Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2014 (2014), Article ID 128919, 12 pages
http://dx.doi.org/10.1155/2014/128919
Research Article

Anti-Inflammatory Mechanism of Polyunsaturated Fatty Acids in Helicobacter pylori-Infected Gastric Epithelial Cells

1Department of Food and Nutrition, Brain Korea 21 PLUS Project, College of Human Ecology, Yonsei University, Seoul 120-749, Republic of Korea
2Department of Microbiology, Hanyang University College of Medicine, Seoul 133-791, Republic of Korea

Received 8 January 2014; Accepted 16 May 2014; Published 2 June 2014

Academic Editor: Philipp M. Lepper

Copyright © 2014 Sun Eun Lee et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. X. Calvet, M. J. Ramirez Lazaro, P. Lehours, and F. Megraud, “Diagnosis and epidemiology of Helicobacter pylori infection,” Helicobacter, vol. 18, 1, pp. 5–11, 2013. View at Google Scholar
  2. P. Sipponen and H. Hyvarinen, “Role of Helicobacter pylori in the pathogenesis of gastritis, peptic ulcer and gastric cancer,” Scandinavian Journal of Gastroenterology, Supplement, vol. 28, no. 196, pp. 3–6, 1993. View at Google Scholar · View at Scopus
  3. D. Y. Graham, “Pathogenic mechanisms leading to Helicobacter pylori-induced inflammation,” European Journal of Gastroenterology and Hepatology, vol. 4, no. 2, pp. S9–S16, 1992. View at Google Scholar · View at Scopus
  4. J. Huang, P. W. O'Toole, P. Doig, and T. J. Trust, “Stimulation of interleukin-8 production in epithelial cell lines by Helicobacter pylori,” Infection and Immunity, vol. 63, no. 5, pp. 1732–1738, 1995. View at Google Scholar · View at Scopus
  5. P. M. Craig, M. C. Territo, W. E. Karnes, and J. H. Walsh, “Helicobacter pylori secretes a chemotactic factor for monocytes and neutrophils,” Gut, vol. 33, no. 8, pp. 1020–1023, 1992. View at Google Scholar · View at Scopus
  6. S. A. Sharma, M. K. R. Tummuru, G. G. Miller, and M. J. Blaser, “Interleukin-8 response of gastric epithelial cell lines to Helicobacter pylori stimulation in vitro,” Infection and Immunity, vol. 63, no. 5, pp. 1681–1687, 1995. View at Google Scholar · View at Scopus
  7. J. E. Crabtree, J. I. Wyatt, L. K. Trejdosiewicz et al., “Interleukin-8 expression in Helicobacter pylori infected, normal, and neoplastic gastroduodenal mucosa,” Journal of Clinical Pathology, vol. 47, no. 1, pp. 61–66, 1994. View at Google Scholar · View at Scopus
  8. S. Backert and M. Naumann, “What a disorder: proinflammatory signaling pathways induced by Helicobacter pylori,” Trends in Microbiology, vol. 18, no. 11, pp. 479–486, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Hoffmann, O. Dittrich-Breiholz, H. Holtmann, and M. Kracht, “Multiple control of interleukin-8 gene expression,” Journal of Leukocyte Biology, vol. 72, no. 5, pp. 847–855, 2002. View at Google Scholar · View at Scopus
  10. H. Kim, J. W. Lim, and K. H. Kim, “Helicobacter pylori-induced expression of interleukin-8 and cyclooxygenase-2 in AGS gastric epithelial cells: mediation by nuclear factor-κB,” Scandinavian Journal of Gastroenterology, vol. 36, no. 7, pp. 706–716, 2001. View at Google Scholar · View at Scopus
  11. P. A. Baeuerle and D. Baltimore, “Nf-κB: ten years after,” Cell, vol. 87, no. 1, pp. 13–20, 1996. View at Publisher · View at Google Scholar · View at Scopus
  12. D. Thanos and T. Maniatis, “NF-κB: a lesson in family values,” Cell, vol. 80, no. 4, pp. 529–532, 1995. View at Google Scholar · View at Scopus
  13. M. Karin, Z.-G. Liu, and E. Zandi, “AP-1 function and regulation,” Current Opinion in Cell Biology, vol. 9, no. 2, pp. 240–246, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. S. H. Chu, H. Kim, J. Y. Seo, J. W. Lim, N. Mukaida, and K. H. Kim, “Role of NF-κB and AP-1 on Helicobater pylori-induced IL-8 expression in AGS cells,” Digestive Diseases and Sciences, vol. 48, no. 2, pp. 257–265, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Yamada, T. Aihara, and S. Okabe, “Mechanism for Helicobacter pylori stimulation of interleukin-8 production in a gastric epithelial cell line (MKN 28): roles of mitogen-activated protein kinase and interleukin-1β,” Biochemical Pharmacology, vol. 61, no. 12, pp. 1595–1604, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. A. G. Turjanski, J. P. Vaqué, and J. S. Gutkind, “MAP kinases and the control of nuclear events,” Oncogene, vol. 26, no. 22, pp. 3240–3253, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. J. H. Seo, J. W. Lim, H. Kim, and K. H. Kim, “Helicobacter pylori in a Korean isolate activates mitogen-activated protein kinases, AP-1, and NF-κB and induces chemokine expression in gastric epithelial AGS cells,” Laboratory Investigation, vol. 84, no. 1, pp. 49–62, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. T.