Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016 (2016), Article ID 5843672, 13 pages
http://dx.doi.org/10.1155/2016/5843672
Research Article

Morin Attenuates Ovalbumin-Induced Airway Inflammation by Modulating Oxidative Stress-Responsive MAPK Signaling

Department of Respiratory Medicine, The First Affiliated Hospital of Nanjing Medical University, 300 Guangzhou Road, Nanjing, Jiangsu 210029, China

Received 17 July 2015; Revised 12 September 2015; Accepted 13 September 2015

Academic Editor: Adam J. Case

Copyright © 2016 Yuan Ma 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. C. Anandan, U. Nurmatov, O. C. P. van Schayck, and A. Sheikh, “Is the prevalence of asthma declining? Systematic review of epidemiological studies,” Allergy, vol. 65, no. 2, pp. 152–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. W.-J. Zha, Y. Qian, Y. Shen et al., “Galangin abrogates ovalbumin-induced airway inflammation via negative regulation of NF-κB,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 767689, 14 pages, 2013. View at Publisher · View at Google Scholar
  3. L.-P. Boulet, J. M. FitzGerald, M. L. Levy et al., “A guide to the translation of the Global Initiative for Asthma (GINA) strategy into improved care,” European Respiratory Journal, vol. 39, no. 5, pp. 1220–1229, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. S. T. Holgate, “Asthma: a simple concept but in reality a complex disease,” European Journal of Clinical Investigation, vol. 41, no. 12, pp. 1339–1352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. B. N. Lambrecht and H. Hammad, “Asthma: the importance of dysregulated barrier immunity,” European Journal of Immunology, vol. 43, no. 12, pp. 3125–3137, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. J. A. Hirota and D. A. Knight, “Human airway epithelial cell innate immunity: relevance to asthma,” Current Opinion in Immunology, vol. 24, no. 6, pp. 740–746, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. J.-L. Malo, J. L'Archevêque, Z. Lummus, and D. Bernstein, “Changes in specific IgE and IgG and monocyte chemoattractant protein-1 in workers with occupational asthma caused by diisocyanates and removed from exposure,” Journal of Allergy and Clinical Immunology, vol. 118, no. 2, pp. 530–533, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. T. Tanabe, T. Shimokawaji, S. Kanoh, and B. K. Rubin, “IL-33 stimulates CXCL8/IL-8 secretion in goblet cells but not normally differentiated airway cells,” Clinical and Experimental Allergy, vol. 44, no. 4, pp. 540–552, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Mukhopadhyay, P. Malik, S. K. Arora, and T. K. Mukherjee, “Intercellular adhesion molecule-1 as a drug target in asthma and rhinitis,” Respirology, vol. 19, no. 4, pp. 508–513, 2014. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Wang, C. Bai, K. Li, K. B. Adler, and X. Wang, “Role of airway epithelial cells in development of asthma and allergic rhinitis,” Respiratory Medicine, vol. 102, no. 7, pp. 949–955, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Orihara and A. Matsuda, “Pathophysiological roles of microvascular alterations in pulmonary inflammatory diseases: possible implications of tumor necrosis factor-alpha and CXC chemokines,” International Journal of Chronic Obstructive Pulmonary Disease, vol. 3, no. 4, pp. 619–627, 2008. View at Google Scholar · View at Scopus
  12. D. Lykouras, F. Sampsonas, A. Kaparianos, K. Karkoulias, and K. Spiropoulos, “Role and pharmacogenomics of TNF-α in asthma,” Mini-Reviews in Medicinal Chemistry, vol. 8, no. 9, pp. 934–942, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Desai and C. Brightling, “Tnf-alpha antagonism in severe asthma?” Recent Patents on Inflammation and Allergy Drug Discovery, vol. 4, no. 3, pp. 193–200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. J.-Y. Kim, J.-H. Sohn, J.-M. Choi et al., “Alveolar macrophages play a key role in cockroach-induced allergic inflammation via TNF-α pathway,” PLoS ONE, vol. 7, no. 10, Article ID e47971, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. D. Laveti, M. Kumar, R. Hemalatha et al., “Anti-inflammatory treatments for chronic diseases: a review,” Inflammation & Allergy-Drug Targets, vol. 12, no. 5, pp. 349–361, 2013. View at Publisher · View at Google Scholar
