Protective Effect of Intestinal Ischemic Preconditioning on Ischemia Reperfusion-Caused Lung Injury in Rats
- 299 Downloads
- 10 Citations
Abstract
Intestinal ischemia reperfusion (IR) causes injury of distant critical organs. Remote intestinal ischemic preconditioning (IP) may confer the cytoprotection in critical organs including lung. The authors hypothesized that intestinal IP would be a prophylactic factor in the prevention of distant lung injury induced by IR. Rats were randomly divided into IR, IP, and Sham (S) group. Compared with IR group in the serum and lung tissue, MPO, MDA, TNF-α, and IL-1 levels were significantly decreased in the IP group. Following the same pattern, NO level in the serum and lung tissue was significantly increased in the IP group. And intestinal IP markedly abolished lung injury scores in contrast to IR group. Moreover, intestinal IP significantly attenuated caspase-3 expression, leading to the low expression of Bax and the high expression of Bcl-2. The present study showed that intestinal IP ameliorates the capacity of anti-oxygen free radical, inhibits the release of pro-inflammatory cytokines and alleviates apoptosis in IR-induced lung injury in rats. Intestinal IP may provide a novel prophylactic strategy for treatment of IR-induced lung injury.
KEY WORDS
ischemic preconditioning ischemia reperfusion lung injury apoptosisNotes
Acknowledgments
This study was supported by the Fundamental Research Funds for the Central Universities (2013JDHZ08) and Specialized Research Fund of the Second Affiliated Hospital of Xi’an Jiaotong University School of Medicine of China, No. RC (XM) 201103.
Conflict of Interests
The authors have declared that no competing interests exist.
References
- 1.Liu, K.X., Y.S. Li, W.Q. Huang, C. Li, J.X. Liu, and Y. Li. 2009. Immediate but not delayed postconditioning during reperfusion attenuates acute lung injury induced by intestinal ischemia/reperfusion in rats: comparison with ischemic preconditioning. Journal of Surgical Research 157: e55–e62.CrossRefPubMedGoogle Scholar
- 2.Dwivedi, A.J., R. Wu, E. Nguyen, S. Higuchi, H. Wang, K. Krishnasastry, C.P. Marini, T.S. Ravikumar, and P. Wang. 2007. Adrenomedullin and adrenomedullin binding protein-1 prevent acute lung injury after gut ischemia-reperfusion. Journal of the American College of Surgeons 205: 284–293.CrossRefPubMedGoogle Scholar
- 3.Sorkine, P., O. Szold, P. Halpern, M. Gutman, M. Greemland, V. Rudick, and G. Goldman. 1997. Gut decontamination reduces bowel ischemia-induced lung injury in rats. Chest 112: 491–495.CrossRefPubMedGoogle Scholar
- 4.Ware, L.B., and M.A. Matthay. 2000. The acute respiratory distress syndrome. New England Journal of Medicine 342: 1334.CrossRefPubMedGoogle Scholar
- 5.Guzel, A., M. Kanter, A. Guzel, A. Pergel, and M. Erboga. 2012. Anti-inflammatory and antioxidant effects of infliximab on acute lung injury in a rat model of intestinal ischemia/reperfusion. Journal of Molecular Histology 43: 361–369.CrossRefPubMedGoogle Scholar
- 6.Ito, K., H. Ozasa, and S. Horikawa. 2005. Edaravone protects against lung injury induced by intestinal ischemia/reperfusion in rat. Free Radical Biology Medicine 38: 369–374.CrossRefPubMedGoogle Scholar
- 7.Sun, Q., Q.T. Meng, Y. Jiang, H.M. Liu, S.Q. Lei, W.T. Su, W.N. Duan, Y. Wu, and Z.Y. Xia. 2013. Protective effect of ginsenoside Rb1 against intestinal ischemia-reperfusion induced acute renal injury in mice. PloS One 8: e80859.CrossRefPubMedCentralPubMedGoogle Scholar
- 8.Shen, M., R.X. Wu, L. Zhao, J. Li, H.T. Guo, R. Fan, Y. Cui, Y.M. Wang, S.Q. Yue, and J.M. Pei. 2012. Resveratrol attenuates ischemia/reperfusion injury in neonatal cardiomyocytes and its underlying mechanism. PloS One 7: e51223.CrossRefPubMedCentralPubMedGoogle Scholar
