo, Kwan-Hee (Department of Life Science, Sangji University) ;
  • Kim, Yang-Sup (Sejong institute of Data Analysis) ;
  • Seok, Soon-Ja (Agricultural Microbiology Division, National Institute of Agricultural Sciences) ;
  • Kim, Jun-Ho (Department of Fine Chemistry and New Materials, Sangji University)
  • Received : 2017.06.09
  • Accepted : 2017.08.24
  • Published : 2017.09.01
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Abstract

Laetiporus sulphrueus var. miniatus is widely distributed worldwide, and has commonly been used as a medicinal mushroom. In the present study, we investigated the effects of water extract and solvent fractions from the Laetiporus miniatus as possible antioxidant, anti-thrombin and anti-invasive agents against phorbol 12-myristate 13-acetate (PMA)- or thrombin-induced matrix metalloproteinase-2 (MMP-2) and MMP-9 activities. Samples were fractionated into n-hexane, $CHCl_3$, ethyl acetate, n-butanol, and water fractions, and individually analysed. The water fraction had the highest extraction yield at 34.90% (w/w), while the n-butanol fraction demonstrated the highest anti-oxidative activity at 81.44%. In the thrombin inhibitory activity test, the water fraction exhibited the highest activity at 94.64%. Even at the concentration of $40{\mu}g/mL$, evaluation of anti-proliferating activity in YD-10B cells did not reveal any cytotoxic effects. Although MMP-9 expression in YD-10B cells increased after the addition of PMA and thrombin, MMP-2 did not. Additionally, MMP-2/-9 levels in PMA-treated YD-10B cells (i.e., both mRNA expression and protein activation) were highly inhibited in the hexane and chloroform fractions. Compared with MMP-2 levels, MMP-9 mRNA expression and proteolytic activity were inhibited to a greater extent by the hexane and chloroform fractions in thrombin-treated YD-10B cells. Taken together, these results support that thrombin induces tumor invasion through MMP-2/9 and suggest that the L. miniatus may act as an effective functional food, conferring anti-oxidative, anti-thrombotic and anti-cancer activities.

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References

  1. Kakar P, Lip GY. Hypertension: endothelial dysfunction, the prothrombotic state and antithrombotic state and antithrombotic therapy. Expert Rev Cardiovasc Ther 2007;5:441-50. https://doi.org/10.1586/14779072.5.3.441
  2. Turpie AG. Oral, direct factor Xa inhibitors in development for the prevention and treatment of thromboembolic diseases. Arterioscler Thromb Vasc Biol 2007;27:1238-47. https://doi.org/10.1161/ATVBAHA.107.139402
  3. Meadows TA, Bhatt DL. Clinical aspects of platelet inhibitors and thrombus formation. Circ Res 2007;100:1261-75. https://doi.org/10.1161/01.RES.0000264509.36234.51
  4. Hirsh J, O'Donnell M, Eikelboom JW. Beyond unfractionated heparin and warfarin: current and future advances. Circulation 2007;116:552-60. https://doi.org/10.1161/CIRCULATIONAHA.106.685974
  5. Hart RG, Benavente O, McBride R, Pearce LA. Antithrombotic therapy to prevent stroke in patients with atrial fibrillation: a meta-analysis. Ann Intern Med 1999;131:492-501.
  6. Kim J, Lee JW, Kim SI, Choi YJ, Lee WK, Jeong MJ, Cha SH, Lee HJ, Chun W, Kim SS. Thrombin-induced migration and matrix metalloproteinase-9 expression are regulated by MAPK and PI3K Pathways in C6 glioma cells. Korean J Physiol Pharmacol 2011;15:211-6. https://doi.org/10.4196/kjpp.2011.15.4.211
  7. Choi MS, Kim YE, Lee WJ, Choi JW, Park GH, Kim SD, Jeon SJ, Go HS, Shin SM, Kim WK, et al. Activation of protease-activated receptor 1 mediates induction of matrix metalloproteinase-9 by thrombin in rat primary astrocytes. Brain Res Bull 2008;76:368-75. https://doi.org/10.1016/j.brainresbull.2008.02.031
  8. Radjabi AR, Sawada K, Jagadeeswaran S, Eichbichler A, Kenny HA, Montag A, Bruno K, Lengyel E. Thrombin induces tumor invasion through the induction and association of matrix metalloproteinase-9 and beta-1 integrin on the cell surface. J Biol Chem 2008;283:2822-34. https://doi.org/10.1074/jbc.M704855200
  9. Juarez J, Clayman G, Nakajima M, Tanabe KK, Saya H, Nicolson GL, Boyd D. Role and regulation of expression of 92-kDa type-IV collagenase (MMP-9) in 2 invasive squamous cell carcinoma cell lines of the oral cavity. Int J Cancer 1993;55:10-8. https://doi.org/10.1002/ijc.2910550104
  10. Chiang YY, Tsai MH, Lin TY, Chiang IP. Expression proprofile of metastasis-related genes in invasive oral cancers. Histol Histopathol 2008;23:1213-22.
