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Inhibitory Effect of the Ethanol Extract of a Rice Bran Mixture Comprising Angelica gigas, Cnidium officinale, Artemisia princeps, and Camellia sinensis on Brucella abortus Uptake by Professional and Nonprofessional Phagocytes

  • Hop, Huynh Tan (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Arayan, Lauren Togonon (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Reyes, Alisha Wehdnesday Bernardo (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Huy, Tran Xuan Ngoc (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Baek, Eun Jin (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Min, WonGi (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Lee, Hu Jang (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Lee, Chun Hee (College of Veterinary Medicine, Kyungpook National University) ;
  • Rhee, Man Hee (College of Veterinary Medicine, Kyungpook National University) ;
  • Kim, Suk (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University)
  • Received : 2017.05.02
  • Accepted : 2017.09.01
  • Published : 2017.10.28

Abstract

In this study, we evaluated the inhibitory effect of a rice bran mixture extract (RBE) on Brucella abortus pathogenesis in professional (RAW 264.7) and nonprofessional (HeLa) phagocytes. We fermented the rice bran mixture and then extracted it with 50% ethanol followed by gas chromatography-mass spectrometry to identify the components in RBE. Our results clearly showed that RBE caused a significant reduction in the adherence of B. abortus in both cell lines. Furthermore, analysis of phagocytic signaling proteins by western blot assay revealed that RBE pretreatment resulted in inhibition of phosphorylation of JNK, ERK, and p38, leading to decline of internalization compared with the controls. Additionally, the intensity of F-actin observed by fluorescence microscopy and FACS was remarkably reduced in RBE-pretreated cells compared with control cells. However, the intracellular replication of B. abortus within phagocytes was not affected by RBE. Taken together, these findings suggest that the phagocytic receptor blocking and suppressive effects of RBE on the MAPK-linked phagocytic signaling pathway could negatively affect the invasion of B. abortus into phagocytes.

