The ginger component 6-shogaol prevents TNF-α-induced barrier loss via inhibition of PI3K/Akt and NF-κB signaling

Molecular Nutrition and Food Research

Volumn 60, Issue 12, 2016, Pages 2576-2586

  Luettig, Julia ^a   Rosenthal, Rita ^a   Lee, In Fah M ^a   Krug, Susanne M ^a   Schulzke, Jörg D ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

6 Shogaol; Ginger; Intestinal barrier; Tight junction; TNF

Indexed keywords

ANTIINFLAMMATORY AGENT; CATECHOL DERIVATIVE; CLAUDIN; CLAUDIN 1; CLDN1 PROTEIN, HUMAN; CLDN2 PROTEIN, HUMAN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; SHOGAOL; TUMOR NECROSIS FACTOR;

B LYMPHOCYTE; CACO-2 CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENETICS; GINGER; HT-29 CELL LINE; HUMAN; INTESTINE; METABOLISM; SIGNAL TRANSDUCTION; TIGHT JUNCTION; UPREGULATION;

ANTI-INFLAMMATORY AGENTS; B-LYMPHOCYTES; CACO-2 CELLS; CATECHOLS; CLAUDIN-1; CLAUDINS; GINGER; HT29 CELLS; HUMANS; INTESTINES; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84987856233     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201600274     Document Type: Article

References (45)

