Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2016, Article ID 9303606, 12 pages
http://dx.doi.org/10.1155/2016/9303606
Research Article

Lipoxin A4 Preconditioning Attenuates Intestinal Ischemia Reperfusion Injury through Keap1/Nrf2 Pathway in a Lipoxin A4 Receptor Independent Manner

1Department of Anesthesiology, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou 510000, China
2Department of Anesthesiology, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou 510000, China
3Department of Anaesthesiology, The University of Hong Kong, Pokfulam 999077, Hong Kong
4Department of Anesthesiology, The Second Affiliated Hospital of Jinan University, Shenzhen 51000, China
5Department of Anesthesiology, Affiliated Hospital of Guangdong Medical University, Zhanjiang 524001, China

Received 1 February 2016; Revised 24 March 2016; Accepted 4 April 2016

Academic Editor: Shao-Yu Chen

Copyright © 2016 Xue Han 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. D. G. Farmer, R. S. Venick, J. Colangelo et al., “Pretransplant predictors of survival after intestinal transplantation: analysis of a single-center experience of more than 100 transplants,” Transplantation, vol. 90, no. 12, pp. 1574–1580, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Vincenti, M. Behrends, K. Dang et al., “Induction of intestinal ischemia reperfusion injury by portal vein outflow occlusion in rats,” Journal of Gastroenterology, vol. 45, no. 11, pp. 1103–1110, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. M. E. Diebel, L. N. Diebel, C. W. Manke, D. M. Liberati, and J. R. Whittaker, “Early tranexamic acid administration: a protective effect on gut barrier function following ischemia/reperfusion injury,” The Journal of Trauma and Acute Care Surgery, vol. 79, no. 6, pp. 1015–1022, 2015. View at Publisher · View at Google Scholar
  4. Y. Chen, V. C. H. Lui, N. V. Rooijen, and P. K. H. Tam, “Depletion of intestinal resident macrophages prevents ischaemia reperfusion injury in gut,” Gut, vol. 53, no. 12, pp. 1772–1780, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Martin, “Prevention of gastrointestinal complications in the critically ill patient,” AACN Advanced Critical Care, vol. 18, no. 2, pp. 158–166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. F. J. Akinrinmade, A. S. Akinrinde, O. O. Soyemi, and A. A. Oyagbemi, “Antioxidant potential of the methanol extract of Parquetina nigrescens mediates protection against intestinal ischemia-reperfusion injury in rats,” Journal of Dietary Supplements, vol. 13, no. 4, pp. 420–432, 2016. View at Publisher · View at Google Scholar
  7. O. Onal, F. Yetisir, A. E. S. Sarer et al., “Prophylactic ozone administration reduces intestinal mucosa injury induced by intestinal ischemia-reperfusion in the rat,” Mediators of Inflammation, vol. 2015, Article ID 792016, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Zhao, S. Zhou, W. Yao et al., “Propofol prevents lung injury after intestinal ischemia-reperfusion by inhibiting the interaction between mast cell activation and oxidative stress,” Life Sciences, vol. 108, no. 2, pp. 80–87, 2014. View at Publisher · View at Google Scholar · View at Scopus
  9. L. M. Aleksunes and J. E. Manautou, “Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease,” Toxicologic Pathology, vol. 35, no. 4, pp. 459–473, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Nguyen, P. Nioi, and C. B. Pickett, “The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress,” The Journal of Biological Chemistry, vol. 284, no. 20, pp. 13291–13295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ge, X. Chi, A. Zhang et al., “Intestinal NF-E2-related factor-2 expression and antioxidant activity changes in rats undergoing orthotopic liver autotransplantation,” Oncology Letters, vol. 6, no. 5, pp. 1307–1312, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. J. A. Chandrasekharan and N. Sharma-Wali, “Lipoxins: nature’s way to resolve inflammation,” Journal of Inflammation Research, vol. 8, pp. 181–192, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. P. Maderna and C. Godson, “Lipoxins: