Skip to main content
SpringerLink
Log in

Involvement of NF-κB in the inhibitory actions of Platycarya strobilacea on the TNF-α-induced monocyte adhesion to colon epithelial cells and chemokine expression

  • Articles
  • Drug Efficacy and Safety
  • Published:
Archives of Pharmacal Research Aims and scope Submit manuscript

Abstract

Oxidative stress and the activation of nuclear factor (NF)-κB play crucial roles in the pathogenesis of inflammatory bowel disease (IBD). In the present study, we examined the effects of the ethanol extract of Platycarya strobilacea Sieb. stem (EPS) on TNF-α-induced monocyte adhesion to HT29 human colon epithelial cells, an initial step of colon inflammation. EPS contained high amount of polyphenols (0.241±0.017 mg of catechin equivalent/g of extract) and showed substantial DPPH radical scavenging activity. In addition, EPS significantly suppressed TNF-α-induced reactive oxygen species (ROS) increase. Moreover, TNF-α-induced monocyte adhesion to HT29 colon epithelial cells was significantly suppressed by EPS in a concentration-dependent manner. The reduced adhesion by EPS was correlated with suppressed expression of MCP-1 and IL-8, the major chemokines in IBD. EPS also prevented the TNF-α-induced nuclear translocation of NF-κB, one of the redox-sensitive transcription factors, in a concentration-dependent manner. Taken together, our results suggest that the anti-oxidant components of EPS prevent TNF-α-induced NF-κB activation, chemokine induction, and monocyte adhesion at the site of intestinal inflammation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Araki, Y., Sugihara, H., and Hattori, T., The free radical scavengers edaravone and tempol suppress experimental dextran sulfate sodium-induced colitis in mice. Int. J. Mol. Med., 17, 331–334 (2006).

    PubMed  CAS  Google Scholar 

  • Ardizzone, S. and Bianchi, P. G., A practical guide to the management of distal ulcerative colitis. Drugs, 55, 519–542 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Banks, C., Bateman, A., Payne, R., Johnson, P., and Sheron, N., Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn’s disease. J. Pathol., 199, 28–35 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Barnes, P. J. and Karin, M., Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med., 336,1066–1071 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Beak, S. M., Lee, Y. S., and Kim, J. A., NADPH oxidase and cyclooxygenase mediate the ultraviolet B-induced generation of reactive oxygen species and activation of nuclear factor-kappaB in HaCaT human keratinocytes. Biochimie, 86, 425–429 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Begue, B., Wajant, H., Bambou, J. C., Dubuquoy, L., Siegmund, D., Beaulieu, J. F., Canioni, D., Berrebi, D., Brousse, N., Desreumaux, P., Schmitz, J., Lentze, M. J., Goulet, O., Cerf-Bensussan, N., and Ruemmele, F. M., Implication of TNF-related apoptosis-inducing ligand in inflammatory intestinal epithelial lesions. Gastroenterology, 130, 1962–1974 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Blois, M. S., Antioxidant determinations by the use of a stable free radical. Nature, 181, 1199–1200 (1958).

    Article  CAS  Google Scholar 

  • Boirivant, M., Marini, M., Di Felice, G.., Pronio, A. M., Montesani, C., Tersigni, R., and Strober, W., Lamina propria T cells in Crohn’s disease and other gastrointestinal inflammation show defective CD2 pathway-induced apoptosis. Gastroenterology, 116, 557–565 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Choi, Y. H., Chae, S. G., Kim, J. H., Kang, S., Baek, N. I., and Han, J. T., Isolation of an antifungal compound from aerial parts of platycarya strobilacea. J. Appl. Biol. Chem., 46: 268–270 (2003).

    CAS  Google Scholar 

  • Collins, T., Endothelial nuclear factor-êB and the initiation of the atherosclerotic lesion. Lab. Invest., 68, 499–508 (1993).

    PubMed  CAS  Google Scholar 

  • Cooper, D., Stokes, K.Y., Tailor, A., and Granger, D. N., Oxidative stress promotes blood cell-endothelial cell interactions in the microcirculation. Cardiovasc. Toxicol., 2, 165–180 (2002).

    PubMed  CAS  Google Scholar 

  • Craven, P. A., Pfanstiel, J., Saito, R., and DeRubertis, F. R., Actions of sulfasalazine and 5-aminosalicylic acid as reactive oxygen scavengers in the suppression of bile acid-induced increases in colonic epithelial cell loss and proliferative activity. Gastroenterology, 92, 1998–2008 (1987).