  16. H. S. Lee, K.-H. Jung, S.-W. Hong et al., “Morin protects acute liver damage by carbon tetrachloride (CCl4) in rat,” Archives of Pharmacal Research, vol. 31, no. 9, pp. 1160–1165, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. V. Sivaramakrishnan and S. N. Devaraj, “Morin regulates the expression of NF-κB-p65, COX-2 and matrix metalloproteinases in diethylnitrosamine induced rat hepatocellular carcinoma,” Chemico-Biological Interactions, vol. 180, no. 3, pp. 353–359, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Kapoor and P. Kakkar, “Protective role of morin, a flavonoid, against high glucose induced oxidative stress mediated apoptosis in primary rat hepatocytes,” PLoS ONE, vol. 7, no. 8, Article ID e41663, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Kumar, T. Ahmad, A. Sharma et al., “Let-7 microRNA-mediated regulation of IL-13 and allergic airway inflammation,” Journal of Allergy and Clinical Immunology, vol. 128, no. 5, pp. 1077–1085.e10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. G. Gloire, S. Legrand-Poels, and J. Piette, “NF-κB activation by reactive oxygen species: fifteen years later,” Biochemical Pharmacology, vol. 72, no. 11, pp. 1493–1505, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Bibi, V. Vinokur, D. Waisman et al., “Zn/Ga-DFO iron-chelating complex attenuates the inflammatory process in a mouse model of asthma,” Redox Biology, vol. 2, pp. 814–819, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Konno, H. Yamakawa, H. Utsunomiya, K. Ito, S. Sato, and A. Yajima, “Expression of survivin and Bcl-2 in the normal human endometrium,” Molecular Human Reproduction, vol. 6, no. 6, pp. 529–534, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. C.-D. Lu, D. C. Altieri, and N. Tanigawa, “Expression of a novel antiapoptosis gene, survivin, correlated with tumor cell apoptosis and p53 accumulation in gastric carcinomas,” Cancer Research, vol. 58, no. 9, pp. 1808–1812, 1998. View at Google Scholar · View at Scopus
  24. I.-T. Lee and C.-M. Yang, “Role of NADPH oxidase/ROS in pro-inflammatory mediators-induced airway and pulmonary diseases,” Biochemical Pharmacology, vol. 84, no. 5, pp. 581–590, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Baregamian, J. Song, C. E. Bailey, J. Papaconstantinou, B. M. Evers, and D. H. Chung, “Tumor necrosis factor-α and apoptosis signal-regulating kinase 1 control reactive oxygen species release, mitochondrial autophagy and c-Jun N-terminal kinase/p38 phosphorylation during necrotizing enterocolitis,” Oxidative Medicine and Cellular Longevity, vol. 2, no. 5, pp. 297–306, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. J. T. Olin and M. E. Wechsler, “Asthma: pathogenesis and novel drugs for treatment,” The British Medical Journal, vol. 349, Article ID g5517, 2014. View at Publisher · View at Google Scholar
  27. H. McClafferty, “An overview of integrative therapies in asthma treatment,” Current Allergy and Asthma Reports, vol. 14, no. 10, p. 464, 2014. View at Publisher · View at Google Scholar · View at Scopus
  28. M. del Carmen Vennera and C. Picado, “Novel diagnostic approaches and biological therapeutics for intrinsic asthma,” International Journal of General Medicine, vol. 8, no. 7, pp. 365–371, 2014. View at Publisher · View at Google Scholar · View at Scopus