-C. Hsu, M. R. Young, J. Cmarik, and N. H. Colburn, “Activator protein 1 (AP-1)- and nuclear factor κB (NF-κB)-dependent transcriptional events in carcinogenesis,” Free Radical Biology and Medicine, vol. 28, no. 9, pp. 1338–1348, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Liebmann, “Regulation of MAP kinase activity by peptide receptor signalling pathway: paradigms of multiplicity,” Cellular Signalling, vol. 13, no. 11, pp. 777–785, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Carpenter, “The EGF receptor: a nexus for trafficking and signaling,” Bioessays, vol. 22, no. 8, pp. 697–707, 2000. View at Google Scholar
  21. S. Keates, S. Sougioultzis, A. C. Keates et al., “cag+ Helicobacter pylori Induce Transactivation of the Epidermal Growth Factor Receptor in AGS Gastric Epithelial Cells,” The Journal of Biological Chemistry, vol. 276, no. 51, pp. 48127–48134, 2001. View at Google Scholar · View at Scopus
  22. C. Wallasch, J. E. Crabtree, D. Bevec, P. A. Robinson, H. Wagner, and A. Ullrich, “Helicobacter pylori-stimulated EGF receptor transactivation requires metalloprotease cleavage of HB-EGF,” Biochemical and Biophysical Research Communications, vol. 295, no. 3, pp. 695–701, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. A. Hashimoto, M. Kurosaki, N. Gotoh, M. Shibuya, and T. Kurosaki, “Shc regulates epidermal growth factor-induced activation of the JNK signaling pathway,” The Journal of Biological Chemistry, vol. 274, no. 29, pp. 20139–20143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. U. Kikkawa, H. Matsuzaki, and T. Yamamoto, “Protein kinase Cδ (PKCδ): activation mechanisms and functions,” The Journal of Biological Chemistry, vol. 132, no. 6, pp. 831–839, 2002. View at Google Scholar · View at Scopus
  25. K. Kassai, T. Yoshikawa, N. Yoshida, A. Hashiramoto, M. Kondo, and H. Murase, “Helicobacter pylori water extract induces interleukin-8 production by gastric epithelial cells,” Digestive Diseases and Sciences, vol. 44, no. 2, pp. 237–242, 1999. View at Google Scholar · View at Scopus
  26. S. Brandt, S. Wessler, R. Hartig, and S. Backert, “Helicobacter pylori activates protein kinase C delta to control Raf in MAP kinase signalling: role in AGS epithelial cell scattering and elongation,” Cell Motility and the Cytoskeleton, vol. 66, no. 10, pp. 874–892, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. O. Sokolova, M. Vieth, and M. Naumann, “Protein kinase C isozymes regulate matrix metalloproteinase-1 expression and cell invasion in Helicobacter pylori infection,” Gut, vol. 62, no. 3, pp. 358–367, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. P. C. Calder, “n-3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases,” American Journal of Clinical Nutrition, vol. 83, no. 6, pp. 1505S–1519S, 2006. View at Google Scholar · View at Scopus
  29. P. C. Calder, “Dietary modification of inflammation with lipids,” Proceedings of the Nutrition Society, vol. 61, no. 3, pp. 345–358, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. A. P. Simopoulos, “Omega-3 fatty acids in inflammation and autoimmune diseases,” Journal of the American College of Nutrition, vol. 21, no. 6, pp. 495–505, 2002. View at Google Scholar · View at Scopus
  31. M. J. James, R. A. Gibson, and L. G. Cleland, “Dietary polyunsaturated fatty acids and inflammatory mediator production,” American Journal of Clinical Nutrition, vol. 71, no. 1, pp. 343S–348S, 2000. View at Google Scholar · View at Scopus