    PubMed  CAS  Google Scholar 

  • Daig, R., Andus, T., Aschenbrenner, E., Falk, W., Scholmerich, J., and Gross, V., Increased IL-8 expression in the colon mucosa of patients with inflammatory bowel disease. Gut, 38, 216–222 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Ding, S. Z., Minohara, Y., Fan, X. J., Wang, J., Reyes, V. E., Patel, J., Dirden-Kramer, B., Boldogh, I., Ernst, P. B., and Crowe, S. E., Helicobacter pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect. Immun., 75, 4030–4039 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Dryden, G. W., Song, M., and McClain, C., Polyphenols and gastrointestinal diseases. Curr. Opin. Gastroenterol., 22, 165–170 (2006)

    Article  PubMed  CAS  Google Scholar 

  • Fiers, W., Beyaert, R., Declercq, W., and Vandenabeele, P., More than one way to die: apoptosis, necrosis and reactive oxygen damage. Oncogene, 18, 7719–7730 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Goossens, V., Stangé, G., Moens, K., Pipeleers, D., and Grooten, J., Regulation of tumor necrosis factor-induced, mitochondria-and reactive oxygen species-dependent cell death by the electron flux through the electron transport chain complex I. Antioxid. Redox Signal., 1, 285–295 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Grimm, M. C., Elsbury, S. K., Pavli, P., and Doe, W. F., Enhanced expression and production of monocyte chemoattractant protein-1 in inflammatory bowel disease mucosa. J. Leukoc. Biol., 59, 804–812 (1996).

    PubMed  CAS  Google Scholar 

  • Grisham, M. B., Granger, D. N., and Lefer, D. J., Modulation of leukocyte-endothelial interactions by reactive metabolites of oxygen and nitrogen: relevance to ischemic heart disease. Free Radic. Biol. Med., 25, 404–433 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Hanauer, S. B. and Sandborn, W., Management of Crohn’s disease in adults. Am. J. Gastroenterol., 96, 635–643 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Harris, P. and Ralph, P., Human leukemic models of myelomonocytic development: a review of the HL-60 and U937 cell lines. J. Leukoc. Biol., 37, 407–422 (1985).

    PubMed  CAS  Google Scholar 

  • Isozaki, Y., Yoshida, N., Kuroda, M., Takagi, T., Handa, O., Kokura, S., Ichikawa, H., Naito, Y., Okanoue, T., and Yoshikawa, T., Effect of a novel water-soluble vitamin E derivative as a cure for TNBS-induced colitis in rats. Int. J. Mol. Med., 17, 497–502 (2006).

    PubMed  CAS  Google Scholar 

  • Izzo, R. S., Witkon, K., Chen, A. I., Hadjiyane, C., Weinstein, M. I., and Pellecchia, C., Interleukin 8 and neutrophil markers in colonic mucosa from patients with ulcerative colitis. Am. J. Gastroenterol., 87, 1447–1452 (1992).

    PubMed  CAS  Google Scholar 

  • Kalra, N., Seth, K., Prasad, S., Singh, M., Pant, A. B., and Shukla, Y. Theaflavins induced apoptosis of LNCaP cells is mediated through induction of p53, down-regulation of NFkappa B and mitogen-activated protein kinases pathways. Life Sci., 80, 2137–2146 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Kankuri, E., Vaali, K., Knowles, R. G., Lahde, M., Korpela, R., Vapaatalo, H., and Moilanen, E., Suppression of acute experimental colitis by a highly selective inducible nitric-oxide synthase inhibitor, N-[3-(aminomethyl)benzyl]acetamidine. J. Pharmacol. Exp. Ther., 298, 1128–1132 (2001).

    PubMed  CAS  Google Scholar 

  • Kim, Y. I., Lee, S. H., and Cho, T. S., Isolation of anticancer agents from the leaves of Platycarya strobilacea S. et Z. Kor. J. Pharmacog., 27, 238–245 (1996).

    CAS  Google Scholar 

  • Kim, Y. S., Morgan, M. J., Choksi, S., and Liu, Z.G., TNF-induced activation of the Nox1 NADPH oxidase and its role in the induction of necrotic cell death. Mol. Cell, 26, 675–687 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Kolios, G., Wright, K. L., Jordan, N. J., Leithead, J. B., Robertson, D. A., and Westwick, J., C-X-C and C-C chemokine expression and secretion by the human colonic epithelial cell line, HT-29: differential effect of T lymphocyte-derived cytokines. Eur. J. Immunol., 29, 530–536 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Lee, J. H., Kwon, Y. S., and Kim, C. M., Flavonoids from the stem bark of Platycarya strobilacea. Kor. J. Pharmacog., 29, 353–356 (1998).

    CAS  Google Scholar 

  • Li, J. M., Fan, L. M., Christie, M. R., and Shah, A. M., Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol. Cell Biol., 25, 2320–2330 (2005).

    Article  PubMed  CAS  Google Scholar 

  • MacDermott, R. P., Alterations of the mucosal immune system in inflammatory bowel disease. Gastroenterology, 31, 907–916 (1996).