  29. W. W. Busse and R. F. Lemanske Jr., “Asthma,” The New England Journal of Medicine, vol. 344, no. 5, pp. 350–362, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. C. H. Fanta, “Asthma,” The New England Journal of Medicine, vol. 360, no. 10, pp. 1002–1014, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Page-McCaw, A. J. Ewald, and Z. Werb, “Matrix metalloproteinases and the regulation of tissue remodelling,” Nature Reviews Molecular Cell Biology, vol. 8, no. 3, pp. 221–233, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. K. J. Greenlee, Z. Werb, and F. Kheradmand, “Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted,” Physiological Reviews, vol. 87, no. 1, pp. 69–98, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. G. V. Halade, Y.-F. Jin, and M. L. Lindsey, “Matrix metalloproteinase (MMP)-9: a proximal biomarker for cardiac remodeling and a distal biomarker for inflammation,” Pharmacology and Therapeutics, vol. 139, no. 1, pp. 32–40, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. N. Liu, W. J. Zha, Y. Ma et al., “Galangin attenuates airway remodelling by inhibiting TGF-β1-mediated ROS generation and MAPK/Akt phosphorylation in asthma,” Scientific Reports, vol. 9, no. 5, Article ID 11758, 2015. View at Publisher · View at Google Scholar
  35. J. Swierkot, K. Bogunia-Kubik, B. Nowak et al., “Analysis of associations between polymorphisms within genes coding for tumour necrosis factor (TNF)-alpha and TNF receptors and responsiveness to TNF-alpha blockers in patients with rheumatoid arthritis,” Joint Bone Spine, vol. 82, no. 2, pp. 94–99, 2015. View at Publisher · View at Google Scholar
  36. J. C. Peng, J. Shen, and Z. H. Ran, “Novel agents in the future: therapy beyond anti-TNF agents in inflammatory bowel disease,” Journal of Digestive Diseases, vol. 15, no. 11, pp. 585–590, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Sato, M. Takaishi, S. Tokuoka, and S. Sano, “Involvement of TNF-α converting enzyme in the development of psoriasis-like lesions in a mouse model,” PLoS ONE, vol. 9, no. 11, Article ID e112408, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Ji, I. von Schéele, J. Bergström et al., “Compartment differences of inflammatory activity in chronic obstructive pulmonary disease,” Respiratory Research, vol. 15, no. 1, article 104, 2014. View at Publisher · View at Google Scholar
  39. G. Rajashekhar, M. Shivanna, U. B. Kompella, Y. Wang, and S. P. Srinivas, “Role of MMP-9 in the breakdown of barrier integrity of the corneal endothelium in response to TNF-α,” Experimental Eye Research, vol. 122, no. 5, pp. 77–85, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Yabluchanskiy, Y. Ma, R. P. Iyer, M. E. Hall, and M. L. Lindsey, “Matrix metalloproteinase-9: many shades of function in cardiovascular disease,” Physiology, vol. 28, no. 6, pp. 391–403, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. C. Miraglia, R. Scian, C. G. Samartino et al., “Brucella abortus induces TNF-α-dependent astroglial MMP-9 secretion through mitogen-activated protein kinases,” Journal of Neuroinflammation, vol. 10, article 47, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. S.-J. Suh, C.-H. Kwak, T.-W. Chung et al., “Pimaric acid from Aralia cordata has an inhibitory effect on TNF-α-induced MMP-9 production and HASMC migration via down-regulated NF-κB and AP-1,” Chemico-Biological Interactions, vol. 199, no. 2, pp. 112–119, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Pawliczak, “The role of radical oxygen species in airway inflammation,” Polski Merkuriusz Lekarski, vol. 14, no. 84, pp. 493–496, 2003. View at Google Scholar · View at Scopus
  44. L. Zuo, N. P. Otenbaker, B. A. Rose, and K. S. Salisbury, “Molecular mechanisms of reactive oxygen species-related pulmonary inflammation and asthma,” Molecular Immunology, vol. 56, no. 1-2, pp. 57–63, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Dröge, “Free radicals in the physiological control of cell function,” Physiological Reviews, vol. 82, no. 1, pp. 47–95, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Sakon, X. Xue, M. Takekawa et al., “NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death,” The EMBO Journal, vol. 22, no. 15, pp. 3898–3909, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Kamata, S.-I. Honda, S. Maeda, L. Chang, H. Hirata, and M. Karin, “Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases,” Cell, vol. 120, no. 5, pp. 649–661, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Zhang and X. Li, “Lipopolysaccharide-regulated production of bone sialoprotein and interleukin-8 in human periodontal ligament fibroblasts: the role of toll-like receptors 2 and 4 and the MAPK pathway,” Journal of Periodontal Research, vol. 50, no. 2, pp. 141–151, 2015. View at Publisher · View at Google Scholar