  32. J. Bassaganya-Riera, R. Hontecillas, and D. C. Beitz, “Colonic anti-inflammatory mechanisms of conjugated linoleic acid,” Clinical Nutrition, vol. 21, no. 6, pp. 451–459, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Mullen, C. E. Loscher, and H. M. Roche, “Anti-inflammatory effects of EPA and DHA are dependent upon time and dose-response elements associated with LPS stimulation in THP-1-derived macrophages,” The Journal of Nutritional Biochemistry, vol. 21, no. 5, pp. 444–450, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. W. Chen, W. J. Esselman, D. B. Jump, and J. V. Busik, “Anti-inflammatory effect of docosahexaenoic acid on cytokine-induced adhesion molecule expression in human retinal vascular endothelial cells,” Investigative Ophthalmology and Visual Science, vol. 46, no. 11, pp. 4342–4347, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Erdinest, O. Shmueli, Y. Grossman, H. Ovadia, and A. Solomon, “Anti-inflammatory effects of alpha linolenic acid on human corneal epithelial cells,” Investigative Ophthalmology and Visual Science, vol. 53, no. 8, pp. 4396–4406, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Moloney, S. Toomey, E. Noone et al., “Antidiabetic effects of cis-9, trans-11-conjugated linoleic acid may be mediated via anti-inflammatory effects in white adipose tissue,” Diabetes, vol. 56, no. 3, pp. 574–582, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Ren and S. H. Chung, “Anti-inflammatory effect of α-linolenic acid and its mode of action through the inhibition of nitric oxide production and inducible nitric oxide synthase gene expression via NF-κB and mitogen-activated protein kinase pathways,” Journal of Agricultural and Food Chemistry, vol. 55, no. 13, pp. 5073–5080, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. Y.-G. Zhang, Q. Du, W.-G. Fang, M.-L. Jin, and X.-X. Tian, “Tyrphostin AG1478 supresses proliferation and invasion of human breast cancer cells,” International Journal of Oncology, vol. 33, no. 3, pp. 595–602, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. B. T. S. Susarla and M. B. Robinson, “Rottlerin, an inhibitor of protein kinase Cδ (PKCδ), inhibits astrocytic glutamate transport activity and reduces GLAST immunoreactivity by a mechanism that appears to be PKCδ-independent,” Journal of Neurochemistry, vol. 86, no. 3, pp. 635–645, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. J. V. Duncia, J. B. Santella III, C. A. Higley et al., “MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products,” Bioorganic and Medicinal Chemistry Letters, vol. 8, no. 20, pp. 2839–2844, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. B. L. Bennett, D. T. Sasaki, B. W. Murray et al., “SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 24, pp. 13681–13686, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Joshi-Barve, S. S. Barve, K. Amancherla et al., “Palmitic acid induces production of proinflammatory cytokine interleukin-8 from hepatocytes,” Hepatology, vol. 46, no. 3, pp. 823–830, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. M. Ajuwon and M. E. Spurlock, “Palmitate activates the NF-κB transcription factor and induces IL-6 and TNFα expression in 3T3-L1 adipocytes,” Journal of Nutrition, vol. 135, no. 8, pp. 1841–1846, 2005. View at Google Scholar · View at Scopus
  44. G. Zhao, T. D. Etherton, K. R. Martin et al., “Anti-inflammatory effects of polyunsaturated fatty acids in THP-1 cells,” Biochemical and Biophysical Research Communications, vol. 336, no. 3, pp. 909–917, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. R. De Caterina, W. Bernini, M. A. Carluccio, J. K. Liao, and P. Libby, “Structural requirements for inhibition of cytokine-induced endothelial activation by unsaturated fatty acids,” Journal of Lipid Research, vol. 39, no. 5, pp. 1062–1070, 1998. View at Google Scholar · View at Scopus
  46. T. M. Stulnig and M. Zeyda, “Immunomodulation by polyunsaturated fatty acids: impact on T-cell signaling,” Lipids, vol. 39, no. 12, Article ID L9554, pp. 1171–1175, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. D. W. L. Ma, J. Seo, K. C. Switzer et al., “n-3 PUFA and membrane microdomains: a new frontier in bioactive lipid research,” The Journal of Nutritional Biochemistry, vol. 15, no. 11, pp. 700–706, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. P. D. Schley, D. N. Brindley, and C. J. Field, “(n-3) PUFA alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells,” Journal of Nutrition, vol. 137, no. 3, pp. 548–553, 2007. View at Google Scholar · View at Scopus
