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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.
    Pubmed CrossRef
  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.
    CrossRef
  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.
    Pubmed PMC CrossRef
  5. Attele AS, Wu JA, Yuan CS. 1999. Ginseng pharmacology:multiple constituents and multiple actions. Biochem. Pharmacol. 58: 1685-1693.
    CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed PMC
  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.
    Pubmed PMC CrossRef
  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.
    Pubmed PMC CrossRef
  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.
    Pubmed PMC CrossRef
  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.
    Pubmed PMC CrossRef
  16. Lauber K, Bohn E, Kröber SM, Xiao Y. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717-730
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed PMC CrossRef
  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.
    CrossRef
  20. Gruenheid S, Finlay BB. 2003. Microbial pathogenesis and cytoskeletal function. Nature 422: 775-781.
    Pubmed CrossRef
  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.
    Pubmed PMC CrossRef
  22. Schorey JS, Cooper AM. 2003. Macrophage signaling upon mycobacterial infection: the MAP kinases lead the way. Cell. Microbiol. 5: 133-142.
    Pubmed CrossRef
  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.
    Pubmed PMC CrossRef
  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.
    Pubmed CrossRef
  25. Sun Y, O’Riordan MX. 2013. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv. Appl. Microbiol. 85: 93-118.
    Pubmed PMC CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(10): 1885-1891

Published online October 28, 2017 https://doi.org/10.4014/jmb.1704.04064

Copyright © The Korean Society for Microbiology and Biotechnology.

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

Huynh Tan Hop 1, Lauren Togonon Arayan 1, Alisha Wehdnesday Bernardo Reyes 1, Tran Xuan Ngoc Huy 1, Eun Jin Baek 1, WonGi Min 1, Hu Jang Lee 1, Chun Hee Lee 2, Man Hee Rhee 2 and Suk Kim 1*

1Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University, Jinju 52828, Republic of Korea, 2College of Veterinary Medicine, Kyungpook National University, Daegu 41566, Republic of Korea

Received: May 2, 2017; Accepted: September 1, 2017

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: B. abortus, phagocyte, rice bran mixture extract, phagocytic signaling, pathogenesis

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.
    Pubmed CrossRef
  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.
    CrossRef
  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.
    Pubmed KoreaMed CrossRef
  5. Attele AS, Wu JA, Yuan CS. 1999. Ginseng pharmacology:multiple constituents and multiple actions. Biochem. Pharmacol. 58: 1685-1693.
    CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed CrossRef
  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.
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed KoreaMed
  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.
    Pubmed KoreaMed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  16. Lauber K, Bohn E, Kröber SM, Xiao Y. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717-730
    CrossRef
  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.
    Pubmed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  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.
    CrossRef
  20. Gruenheid S, Finlay BB. 2003. Microbial pathogenesis and cytoskeletal function. Nature 422: 775-781.
    Pubmed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  22. Schorey JS, Cooper AM. 2003. Macrophage signaling upon mycobacterial infection: the MAP kinases lead the way. Cell. Microbiol. 5: 133-142.
    Pubmed CrossRef
  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.
    Pubmed KoreaMed CrossRef
  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.
    Pubmed CrossRef
  25. Sun Y, O’Riordan MX. 2013. Regulation of bacterial pathogenesis by intestinal short-chain fatty acids. Adv. Appl. Microbiol. 85: 93-118.
    Pubmed KoreaMed CrossRef