1. Ali, B. H., Blunden, G., Tanira, M. O., Nemmar, A., Some phytochemical, pharmacological and toxicological properties of ginger (Zingiber officinale Roscoe): a review of recent research. Food Chem. Toxicol. 2008, 46, 409–420.
2. Chrubasik, S., Pittler, M. H., Roufogalis, B. D., Zingiberis rhizoma: a comprehensive review on the ginger effect and efficacy profiles. Phytomedicine 2005, 12, 684–701.
3. Kundu, J. K., Na, H. K., Surh, Y. J., Ginger-derived phenolic substances with cancer preventive and therapeutic potential. Forum Nutr. 2009, 61, 182–192.
4. Dugasani, S., Pichika, M. R., Nadarajah, V. D., Balijepalli, M. K. et al., Comparative antioxidant and anti-inflammatory effects of [6]-gingerol, [8]-gingerol, [10]-gingerol and [6]-shogaol. J. Ethnopharmacol. 2010, 127, 515–520.
5. Ling, H., Yang, H., Tan, S. H., Chui, W. K., Chew, E. H., 6-Shogaol, an active constituent of ginger, inhibits breast cancer cell invasion by reducing matrix metalloproteinase-9 expression via blockade of nuclear factor-kappaB activation. Br. J. Pharmacol. 2010, 161, 1763–1777.
6. Pan, M. H., Hsieh, M. C., Hsu, P. C., Ho, S. Y. et al., 6-Shogaol suppressed lipopolysaccharide-induced up-expression of iNOS and COX-2 in murine macrophages. Mol. Nutr. Food Res. 2008, 52, 1467–1477.
7. Sohn, Y., Han, N. Y., Lee, M. J., Cho, H. J., Jung, H. S., [6]-Shogaol inhibits the production of proinflammatory cytokines via regulation of NF-kappaB and phosphorylation of JNK in HMC-1 cells. Immunopharmacol. Immunotoxicol. 2013, 35, 462–470.
8. Neurath, M. F., Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 2014, 14, 329–342.
9. Heller, F., Florian, P., Bojarski, C., Richter, J. et al., Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterology 2005, 129, 550–564.
10. Zeissig, S., Bürgel, N., Günzel, D., Richter, J. et al., Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut 2007, 56, 61–72.
11. Günzel, D., Yu, A. S., Claudins and the modulation of tight junction permeability. Physiol. Rev. 2013, 93, 525–569.
12. Inai, T., Kobayashi, J., Shibata, Y., Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur. J. Cell Biol. 1999, 78, 849–855.
13. Furuse, M., Hata, M., Furuse, K., Yoshida, Y. et al., Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J. Cell Biol. 2002, 156, 1099–1111.
14. Bürgel, N., Bojarski, C., Mankertz, J., Zeitz, M. et al., Mechanisms of diarrhea in collagenous colitis. Gastroenterology 2002, 123, 433–443.
15. Lameris, A. L., Huybers, S., Kaukinen, K., Makela, T. H. et al., Expression profiling of claudins in the human gastrointestinal tract in health and during inflammatory bowel disease. Scand. J. Gastroenterol. 2013, 48, 58–69.
16. Amasheh, S., Meiri, N., Gitter, A. H., Schöneberg, T. et al., Claudin-2 expression induces cation-selective channels in tight junctions of epithelial cells. J. Cell Sci. 2002, 115, 4969–4976.
17. Rosenthal, R., Milatz, S., Krug, S. M., Oelrich, B. et al., Claudin-2, a component of the tight junction, forms a paracellular water channel. J. Cell Sci. 2010, 123, 1913–1921.
18. Kreusel, K. M., Fromm, M., Schulzke, J. D., Hegel, U., Cl- secretion in epithelial monolayers of mucus-forming human colon cells (HT-29/B6). Am. J. Physiol. 1991, 261, C574–C582.
19. Schmitz, H., Fromm, M., Bentzel, C. J., Scholz, P. et al., Tumor necrosis factor-alpha (TNFalpha) regulates the epithelial barrier in the human intestinal cell line HT-29/B6. J. Cell Sci. 1999, 112, 137–146.
20. Mankertz, J., Amasheh, M., Krug, S. M., Fromm, A. et al., TNFalpha up-regulates claudin-2 expression in epithelial HT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res. 2009, 336, 67–77.
21. Amasheh, M., Fromm, A., Krug, S. M., Amasheh, S. et al., TNFalpha-induced and berberine-antagonized tight junction barrier impairment via tyrosine kinase, Akt and NFkappaB signaling. J. Cell Sci. 2010, 123, 4145–4155.
22. Capaldo, C. T., Farkas, A. E., Hilgarth, R. S., Krug, S. M. et al., Proinflammatory cytokine-induced tight junction remodeling through dynamic self-assembly of claudins. Mol. Biol. Cell 2014, 25, 2710–2719.
23. Sabina, E. P., Rasool, M., Mathew, L., Ezilrani, P., Indu, H., 6-Shogaol inhibits monosodium urate crystal-induced inflammation–an in vivo and in vitro study. Food Chem. Toxicol. 2010, 48, 229–235.