resolutionary road,” British Journal of Pharmacology, vol. 158, no. 4, pp. 947–959, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. C. F. Wenceslau, C. G. Mccarthy, T. Szasz, and R. C. Webb, “Lipoxin A4 mediates aortic contraction via rhoa/rho kinase, endothelial dysfunction and reactive oxygen species,” Journal of Vascular Research, vol. 51, no. 6, pp. 407–417, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. Wu, H. Zhai, Y. Wang et al., “Aspirin-triggered lipoxin A4 attenuates lipopolysaccharide-induced intracellular ROS in BV2 microglia cells by inhibiting the function of NADPH oxidase,” Neurochemical Research, vol. 37, no. 8, pp. 1690–1696, 2012. View at Publisher · View at Google Scholar
  16. E. Börgeson, J. Lönn, I. Bergström et al., “Lipoxin A4 inhibits Porphyromonas gingivalis-induced aggregation and reactive oxygen species production by modulating neutrophil-platelet interaction and CD11b expression,” Infection and Immunity, vol. 79, no. 4, pp. 1489–1497, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Zong, J. Li, X. Chen et al., “Lipoxin A4 attenuates cell invasion by inhibiting ROS/ERK/MMP pathway in pancreatic cancer,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 6815727, 9 pages, 2016. View at Publisher · View at Google Scholar
  18. N. Chiang, C. N. Serhan, S.-E. Dahlén et al., “The lipoxin receptor ALX: potent ligand-specific and stereoselective actions in vivo,” Pharmacological Reviews, vol. 58, no. 3, pp. 463–487, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Sobrado, M. P. Pereira, I. Ballesteros et al., “Synthesis of lipoxin A4 by 5-lipoxygenase mediates PPARgamma-dependent, neuroprotective effects of rosiglitazone in experimental stroke,” The Journal of Neuroscience, vol. 29, no. 12, pp. 3875–3884, 2009. View at Publisher · View at Google Scholar
  20. X. Chi, W. Yao, H. Xia et al., “Elevation of HO-1 expression mitigates intestinal ischemia-reperfusion injury and restores tight junction function in a rat liver transplantation model,” Oxidative Medicine and Cellular Longevity, vol. 2015, Article ID 986075, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Qiao, J. Qian, Q. Lu, Y. Tian, Q. Chen, and Y. Zhang, “Protective effects of butyrate on intestinal ischemia-reperfusion injury in rats,” The Journal of Surgical Research, vol. 197, no. 2, pp. 324–330, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. Z. Chen, Z. Wu, C. Huang et al., “Effect of lipoxin A4 on myocardial ischemia reperfusion injury following cardiac arrest in a rabbit model,” Inflammation, vol. 36, no. 2, pp. 468–475, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Gong, S. Guo, H.-B. Li, S.-Y. Yuan, Y. Shang, and S.-L. Yao, “BML-111, a lipoxin receptor agonist, protects haemorrhagic shock-induced acute lung injury in rats,” Resuscitation, vol. 83, no. 7, pp. 907–912, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Ren, N. F. Villeneuve, T. Jiang et al., “Brusatol enhances the efficacy of chemotherapy by inhibiting the Nrf2-mediated defense mechanism,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 4, pp. 1433–1438, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. C. J. Chiu, A. H. McArdle, R. Brown, H. J. Scott, and F. N. Gurd, “Intestinal mucosal lesion in low-flow states. I. A morphological, hemodynamic, and metabolic reappraisal,” Archives of Surgery, vol. 101, no. 4, pp. 478–483, 1970. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Luo, D. Yuan, W. Yao et al., “Dexmedetomidine protects against apoptosis induced by hypoxia/reoxygenation through the inhibition of gap junctions in NRK-52E cells,” Life Sciences, vol. 122, pp. 72–77, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. X.-Q. Chen, S.-H. Wu, Y. Zhou, and Y.-R. Tang, “Involvement of K+ channel-dependant pathways in lipoxin A4-induced protective effects on hypoxia/reoxygenation injury of cardiomyocytes,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 88, no. 5, pp. 391–397, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Li, W. Yao, Z. Liu et al., “Hyperglycemia abrogates ischemic postconditioning cardioprotection by impairing AdipoR1/Caveolin-3/STAT3 signaling in diabetic rats,” Diabetes, vol. 65, no. 4, pp. 942–955, 2016. View at Publisher · View at Google Scholar