    Article  CAS  Google Scholar 

  • McCormack, G., Moriarty, D., O’Donoghue, D. P., McComick, P. A., Sheahab, K., and Baird, A. W., Tissue cytokine and chemokine expression in inflammatory bowel disease. Inflamm. Res., 50, 491–495 (2001).

    Article  PubMed  CAS  Google Scholar 

  • McPhillips, K., Janssen, W. J., Ghosh, M., Byrne, A., Gardai, S., Remigio, L., Bratton, D. L., Kang, J. L., and Henson, P., TNF-alpha inhibits macrophage clearance of apoptotic cells via cytosolic phospholipase A2 and oxidant-dependent mechanisms. J. Immunol., 178, 8117–8126 (2007).

    PubMed  CAS  Google Scholar 

  • Matthews, N., Neale, M. L., Jackson, S. K., and Stark, J. M., Tumour cell killing by tumour necrosis factor: inhibition by anaerobic conditions, free-radical scavengers and inhibitors of arachidonate metabolism. Immunology, 62, 153–155 (1987).

    PubMed  CAS  Google Scholar 

  • Mazzucchelli, L., Hauser, C., Zgraggen, K., Wagner, H., Hess, M., Laissue, J. A., and Mueller, C., Expression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation. Am. J. Pathol., 144, 997–1007 (1994).

    PubMed  CAS  Google Scholar 

  • Mazzon, E., Muià, C., Paola, R. D., Genovese, T., Menegazzi, M., De Sarro, A., Suzuki, H., and Cuzzocrea, S., Green tea polyphenol extract attenuates colon injury induced by experimental colitis. Free Radic. Res., 39, 1017–1025 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Nakase, H., Okazaki, K., Tabata, Y., Uose, S., Ohana, M., Uchida, K., Nishi, T., Debreceni, A., Itoh, T., Kawanami, C., Iwano, M., Ikada, Y., and Chiba, T., An oral drug delivery system targeting immune-regulating cells ameliorates mucosal injury in trinitrobenzene sulfonic acid-induced colitis. J. Pharmacol. Exp. Ther., 297, 1122–1128 (2001).

    PubMed  CAS  Google Scholar 

  • Neish, A. S., Williams, A. J., Palmer, H. J., Whitley, M. Z., and Collins, T., Functional analysis of the human vascular cell adhesion molecule 1 promoter. J. Exp. Med., 176, 1583–1593 (1992).

    Article  PubMed  CAS  Google Scholar 

  • Puleston, J., Cooper, M., Murch, S., Bid, K., Makh, S., Ashwood, P., Bingham, A.H., Green, H., Moss, P., Dhillon, A., Morris, R., Strobel, S., Gelinas, R., Pounder, R. E., and Platt, A., A distinct subset of chemokines dominates the mucosal chemokine response in inflammatory bowel disease. Aliment. Pharmacol. Ther., 21, 109–120 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Reinecker, H. C., Loh, E. Y., Ringler, D. J., Mehta, A., Rombeau, J. L., and Mac Dermott, R. P., Monocyte-chemoattractant protein 1 gene expression in intestinal epithelial cells and inflammatory bowel disease mucosa. Gastroenterology, 108, 40–50 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Sartor, R. B., Pathogenesis and immune mechanisms of chronic inflammatory bowel disease. Am. J. Gastroenterol., 92, 58–118 (1997).

    Google Scholar 

  • Scheerens, H., Hessel, E., de Waal-Malefyt, R., Leach, M. W., and Rennick, D., Characterization of chemokines and chemokine receptors in two murine models of inflammatory bowel disease: IL-10-/-mice and Rag-2-/-mice reconstituted with CD4+CD45RBhigh T cells. Eur. J. Immunol., 31, 1465–1474 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Schreiber, S., Raedler, A., Stenson, W. F., and MacDermott, R. P., The immunology of inflammatory bowel disease. Gastroenterol. Clin. North. Am., 21, 451–502 (1992).

    PubMed  CAS  Google Scholar 

  • Schreiber, S., Monocytes or T cells in Crohn’s disease: does IL-16 allow both to play at that game? Gut, 49, 746–749 (2001).

    Article  Google Scholar 

  • Schuerer-Maly, C. C., Eckmann, L., Kagnoff, M. F., Falco, M. T., and Maly, F. E., Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide. Immunology, 81, 85–91 (1994).

    PubMed  CAS  Google Scholar 

  • Segui, J., Gil, F., Gironella, M., Alvarez, M., Gimeno, M., Coronel, P., Closa, D., Pique, J. M., and Panes, J., Down-regulation of endothelial adhesion molecules and leukocyte adhesion by treatment with superoxide dismutase is beneficial in chronic immune experimental colitis. Inflamm. Bowel. Dis., 11, 872–882 (2005).