24. Kim, S. O., Kim, M. R., [6]-Gingerol prevents disassembly of cell junctions and activities of MMPs in invasive human pancreas cancer cells through ERK/NF-kappa B/snail signal transduction pathway. Evid. Based Complement. Alternat. Med. 2013, 2013, 761852, 1–9.
25. Cui, W., Li, L. X., Sun, C. M., Wen, Y. et al., Tumor necrosis factor alpha increases epithelial barrier permeability by disrupting tight junctions in Caco-2 cells. Braz. J. Med. Biol. Res. 2010, 43, 330–337.
26. Gitter, A. H., Bendfeldt, K., Schmitz, H., Schulzke, J. D. et al., Epithelial barrier defects in HT-29/B6 colonic cell monolayers induced by tumor necrosis factor-alpha. Ann. N Y Acad. Sci. 2000, 915, 193–203.
27. McKay, D. M., Singh, P. K., Superantigen activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via IFN-gamma and TNF alpha: inhibition of increased permeability, but not diminished secretory responses by TGF-beta2. J. Immunol. 1997, 159, 2382–2390.
28. Baker, O. J., Camden, J. M., Redman, R. S., Jones, J. E. et al., Proinflammatory cytokines tumor necrosis factor-alpha and interferon-gamma alter tight junction structure and function in the rat parotid gland Par-C10 cell line. Am. J. Physiol. Cell Physiol. 2008, 295, C1191–C1201.
29. Poritz, L. S., Garver, K. I., Tilberg, A. F., Koltun, W. A., Tumor necrosis factor alpha disrupts tight junction assembly. J. Surg. Res. 2004, 116, 14–18.
30. Fujita, H., Chalubinski, M., Rhyner, C., Indermitte, P. et al., Claudin-1 expression in airway smooth muscle exacerbates airway remodeling in asthmatic subjects. J. Allergy Clin. Immunol. 2011, 127, 1612–1621 e1618.
31. Kondo, J., Sato, F., Kusumi, T., Liu, Y. et al., Claudin-1 expression is induced by tumor necrosis factor-alpha in human pancreatic cancer cells. Int. J. Mol. Med. 2008, 22, 645–649.
32. Liu, Y., Wang, L., Lin, X. Y., Wang, J. et al., Anti-apoptotic effect of claudin-1 on TNF-alpha-induced apoptosis in human breast cancer MCF-7 cells. Tumour Biol. 2012, 33, 2307–2315.
33. Shiozaki, A., Bai, X. H., Shen-Tu, G., Moodley, S. et al., Claudin 1 mediates TNFalpha-induced gene expression and cell migration in human lung carcinoma cells. PLoS One 2012, 7, e38049.
34. Cao, M., Wang, P., Sun, C., He, W., Wang, F., Amelioration of IFN-gamma and TNF-alpha-induced intestinal epithelial barrier dysfunction by berberine via suppression of MLCK-MLC phosphorylation signaling pathway. PLoS One 2013, 8, e61944.
35. Tang, Y., Clayburgh, D. R., Mittal, N., Goretsky, T. et al., Epithelial NF-kappaB enhances transmucosal fluid movement by altering tight junction protein composition after T cell activation. Am. J. Pathol. 2010, 176, 158–167.
36. Oeckinghaus, A., Hayden, M. S., Ghosh, S., Crosstalk in NF-kappaB signaling pathways. Nat. Immunol. 2011, 12, 695–708.
37. Wu, Y., Zhou, B. P., TNF-alpha/NF-kappaB/Snail pathway in cancer cell migration and invasion. Br. J. Cancer 2010, 102, 639–644.
38. Andresen, L., Jorgensen, V. L., Perner, A., Hansen, A. et al., Activation of nuclear factor kappaB in colonic mucosa from patients with collagenous and ulcerative colitis. Gut 2005, 54, 503–509.
39. Atreya, I., Atreya, R., Neurath, M. F., NF-kappaB in inflammatory bowel disease. J. Intern. Med. 2008, 263, 591–596.
40. Ellis, R. D., Goodlad, J. R., Limb, G. A., Powell, J. J. et al., Activation of nuclear factor kappa B in Crohn's disease. Inflamm. Res. 1998, 47, 440–445.
41. Tan, B. S., Kang, O., Mai, C. W., Tiong, K. H. et al., 6-Shogaol inhibits breast and colon cancer cell proliferation through activation of peroxisomal proliferator activated receptor gamma (PPARgamma). Cancer Lett. 2013, 336, 127–139.
42. Luettig, J., Rosenthal, R., Barmeyer, C., Schulzke, J. D., Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers 2015, 3, e977176.
43. Gonzalez-Mariscal, L., Chavez de Ramirez, B., Lazaro, A., Cereijido, M., Establishment of tight junctions between cells from different animal species and different sealing capacities. J. Membr. Biol. 1989, 107, 43–56.
44. Zick, S. M., Djuric, Z., Ruffin, M. T., Litzinger, A. J. et al., Pharmacokinetics of 6-gingerol, 8-gingerol, 10-gingerol, and 6-shogaol and conjugate metabolites in healthy human subjects. Cancer Epidemiol. Biomarkers Prev. 2008, 17, 1930–1936.
45. Yu, Y., Zick, S., Li, X., Zou, P. et al., Examination of the pharmacokinetics of active ingredients of ginger in humans. Am. Assoc. Pharm. Sci. J. 2011, 13, 417–426.