  29. H. Li, W. Yao, M. G. Irwin et al., “Adiponectin ameliorates hyperglycemia-induced cardiac hypertrophy and dysfunction by concomitantly activating Nrf2 and Brg1,” Free Radical Biology & Medicine, vol. 84, pp. 311–321, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. W. Yao, G. Luo, G. Zhu et al., “Propofol activation of the Nrf2 pathway is associated with amelioration of acute lung injury in a rat liver transplantation model,” Oxidative Medicine and Cellular Longevity, vol. 2014, Article ID 258567, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. L. M. Gonzalez, A. J. Moeser, and A. T. Blikslager, “Animal models of ischemia-reperfusion-induced intestinal injury: progress and promise for translational research,” American Journal of Physiology—Gastrointestinal and Liver Physiology, vol. 308, no. 2, pp. G63–G75, 2015. View at Publisher · View at Google Scholar · View at Scopus
  32. C. Liu, C. Zhu, G. Wang, R. Xu, and Y. Zhu, “Higenamine regulates Nrf2-HO-1-Hmgb1 axis and attenuates intestinal ischemia-reperfusion injury in mice,” Inflammation Research, vol. 64, no. 6, pp. 395–403, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. G. Bannenberg, R.-L. Moussignac, K. Gronert et al., “Lipoxins and novel 15-epi-lipoxin analogs display potent anti-inflammatory actions after oral administration,” British Journal of Pharmacology, vol. 143, no. 1, pp. 43–52, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. Y.-P. Sun, E. Tjonahen, R. Keledjian et al., “Anti-inflammatory and pro-resolving properties of benzo-lipoxin A4 analogs,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 81, no. 5-6, pp. 357–366, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Wu, Y.-P. Wang, P. Guo et al., “A lipoxin A4 analog ameliorates blood-brain barrier dysfunction and reduces MMP-9 expression in a rat model of focal cerebral ischemia-reperfusion injury,” Journal of Molecular Neuroscience, vol. 46, no. 3, pp. 483–491, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. H.-B. Li, G.-Z. Wang, J. Gong et al., “BML-111 attenuates hemorrhagic shock-induced acute lung injury through inhibiting activation of mitogen-activated protein kinase pathway in rats,” The Journal of Surgical Research, vol. 183, no. 2, pp. 710–719, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Tang, L. Chen, B. Li et al., “BML-111 attenuates acute lung injury in endotoxemic mice,” The Journal of Surgical Research, vol. 200, no. 2, pp. 619–630, 2016. View at Publisher · View at Google Scholar
  38. L. Wu, H.-H. Li, Q. Wu et al., “Lipoxin A4 activates Nrf2 pathway and ameliorates cell damage in cultured cortical astrocytes exposed to oxygen-glucose deprivation/reperfusion insults,” Journal of Molecular Neuroscience, vol. 56, no. 4, pp. 848–857, 2015. View at Publisher · View at Google Scholar
  39. M. A. O'Connell and J. D. Hayes, “The Keap1/Nrf2 pathway in health and disease: from the bench to the clinic,” Biochemical Society Transactions, vol. 43, pp. 687–689, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. T. Satoh, S. R. McKercher, and S. A. Lipton, “Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs,” Free Radical Biology & Medicine, vol. 65, pp. 645–657, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. H. Hao, F. Xu, J. Hao et al., “Lipoxin A4 suppresses lipopolysaccharide-induced hela cell proliferation and migration via NF-kappaB pathway,” Inflammation, vol. 38, pp. 400–408, 2015. View at Google Scholar
  42. Q. Zhao, L. Shao, X. Hu et al., “Lipoxin A4 preconditioning and postconditioning protect myocardial ischemia/reperfusion injury in rats,” Mediators of Inflammation, vol. 2013, Article ID 231351, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. R. Wu, W. Zhou, S. Chen et al., “Lipoxin A4 suppresses the development of endometriosis in an ALX receptor-dependent manner via the p38 MAPK pathway,” British Journal of Pharmacology, vol. 171, no. 21, pp. 4927–4940, 2014. View at Publisher · View at Google Scholar · View at Scopus