Keywords

References

  1. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. 2006. The new global map of human brucellosis. Lancet Infect. Dis. 6: 91e9.
  2. Lee JJ, Kim DH, Kim DG, Lee HJ, Min W, Rhee MH, et al. 2012. Phellinus baumii extract influences pathogenesis of Brucella abortus in phagocyte by disrupting the phagocytic and intracellular trafficking pathway. J. Appl. Microbiol. 114: 329-338.
  3. Arayan LT, Simborio HL, Reyes AW, Hop HT, Min W, Lee HJ, et al. 2015. The effects of red ginseng saponin fraction-A (RGSF-A) on phagocytosis and intracellular signaling in Brucella abortus infected RAW 264.7 cells. FEMS Microbiol. Lett. 362: fnv070.
  4. Pasquevich KA, Estein SM, Garcia-Samartino C, Zwerdling A, Coria LM, Barrionuevo P, et al. 2009. Immunization with recombinant Brucella species outer membrane protein Omp16 and Omp19 in adjuvant induces specific CD4+ and CD8+ T cells as well as systemic and oral protection against Brucella abortus infection. Infect. Immun. 77: 436-445. https://doi.org/10.1128/IAI.01151-08
  5. Attele AS, Wu JA, Yuan CS. 1999. Ginseng pharmacology: multiple constituents and multiple actions. Biochem. Pharmacol. 58: 1685-1693. https://doi.org/10.1016/S0006-2952(99)00212-9
  6. Ng TB, Ling JM, Wang ZT, Cai JN, Xu GJ. 1996. Examination of coumarins, flavonoid and polysaccharopeptide for antibacterial activity. Gen. Pharmacol. 27: 1237-1240. https://doi.org/10.1016/0306-3623(95)02143-4
  7. Rehman SU, Chohan ZH, Gulnaz F, Supuran CT. 2005. Invitro antibacterial, antifungal and cytotoxic activities of some coumarins and their metal complexes. J. Enzyme Inhib. Med. Chem. 20: 333-340. https://doi.org/10.1080/14756360500141911
  8. Choi SR, Lee JH, Kim JY, Park KW, Jeong IY, Shim KH, et al. 2011. Decursin from Angelica gigas Nakai induces apoptosis in RC-58T/h/SA#4 primary human prostate cancer cells via a mitochondria-related caspase pathway. Food Chem. Toxicol. 49: 2517-2523. https://doi.org/10.1016/j.fct.2011.06.016
  9. Yim NH, Lee JH, Cho WK, Yang MC, Kwak DH, Ma JY. 2011. Decursin and decursinol angelate from Angelica gigas Nakai induce apoptosis via induction of TRAIL expression on cervical cancer cells. Eur. J. Integr. Med. 3: 299-307. https://doi.org/10.1016/j.eujim.2011.09.007
  10. Lee S, Lee YS, Jung SH, Shin KH, Kim BK, Kang SS. 2003. Anti-tumor activities of decursinol angelate and decursin from Angelica gigas. Arch. Pharm. Res. 26: 727-730. https://doi.org/10.1007/BF02976682
  11. Li L, Du JK, Zou LY, Wu T, Lee YW, Kim YH. 2013. Decursin isolated from Angelica gigas Nakai rescues PC12 cells from amyloid beta-protein-induced neurotoxicity through Nrf2-mediated upregulation of heme oxygenase-1: potential roles of MAPK. Evid. Based Complement. Altern. Med. 2013: 467245.
  12. Lee KE, Shin JA, Hong IS, Cho NP, Cho SD. 2013. Effect of methanol extracts of Cnidium officinale Makino and Capsella bursa-pastoris on the apoptosis of HSC-2 human oral cancer cells. Exp. Ther. Med. 5: 789-792. https://doi.org/10.3892/etm.2012.871
  13. Choi NY, Kang SY, Kim KJ. 2015. Artemisia princeps inhibits biofilm formation and virulence-factor expression of antibioticresistant bacteria. Biomed. Res. Int. 2015: 239519.
  14. Farooqui A, Khan A, Borghetto I, Kazmi SU, Rubino S, Paglietti B. 2015. Synergistic antimicrobial activity of Camellia sisnensis and Juglans regia against multidrug-resistant bacteria. PLoS One 10: e0118431. https://doi.org/10.1371/journal.pone.0118431
  15. Pham PL, Dupont I, Roy D, Lapointe G, Cernin J. 2000. Production of exopolysaccharide by Lactobacillus rhamnosus R and analysis of its enzymatic degradation during prolonged fermentation. Appl. Environ. Microbiol. 66: 2302-2310. https://doi.org/10.1128/AEM.66.6.2302-2310.2000
  16. Lauber K, Bohn E, Krober SM, Xiao Y. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717-730 https://doi.org/10.1016/S0092-8674(03)00422-7
  17. De Bellis P, Valerio F, Sisto A, Lonigro SL, Lavermicocca P. 2010. Probiotic table olives: microbial populations adhering on olive surface in fermentation sets inoculated with the probiotic strain Lactobacillus paracasei IMPC2.1 in an industrial plant. Int. J. Food Microbiol. 140: 6-13. https://doi.org/10.1016/j.ijfoodmicro.2010.02.024
  18. Park JY, Hong M, Jia Q, Lee YC, Yayeh T, Hyun E, et al. 2012. Pistacia chinensis methanolic extract attenuated MAPK and Akt phosphorylations in ADP stimulated rat platelets in vitro. Evid. Based Complement. Alternat. Med. 2012: 895729.
  19. Hop HT, Simborio HL, Reyes AW, Arayan LT, Min W, Lee HJ, et al. 2015. Immunogenicity and protective effect of recombinant Brucella abortus Ndk (rNdk) against a virulent strain B. abortus 544 infection in BALB/c mice. FEMS Microbiol. Lett. 362: fnv003.
  20. Gruenheid S, Finlay BB. 2003. Microbial pathogenesis and cytoskeletal function. Nature 422: 775-781. https://doi.org/10.1038/nature01603
  21. Lee JJ, Kim DG, Kim DH, Simborio HL, Min W, Lee HJ, et al. 2013. Interplay between clathrin and Rab5 controls the early phagocytic trafficking and intracellular survival of Brucella abortus with HeLa cells. J. Biol. Chem. 288: 28049-28057. https://doi.org/10.1074/jbc.M113.491555
  22. Schorey JS, Cooper AM. 2003. Macrophage signaling upon mycobacterial infection: the MAP kinases lead the way. Cell. Microbiol. 5: 133-142. https://doi.org/10.1046/j.1462-5822.2003.00263.x
  23. Doyle SE, O'Connell RM, Miranda GA, Vaidya SA, Chow EK, Liu PT, et al. 2004. Toll-like receptors induce a phagocytic gene program through p38. J. Exp. Med. 199: 81-90. https://doi.org/10.1084/jem.20031237
  24. Lawhon SD, Maurer R, Suyemoto M, Altier C. 2002. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol. Microbiol. 46: 1451-1464. https://doi.org/10.1046/j.1365-2958.2002.03268.x
  25. Sun Y, O'Riordan MX. 2013. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv. Appl. Microbiol. 85: 93-118.

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