  49. R. Wetzker and F.-D. Böhmer, “Transactivation joins multiple tracks to the ERK/MAPK cascade,” Nature Reviews Molecular Cell Biology, vol. 4, no. 8, pp. 651–657, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. C.-M. Yang, C.-S. Chien, Y.-H. Ma, L.-D. Hsiao, C.-H. Lin, and C.-B. Wu, “Bradykinin B2 receptor-mediated proliferation via activation of the Ras/Raf/MEK/MAPK pathway in rat vascular smooth muscle cells,” Journal of Biomedical Science, vol. 10, no. 2, pp. 208–218, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Adomeit, A. Graness, S. Gross, K. Seedorf, R. Wetzker, and C. Liebmann, “Bradykinin B2 receptor-mediated mitogen-activated protein kinase activation in COS-7 cells requires dual signaling via both protein kinase C pathway and epidermal growth factor receptor transactivation,” Molecular and Cellular Biology, vol. 19, no. 8, pp. 5289–5297, 1999. View at Google Scholar · View at Scopus
  52. N. Prenzel, E. Zwick, H. Daub et al., “EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF,” Nature, vol. 402, no. 6764, pp. 884–888, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Park, M. Yeo, J.-H. Jin et al., “Inhibitory activities and attenuated expressions of 5-LOX with red ginseng in Helicobacter pylori-infected gastric epithelial cells,” Digestive Diseases and Sciences, vol. 52, no. 4, pp. 973–982, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. I. O. Lee, K. H. Lee, J. H. Pyo, J. H. Kim, Y. J. Choi, and Y. C. Lee, “Anti-inflammatory effect of capsaicin in Helicobacter pylori-infected gastric epithelial cells,” Helicobacter, vol. 12, no. 5, pp. 510–517, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. J.-C. Yang, C.-T. Shun, C.-T. Chien, and T.-H. Wang, “Effective prevention and treatment of Helicobacter pylori infection using a combination of catechins and sialic acid in AGS cells and BALB/c mice,” Journal of Nutrition, vol. 138, no. 11, pp. 2084–2090, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. Y.-C. Wang and K.-M. Huang, “In vitro anti-inflammatory effect of apigenin in the Helicobacter pylori-infected gastric adenocarcinoma cells,” Food and Chemical Toxicology, vol. 53, pp. 376–383, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Koosirirat, S. Linpisarn, D. Changsom, K. Chawansuntati, and J. Wipasa, “Investigation of the anti-inflammatory effect of Curcuma longa in Helicobacter pylori-infected patients,” International Immunopharmacology, vol. 10, no. 7, pp. 815–818, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. M. M. Kamiji and R. B. De Oliveira, “Effect of vitamin C administration on gastric colonization by Helicobacter pylori,” Arquivos de Gastroenterologia, vol. 42, no. 3, pp. 167–172, 2005. View at Google Scholar · View at Scopus
  59. M. Jarosz, J. Dzieniszewski, E. Dabrowska-Ufniarz, M. Wartanowicz, S. Ziemlanski, and P. Reed I, “Effects of high dose vitamin C treatment on Helicobacter pylori infection and total vitamin C concentration in gastric juice,” European Journal of Cancer Prevention, vol. 7, no. 6, pp. 449–454, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. M. H. Gail, R. M. Pfeiffer, L. M. Brown et al., “Garlic, vitamin, and antibiotic treatment for Helicobacter pylori: a randomized factorial controlled trial,” Helicobacter, vol. 12, no. 5, pp. 575–578, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Correia, V. Michel, A. A. Matos et al., “Docosahexaenoic acid inhibits helicobacter pylori growth in vitro and mice gastric mucosa colonization,” PLoS ONE, vol. 7, no. 4, Article ID e35072, 2012. View at Publisher · View at Google Scholar · View at Scopus
  62. A. E. Duggan, J. C. Atherton, A. Cockayne et al., “Clarification of the link between polyunsaturated fatty acids and Helicobacter pylori-associated duodenal ulcer disease: a dietary intervention study,” British Journal of Nutrition, vol. 78, no. 4, pp. 515–522, 1997. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Q. Sun, C. J. O'Connor, and A. M. Roberton, “Antibacterial actions of fatty acids and monoglycerides against Helicobacter pylori,” FEMS Immunology and Medical Microbiology, vol. 36, no. 1-2, pp. 9–17, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. L. Thompson, A. Cockayne, and R. C. Spiller, “Inhibitory effect of polyunsaturated fatty acids on the growth of Helicobacter pylori: a possible explanation of the effect of diet on peptic ulceration,” Gut, vol. 35, no. 11, pp. 1557–1561, 1994. View at Google Scholar · View at Scopus