    Article  PubMed  Google Scholar 

  • Schulze-Osthoff, K., Beyaert, R., Vandevoorde, V., Haegeman, G., and Fiers, W., Depletion of the mitochondrial electron transport abrogates the cytotoxic and gene-inductive effects of TNF. EMBO J., 12, 3095–3104 (1993).

    PubMed  CAS  Google Scholar 

  • Singleton, V. L., Orthofer, R., and Lamuela-Raventos, R. M., Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol., 299, 152–178 (1999).

    Article  CAS  Google Scholar 

  • Stokes, K. Y., Clanton, E. C., Russell, J. M., Ross, C. R., and Granger, D. N., NAD(P)H oxidase-derived superoxide mediates hypercholesterolemia-induced leukocyte-endothelial cell adhesion. Circ. Res., 88, 499–505 (2001).

    PubMed  CAS  Google Scholar 

  • Sun, F. F., Lai, P. S., Yue, G., Yin, K., Nagele, R. G., Tong, D. M., Krzesicki, R. F., Chin, J. E., and Wong, P. Y., Pattern of cytokine and adhesion molecule mRNA in hapten-induced relapsing colon inflammation in the rat. Inflammation, 25, 33–45 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Thurberg, B. L. and Collins, T., The nuclear factor-kappa B/inhibitor of kappa B autoregulatory system and atherosclerosis. Curr. Opin. Lipidol., 9, 387–396 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Ukil, A., Maity, S., and Das, P. K., Protection from experimental colitis by theaflavin-3,3′-digallate correlates with inhibition of IKK and NF-kappaB activation. Br. J. Pharmacol., 149, 121–131 (2006).

    Article  PubMed  CAS  Google Scholar 

  • Van Grevenstein, W. M., Hofland, L. J., van Rossen, M. E., van Koetsveld, P. M., Jeekel, J., and van Eijck, C. H., Inflammatory cytokines stimulate the adhesion of colon carcinoma cells to mesothelial monolayers. Dig. Dis. Sci., 52, 2775–2783 (2007).

    Article  PubMed  CAS  Google Scholar 

  • Varilek, G. W., Yang, F., Lee, E. Y., deVilliers, W. J., Zhong, J., Oz, H. S., Westberry, K. F., and McClain, C. J., Green tea polyphenol extract attenuates inflammation in interleukin-2-deficient mice, a model of autoimmunity. J. Nutr., 131, 2034–2039 (2001).

    PubMed  CAS  Google Scholar 

  • Wajant, H., Pfizenmaier, K., and Scheurich, P., Tumor necrosis factor signaling, Cell Death Differ., 10, 45–65 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Xu, Y. C., Wu, R. F., Gu, Y., Yang, Y. S., Yang, M. C., Nwariaku, F. E., and Terada, L. S., Involvement of TRAF4 in oxidative activation of c-Jun N-terminal kinase. J. Biol. Chem., 277, 28051–28057 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Yatrik, M. S., Keiichirou, M., and Frank, J. G., Expression of Peroxisome Proliferator-Activated Receptor-γ in Macrophage Suppresses Experimentally-Induced Colitis. Am. J. Physiol. Gastrointest. Liver Physiol., 292, G657–G666 (2007).

    Google Scholar 

  • Zareie, M., Singh, P. K., Irvine, E. J., Sherman, P. M., McKay, D. M., and Perdue, M. H., Monocytes/macrophage activation by normal bacteria and bacterial products: implications for altered epithelial function in Crohn’s disease. Am. J. Pathol., 158, 1101–1109 (2001).

    PubMed  CAS  Google Scholar 

  • Zimmerman, R. J., Chan, A., and Leadon, S. A., Oxidative damage in murine tumor cells treated in vitro by recombinant human tumor necrosis factor. Cancer Res., 49, 1644–1648 (1989).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. College of Pharmacy, Yeungnam University, Gyeongsan, 712-749, Korea

    Dinesh Babu, Jong Suk Lee, Su-Young Park, Dinesh Thapa, Mi Kyoung Choi, Ah Ra Kim, Young-Joon Park & Jung-Ae Kim

  2. Research Center, Samil Pharmaceutical Co. Ltd., Ansan, 425-852, Korea

    Young-Joon Park

Authors
  1. Dinesh Babu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jong Suk Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Su-Young Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dinesh Thapa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mi Kyoung Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ah Ra Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Young-Joon Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jung-Ae Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jung-Ae Kim.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Babu, D., Lee, J.S., Park, SY. et al. Involvement of NF-κB in the inhibitory actions of Platycarya strobilacea on the TNF-α-induced monocyte adhesion to colon epithelial cells and chemokine expression. Arch. Pharm. Res. 31, 727–735 (2008). https://doi.org/10.1007/s12272-001-1219-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12272-001-1219-0

Key words

Search

Navigation