- 9.Zhang, T., Y. Wang, R. Ban, L. Tong, H. Qiao, H. Lao, H. Zhao, X. Jiang, X. Sun, and F. Zhang. 2012. Oral administration of lactoferrin attenuates intestinal ischemia-reperfusion injury in rats. European Surgical Research 49: 99–106.CrossRefPubMedGoogle Scholar
- 10.Caty, M.G., K.S. Guice, K.T. Oldham, D.G. Remick, and S.I. Kunkel. 1990. Evidence for tumor necrosis factor-induced pulmonary microvascular injury after intestinal ischemia-reperfusion injury. Annals of Surgery 212: 694–700.CrossRefPubMedCentralPubMedGoogle Scholar
- 11.Cámara-Lemarroy, C.R., F.J. Guzmán-de la Garza, P. Cordero-Pérez, G. Alarcón-Galván, J.M. Ibarra-Hernández, L.E. Muñoz-Espinosa, and N.E. Fernández-Garza. 2013. Bupropion reduces the inflammatory response and intestinal injury due to ischemia-reperfusion. Transplantation Proceedings 45: 2502–2505.CrossRefPubMedGoogle Scholar
- 12.Taha, M.O., R. Miranda-Ferreira, A.C. Chang, A.M. Rodrigues, I.S. Fonseca, L.B. Toral, M.R. Cardoso, M.J. Simões, I.S. Oliveira-Junior, H.P. Monteiro, D.J. Fagundes, N.S. Taha, and A. Caricati-Neto. 2012. Effect of ischemic preconditioning on injuries caused by ischemia and reperfusion in rat intestine. Transplantation Proceedings 44: 2304–2308.CrossRefPubMedGoogle Scholar
- 13.Li, C., Y.S. Li, M. Xu, S.H. Wen, X. Yao, Y. Wu, C.Y. Huang, W.Q. Huang, and K.X. Liu. 2013. Limb remote ischemic preconditioning for intestinal and pulmonary protection during elective open infrarenal abdominal aortic aneurysm repair: a randomized controlled trial. Anesthesiology 118: 842–852.CrossRefPubMedGoogle Scholar
- 14.Camara-Lemarroy, C.R. 2014. Remote ischemic preconditioning as treatment for non-ischemic gastrointestinal disorders: beyond ischemia-reperfusion injury. World Journal of Gastroenterology 20: 3572–3581.CrossRefPubMedCentralPubMedGoogle Scholar
- 15.Kanoria, S., R. Jalan, N.A. Davies, A.M. Seifalian, R. Williams, and B.R. Davidson. 2006. Remote ischaemic preconditioning of the hind limb reduces experimental liver warm ischaemia-reperfusion injury. British Journal of Surgery 93: 762–768.CrossRefPubMedGoogle Scholar
- 16.Song, T., Y.F. Peng, S.Y. Guo, Y.H. Liu, and L.Y. Liul. 2007. Brief small intestinal ischemia lessens renal ischemia-reperfusion injury in rats. Comparative Medicine 57: 200–205.PubMedGoogle Scholar
- 17.Holzner, P.A., B. Kulemann, S. Kuesters, S. Timme, J. Hoeppner, U.T. Hopt, and G. Marjanovic. 2011. Impact of remote ischemic preconditioning on wound healing in small bowel anastomoses. World Journal of Gastroenterology 17: 1308–1316.CrossRefPubMedCentralPubMedGoogle Scholar
- 18.Hotter, G., D. Closa, M. Prados, L. Fernández-Cruz, N. Prats, E. Gelpí, and J. Roselló-Catafau. 1996. Intestinal preconditioning is mediated by a transient increase in nitric oxide. Biochemical and Biophysical Research Communications 222: 27–32.CrossRefPubMedGoogle Scholar
- 19.Liu, K.X., C. Li, Y.S. Li, B.L. Yuan, M. Xu, Z. Xia, and W.Q. Huang. 2010. Proteomic analysis of intestinal ischemia/reperfusion injury and ischemic preconditioning in rats reveals the protective role of aldose reductase. Proteomics 10: 4463–4475.CrossRefPubMedGoogle Scholar
- 20.Moore-Olufemi, S.D., S.E. Olufemi, S. Lott, N. Sato, R.A. Kozar, F.A. Moore, R.S. Radhakrishnan, S. Shah, F. Jimenez, B.C. Kone, and C.S. Cox Jr. 2010. Intestinal ischemic preconditioning after ischemia/reperfusion injury in rat intestine: profiling global gene expression patterns. Digestive Disease and Science 55: 1866–1877.CrossRefGoogle Scholar
- 21.Flessas, I.I., A.E. Papalois, K. Toutouzas, F. Zagouri, and G.C. Zografos. 2011. Effects of lazaroids on intestinal ischemia and reperfusion injury in experimental models. Journal of Surgical Research 166: 265–274.CrossRefPubMedGoogle Scholar
- 22.Lee, C.H., C.C. Hsiao, C.Y. Hung, Y.J. Chang, and H.C. Lo. 2012. Long-term enteral arginine supplementation in rats with intestinal ischemia and reperfusion. Journal of Surgical Research 175: 67–75.CrossRefPubMedGoogle Scholar