  11. Wink DA, Hines HB, Cheng RY, Switzer CH, Flores-Santana W, Vitek MP, Ridnour LA, Colton CA. Nitric oxide and redox mechanism in the immune response. J Leukoc Biol 2011;89:873-91. https://doi.org/10.1189/jlb.1010550
  12. Williams MS, Kwon J. T cell receptor stimulation, reactive oxygen species, and cell signaling. Free Radic Biol Med 2004;37:1144-51. https://doi.org/10.1016/j.freeradbiomed.2004.05.029
  13. Nam H, Kim MM. Eugenol with antioxidant activity inhibits MMP-9 related to metastasis in human fibrosarcoma cells. Food Chem Toxicol 2013;55:106-12. https://doi.org/10.1016/j.fct.2012.12.050
  14. Gweon EJ, Kim SJ. Resveratrol induces MMP-9 and cell migration via the p38 kinase and PI-3K pathways in HT1080 human fibrosarcoma cells. Oncol Rep 2013;29:826-34. https://doi.org/10.3892/or.2012.2151
  15. Overeem C van. Laetiporus miniatus (Jungh.) Icon Fung Malay 1925;12:1.
  16. Imazeki R, Hongo T. Colored llustrations of mushrooms of Japan. Vol. II. Osaka: Hoikusha;1989.
  17. Hong MR, Kim YS, Joo AR, Lee JK, Kim YS, Oh DK. Purification and characterization of a thermostable beta-1,3-1,4-glucanase from Laetiporus sulphureus var. miniatus. J Microbiol Biotechnol 2009;19:818-22.
  18. Hwang HS, Lee SH, Baek YM, Kim SW, Jeong YK, Yun JW. Production of extracellular polysaccharides by submerged mycelial culture of Laetiporus sulphureus var. miniatus and their insulinotropic properties. Appl Microbiol Biotechnol 2008;78:419-29. https://doi.org/10.1007/s00253-007-1329-6
  19. Yoshikawa K, Bando S, Arihara S, Matsumura E, Katayama S. A benzofuran glycoside and an acetylenic acid from the fungus Laetiporus sulphureus var. minatus. Chem Pharm Bull (Tokyo) 2001;49:327-9. https://doi.org/10.1248/cpb.49.327
  20. León F, Quintana J, Rivera A, Estévez F, Bermejo J. Lanostanoid tripenes from Laetiporus sulphureus and apoptosis induction on HL-60 human myeloid leukemia cells. J Nat Prod 2004;67:2008-11. https://doi.org/10.1021/np049762o
  21. He JB, Tao J, Miao XS, Bu W, Zhang S, Dong ZJ, Li ZH, Feng T, Liu JK. Seven new drimane-type sesquiterpenoids from cultures of fungus Laetiporus sulphureus. Fitoterapia 2015;102:1-6. https://doi.org/10.1016/j.fitote.2015.01.022
  22. Zhang JW, Wen GL, Zhang L, Duan DM, Ren ZH. Sulphureuine B, a drimane type sesquiterpenoid isolated from Laetiporus sulphureus induces apoptosis in glioma cells. Bangladesh J Pharmacol 2015;10:844-53. https://doi.org/10.3329/bjp.v10i4.23708
  23. Saba E, Son Y, Jeon BR, Kim SE, Lee IK, Yun BS, Rhee MH. Acetyl eburicoic acid from Laetiporus sulphureus var. minatus suppresses inflammation in murine macrophage RAW 264.7 cells. Mycology 2015;43:131-6.
