Mechanisms of lung ischemia-reperfusion injury

Purpose of reviewLungs are extremely susceptible to injury, and despite advances in surgical management and immunosuppression, outcomes for lung transplantation are the worst of any solid organ transplant. The success of lung transplantation is limited by high rates of primary graft dysfunction because of ischemia-reperfusion injury characterized by robust inflammation, alveolar damage, and vascular permeability. This review will summarize major mechanisms of lung ischemia-reperfusion injury with a focus on the most recent findings in this area. Recent findingsOver the past 18 months, numerous studies have described strategies to limit lung ischemia-reperfusion injury in experimental settings, which often reveal mechanistic insight. Many of these strategies involved the use of various antioxidants, anti-inflammatory agents, mesenchymal stem cells, and ventilation with gaseous molecules. Further advancements have been achieved in understanding mechanisms of innate immune cell activation, neutrophil infiltration, endothelial barrier dysfunction, and oxidative stress responses. SummaryMethods for prevention of primary graft dysfunction after lung transplant are urgently needed, and understanding mechanisms of ischemia-reperfusion injury is critical for the development of novel and effective therapeutic approaches. In doing so, both acute and chronic outcomes of lung transplant recipients will be significantly improved.

[1]  D. Sheppard,et al.  Inhibiting Integrin αvβ5 Reduces Ischemia–Reperfusion Injury in an Orthotopic Lung Transplant Model in Mice , 2016, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[2]  S. Keshavjee,et al.  Annexin V homodimer protects against ischemia reperfusion-induced acute lung injury in lung transplantation. , 2016, The Journal of thoracic and cardiovascular surgery.

[3]  X. Cui,et al.  Inflation with carbon monoxide in rat donor lung during cold ischemia phase ameliorates graft injury , 2016, Experimental biology and medicine.

[4]  R. Vieira,et al.  Creatine supplementation attenuates pulmonary and systemic effects of lung ischemia and reperfusion injury. , 2016, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[5]  L. Turrell,et al.  δV1‐1 Reduces Pulmonary Ischemia Reperfusion‐Induced Lung Injury by Inhibiting Necrosis and Mitochondrial Localization of PKCδ and p53 , 2016, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[6]  S. Miyoshi,et al.  Early Growth Response-1 Plays an Important Role in Ischemia-Reperfusion Injury in Lung Transplants by Regulating Polymorphonuclear Neutrophil Infiltration , 2015, Transplantation.

[7]  W. Fu,et al.  Mesenchymal stem cells attenuate acute ischemia-reperfusion injury in a rat model , 2015, Experimental and therapeutic medicine.

[8]  J. Christie,et al.  Primary graft dysfunction: lessons learned about the first 72 h after lung transplantation , 2015, Current opinion in organ transplantation.

[9]  P. V. Van Schil,et al.  Longitudinal quantification of radical bursts during pulmonary ischaemia and reperfusion. , 2015, European Journal of Cardio-Thoracic Surgery.

[10]  Jun She,et al.  Bone marrow-derived mesenchymal stem cells enhance autophagy via PI3K/AKT signalling to reduce the severity of ischaemia/reperfusion-induced lung injury , 2015, Journal of cellular and molecular medicine.

[11]  C. F. Andrade,et al.  Oxidative Stress and Lung Ischemia-Reperfusion Injury , 2015, Oxidative medicine and cellular longevity.

[12]  E. Charles,et al.  Sphingosine-1-phosphate receptor 1 agonism attenuates lung ischemia-reperfusion injury. , 2015, American journal of physiology. Lung cellular and molecular physiology.

[13]  M. Mulligan,et al.  Differential toll-like receptor activation in lung ischemia reperfusion injury. , 2015, The Journal of thoracic and cardiovascular surgery.

[14]  Xiaomei Liu,et al.  Effects of sevoflurane on tight junction protein expression and PKC-α translocation after pulmonary ischemia–reperfusion injury , 2015, Experimental & Molecular Medicine.

[15]  C. Bai,et al.  Autophagy protects against ischemia/reperfusion-induced lung injury through alleviating blood-air barrier damage. , 2015, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[16]  Mark J. Miller,et al.  DAP12 Expression in Lung Macrophages Mediates Ischemia/Reperfusion Injury by Promoting Neutrophil Extravasation , 2015, The Journal of Immunology.

[17]  M. Mulligan,et al.  Role of toll-like receptor-4 in lung ischemia-reperfusion injury. , 2015, The Annals of thoracic surgery.

[18]  M. Mulligan,et al.  Functional roles of tumor necrosis factor-alpha and interleukin 1-Beta in hypoxia and reoxygenation. , 2015, The Annals of thoracic surgery.

[19]  R. Proia,et al.  Emerging biology of sphingosine-1-phosphate: its role in pathogenesis and therapy. , 2015, The Journal of clinical investigation.