- 23.Kostopanagiotou, G., E.D. Avgerinos, E. Markidou, P.C. Voiniadis, K. Chondros, V. Smyrniotis Theodoraki, and N. Arkadopoulos. 2011. Protective effect of NAC preconditioning against ischemia- reperfusion injury in piglet small bowel transplantation: effects on plasma TNF, IL-8, hyaluronic acid, and NO. Journal of Surgical Research 168: 301–305.CrossRefPubMedGoogle Scholar
- 24.Moore-Olufemi, S.D., R.A. Kozar, F.A. Moore, N. Sato, H.T. Hassoun, C.S. Cox Jr., and B.C. Kone. 2005. Ischemic preconditioning protects against gut dysfunction and mucosal injury after ischemia/reperfusion injury. Shock 23: 258–263.PubMedGoogle Scholar
- 25.Sayan, H., V.H. Ozacmak, F. Sen, M. Cabuk, D.Y. Atik, A.A. Igdem, and I.D. Ozacmak. 2009. Pharmacological preconditioning with erythropoietin reduces ischemia-reperfusion injury in the small intestine of rats. Life Science 84: 364–371.CrossRefGoogle Scholar
- 26.Sukhotnik, I., N. Slijper, Y. Pollak, E. Chemodanov, R. Shaoul, A.G. Coran, and J.G. Mogilner. 2011. Parenteral omega-3 fatty acids (Omegaven) modulate intestinal recovery after intestinal ischemia-reperfusion in a rat model. Journal Of Pediatric Surgery 46: 1353–1360.CrossRefPubMedGoogle Scholar
- 27.Zhao, C., J. Sun, C. Fang, and F. Tang. 2014. 1,8-cineol attenuates LPS-induced acute pulmonary inflammation in mice. Inflammation 37: 566–572.CrossRefPubMedGoogle Scholar
- 28.Chen, L., L. Zhao, C. Zhang, and Z. Lan. 2014. Protective effect of p-cymene on lipopolysaccharide-induced acute lung injury in mice. Inflammation 37: 358–364.CrossRefPubMedGoogle Scholar
- 29.An, S., Y. Hishikawa, J. Liu, and T. Koji. 2007. Lung injury after ischemia-reperfusion of small intestine in rats involves apoptosis of type II alveolar epithelial cells mediated by TNF-alpha and activation of Bid pathway. Apoptosis 12: 1989–2001.CrossRefPubMedGoogle Scholar
- 30.Guo, Q., J. Jin, J.X. Yuan, A. Zeifman, J. Chen, B. Shen, and J. Huang. 2011. VEGF, Bcl-2 and Bad regulated by angiopoietin-1 in oleic acid induced acute lung injury. Biochemical and Biophysical Research Communications 413: 630–636.CrossRefPubMedGoogle Scholar
- 31.Avgerinos, E.D., G. Kostopanagiotou, C. Costopanagiotou, N. Kopanakis, I. Andreadou, M. Lekka, G. Nakos, and V. Smyrniotis. 2010. Intestinal preconditioning ameliorates ischemia-reperfusion induced acute lung injury in rats: an experimental study. Journal of Surgical Research 160: 294–301.CrossRefPubMedGoogle Scholar
- 32.Chen, W., X.B. Fu, S.L. Ge, T.Z. Sun, G. Zhou, B. Han, Y.R. Du, H.H. Li, and Z.Y. Sheng. 2005. Intravenous acid fibroblast growth factor protects intestinal mucosal cells against ischemia-reperfusion injury via regulating Bcl-2/Bax expression. World Journal of Gastroenterology 11: 3419–3425.CrossRefPubMedCentralPubMedGoogle Scholar
- 33.An, S., Y. Hishikawa, and T. Koji. 2005. Induction of cell death in rat small intestine by ischemia reperfusion: differential roles of Fas/Fas ligand and Bcl-2/Bax systems depending upon cell types. Histochemistry and Cell Biology 123: 249–261.CrossRefPubMedGoogle Scholar
- 34.Bratton, S.B., M. MacFarlane, K. Cain, and G.M. Cohen. 2000. Protein complexes activate distinct caspase cascades in death receptor and stress-induced apoptosis. Experimental Cell Research 256: 27–33.CrossRefPubMedGoogle Scholar
- 35.Xiao, F., W. Gao, X. Wang, and T. Chen. 2012. Amplification activation loop between caspase-8 and -9 dominates artemisinin-induced apoptosis of ASTC-a-1 cells. Apoptosis 17: 600–611.CrossRefPubMedGoogle Scholar
- 36.Qu, T., B. Huang, L. Zhang, L. Li, F. Xu, W. Huang, C. Li, Y. Du, and G. Zhang. 2014. Identification and functional characterization of Two executioner caspases in Crassostrea gigas. PloS One 9: e89040.CrossRefPubMedCentralPubMedGoogle Scholar