  49. I.-T. Lee, R.-H. Shih, C.-C. Lin, J.-T. Chen, and C.-M. Yang, “Role of TLR4/NADPH oxidase/ROS-activated p38 MAPK in VCAM-1 expression induced by lipopolysaccharide in human renal mesangial cells,” Cell Communication and Signaling, vol. 10, article 33, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. K.-B. Roh, E. Jung, D. Park, and J. Lee, “Fumaric acid attenuates the eotaxin-1 expression in TNF-α-stimulated fibroblasts by suppressing p38 MAPK-dependent NF-κB signaling,” Food and Chemical Toxicology, vol. 58, no. 1, pp. 423–431, 2013. View at Publisher · View at Google Scholar · View at Scopus
  51. J. K. Patel, R. L. Clifford, K. Deacon, and A. J. Knox, “Ciclesonide inhibits TNFα- and IL-1β-induced monocyte chemotactic protein-1 (MCP-1/CCL2) secretion from human airway smooth muscle cells,” American Journal of Physiology: Lung Cellular and Molecular Physiology, vol. 302, no. 8, pp. L785–L792, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Hollander, B. Sitkauskiene, R. Sakalauskas, U. Westin, and S. M. Janciauskiene, “Serum and bronchial lavage fluid concentrations of IL-8, SLPI, sCD14 and sICAM-1 in patients with COPD and asthma,” Respiratory Medicine, vol. 101, no. 9, pp. 1947–1953, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. K. S. Lee, S. M. Jin, H. J. Kim, and Y. C. Lee, “Matrix metalloproteinase inhibitor regulates inflammatory cell migration by reducing ICAM-1 and VCAM-1 expression in a murine model of toluene diisocyanate-induced asthma,” The Journal of Allergy and Clinical Immunology, vol. 111, no. 6, pp. 1278–1284, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. I. Rahman and W. MacNee, “Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches,” Free Radical Biology and Medicine, vol. 28, no. 9, pp. 1405–1420, 2000. View at Publisher · View at Google Scholar · View at Scopus
  55. R. F. Schwabe and D. A. Brenner, “Mechanisms of liver injury. I. TNF-α-induced liver injury: role of IKK, JNK, and ROS pathways,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 290, no. 4, pp. G583–G589, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. I. Rahman, B. Mulier, P. S. Gilmour et al., “Oxidant-mediated lung epithelial cell tolerance: the role of intracellular glutathione and nuclear factor-kappaB,” Biochemical Pharmacology, vol. 62, no. 6, pp. 787–794, 2001. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Zafarullah, W. Q. Li, J. Sylvester, and M. Ahmad, “Molecular mechanisms of N-acetylcysteine actions,” Cellular and Molecular Life Sciences, vol. 60, no. 1, pp. 6–20, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Kano, M. Almanan, B. S. Bochner, and N. Zimmermann, “Mechanism of Siglec-8-mediated cell death in IL-5-activated eosinophils: role for reactive oxygen species-enhanced MEK/ERK activation,” Journal of Allergy and Clinical Immunology, vol. 132, no. 2, pp. 437–445, 2013. View at Publisher · View at Google Scholar · View at Scopus
  59. C. G. Pham, S. Papa, C. Bubici, F. Zazzeroni, and G. Franzoso, “Oxygen JNKies: phosphatases overdose on ROS,” Developmental Cell, vol. 8, no. 4, pp. 452–454, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Sano, K. Fukuda, T. Sato et al., “ERK and p38 MAPK, but not NF-κB, are critically involved in reactive oxygen species-mediated induction of IL-6 by angiotensin II in cardiac fibroblasts,” Circulation Research, vol. 89, no. 8, pp. 661–669, 2001. View at Publisher · View at Google Scholar · View at Scopus
  61. E. Youl, R. Magous, G. Cros, and C. Oiry, “MAP Kinase cross talks in oxidative stress-induced impairment of insulin secretion. Involvement in the protective activity of quercetin,” Fundamental and Clinical Pharmacology, vol. 28, no. 6, pp. 608–615, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. I.-T. Lee, S.-F. Luo, C.-W. Lee et al., “Overexpression of HO-1 protects against TNF-α-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress,” The American Journal of Pathology, vol. 175, no. 2, pp. 519–532, 2009. View at Publisher · View at Google Scholar · View at Scopus