  24. Oh SH, Choi SY, Lee NR, Lee JN, Kim DS, Lee SH, Park SM. Cell migration and anti-inflammatory effect of Red Ginseng extracts fermented with Laetiporus sulphureus. J Soc Cosmet Sci Korea 2014;40:297-305.
  25. Sinanoglou VJ, Zoumpoulakis P, Heropoulos G, Proestos C, Ciric A, Petrovic J, Glamoclija J, Sokovic M. Lipid and fatty acid profile of the edible fugus Laetiporus sulphurous.Antifungal and antibacterial properties. J Food Sci Technol 2015;52:3264-72.
  26. Klaus A, Kozarski M, Niksic M, Jakovljevic D, Todorovic N, Stefanoska I, Van Griensven LJ. The edible mushroom Laetiporus sulphureus as potential source of natural antioxidants. Int J Food Sci Nutr 2013;64:599-610. https://doi.org/10.3109/09637486.2012.759190
  27. Blois MS. Antioxidant determinations by the use of a stale free radical. Nature 1958;181:1199-200. https://doi.org/10.1038/1811199a0
  28. Kim YJ, Kim CK, Kwon YJ. Isolation of antioxidative components of Perillae semen. Korean J Food Sci Technol 1997;29:38-43.
  29. Doljak B, Stegnar M, Urleb U, Kreft S, Umek A, Ciglaric M, Strukelj B, Popovic T. Screening for selective thrombin inhibitor in mushrooms. Blood Coagul Fibrinolysis 2001;12:123-8. https://doi.org/10.1097/00001721-200103000-00006
  30. Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrovic P, Niksic M, Vrvic MM, Griensven LV. Antioxidants of edible mushrooms. Molecules 2015;20:19489-525. https://doi.org/10.3390/molecules201019489
  31. Yun YP, Do JH, Ko SR, Ryu SY, Kim JH, Song HC, Park YD, Ahn KS, Kim SH. Effects of Korean red ginseng and its mixed prescription on the high molecular weight dextran-induced blood stasis in rats and human platelet aggregation. J Ethnopharmacol 2001;77:259-64. https://doi.org/10.1016/S0378-8741(01)00303-8
  32. Vitseva O, Varghese S, Chakrabarti S, Folts JD, Freedman JE. Grape seed and skin extracts inhibit platelet function and release of reactive oxygen intermediates. J Cardiovasc Pharmacol 2005;46:445-51. https://doi.org/10.1097/01.fjc.0000176727.67066.1c
  33. Kim KH, Lee HJ, Lee JH, Jang YS, Kim DK, Shim BS, Cho KH, Ko SG, Ahn KS, Kim SH. Blockade of glycoprotein IIb/IIIa mediates the antithrombotic activity of butanol fraction of Actinostemma lobatum Maxim. J Ethnopharmacol 2008;116:431-8. https://doi.org/10.1016/j.jep.2007.12.012
  34. Kim EJ, Che ZM, Park YJ, Hwang YS, Kim KY, Jung DW, Jeon NK, Choi YW, Lee EJ, Kim J. Morphogenesis and biological significance of spindle cell transformation in a spindle cell carcinoma. Cancer Lett 2009;275:61-71. https://doi.org/10.1016/j.canlet.2008.10.004
  35. Koo BH, Park MY, Jeon OH, Kim DS. Regulatory mechanism of matrix metalloproteinase-2 enzymatic activity by factor Xa and thrombin. J Biol Chem 2009;284:23375-85. https://doi.org/10.1074/jbc.M109.036848
  36. Hwang YS, Park KK,Chung WY. Kalopanaxsaponin a inhibits the invasion of human oral squamous cell carcinoma by reducing metalloproteinase-9 mRNA stability and protein trafficking. Biol Pharm Bull 2012;35:289-300. https://doi.org/10.1248/bpb.35.289
  37. Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC. Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF-kappaB and AP-1. Carcinogenesis 2008;29:147-56.
  38. Park SK, Hwang YS, Park KK, Park HJ, Seo JY, Chung WY. Kalopanaxsaponin a inhibits PMA-induced invasion by reducing metalloproteinase-9 via PI3K/Akt- and PKCdelta-mediated signaling in MCF-7 human breast cancer cells. Carcinogenesis 2009;30:1225-33. https://doi.org/10.1093/carcin/bgp111