[20]  J. Belperio,et al.  Neutrophil extracellular traps are pathogenic in primary graft dysfunction after lung transplantation. , 2015, American journal of respiratory and critical care medicine.

[21]  Wei Lin,et al.  Oxidant stress regulatory genetic variation in recipients and donors contributes to risk of primary graft dysfunction after lung transplantation. , 2015, The Journal of thoracic and cardiovascular surgery.

[22]  D. Kreisel,et al.  Human recombinant apyrase therapy protects against canine pulmonary ischemia-reperfusion injury. , 2015, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[23]  C. Bai,et al.  Increased lung ischemia-reperfusion injury in aquaporin 1 null mice is mediated via decreased HIF-2α stability , 2015 .

[24]  U. Francisco Lung Ischemia-Reperfusion is a Sterile Inflammatory Process Influenced by Commensal Microbiota in Mice , 2015 .

[25]  C. F. Andrade,et al.  N-acetylcysteine administration confers lung protection in different phases of lung ischaemia-reperfusion injury. , 2014, Interactive cardiovascular and thoracic surgery.

[26]  R. Vieira,et al.  Methylene blue attenuates ischemia--reperfusion injury in lung transplantation. , 2014, The Journal of surgical research.

[27]  A. Fisher,et al.  Shear stress-related mechanosignaling with lung ischemia: lessons from basic research can inform lung transplantation. , 2014, American journal of physiology. Lung cellular and molecular physiology.

[28]  Hao Wang,et al.  Infusion of Mesenchymal Stem Cells Protects Lung Transplants from Cold Ischemia-Reperfusion Injury in Mice , 2014, Lung.

[29]  T. Nagayasu,et al.  The Poly(Adenosine Diphosphate-Ribose) Polymerase Inhibitor PJ34 Reduces Pulmonary Ischemia-Reperfusion Injury in Rats , 2014, Transplantation.

[30]  K. Jones,et al.  Mast cells in a murine lung ischemia-reperfusion model of primary graft dysfunction , 2014, Respiratory Research.

[31]  R. Ploeg,et al.  The Role of Hypoxia‐Inducible Factors in Organ Donation and Transplantation: The Current Perspective and Future Opportunities , 2014, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[32]  C. Bai,et al.  Protective effects of keratinocyte growth factor-2 on ischemia-reperfusion-induced lung injury in rats. , 2014, American journal of respiratory cell and molecular biology.

[33]  Zhigang Wang,et al.  Hypoxia-inducible factor 1 alpha contributes to pulmonary vascular dysfunction in lung ischemia-reperfusion injury. , 2014, International journal of clinical and experimental pathology.

[34]  Haibo Zhang,et al.  α1-Antitrypsin inhibits ischemia reperfusion-induced lung injury by reducing inflammatory response and cell death. , 2014, The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation.

[35]  A. Sharma,et al.  Receptor for Advanced Glycation End Products (RAGE) on iNKT Cells Mediates Lung Ischemia–Reperfusion Injury , 2013, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[36]  Hui Guo,et al.  Participation of autophagy in lung ischemia-reperfusion injury in vivo. , 2013, The Journal of surgical research.

[37]  J. Debnath,et al.  Autophagy as a stress-response and quality-control mechanism: implications for cell injury and human disease. , 2013, Annual review of pathology.

[38]  D. Kreisel,et al.  Innate immunity and organ transplantation: focus on lung transplantation , 2013, Transplant international : official journal of the European Society for Organ Transplantation.

[39]  Y. Iwakura,et al.  Natural killer T cell-derived IL-17 mediates lung ischemia-reperfusion injury. , 2011, American journal of respiratory and critical care medicine.

[40]  D. Kreisel,et al.  Short- and long-term outcomes of 1000 adult lung transplant recipients at a single center. , 2011, The Journal of thoracic and cardiovascular surgery.

[41]  Grace Y Chen,et al.  Sterile inflammation: sensing and reacting to damage , 2010, Nature Reviews Immunology.

[42]  P. V. Van Schil,et al.  Lung ischemia-reperfusion injury: a molecular and clinical view on a complex pathophysiological process. , 2010, American journal of physiology. Heart and circulatory physiology.

[43]  G. Stukenborg,et al.  Adenosine A2A receptor activation on CD4+ T lymphocytes and neutrophils attenuates lung ischemia-reperfusion injury. , 2010, The Journal of thoracic and cardiovascular surgery.

[44]  D. Kreisel,et al.  Apyrase treatment prevents ischemia-reperfusion injury in rat lung isografts. , 2009, The Journal of thoracic and cardiovascular surgery.

[45]  M. Casiraghi,et al.  Novel critical role of Toll-like receptor 4 in lung ischemia-reperfusion injury and edema. , 2009, American journal of physiology. Lung cellular and molecular physiology.

[46]  I. Kron,et al.  NADPH oxidase in bone marrow-derived cells mediates pulmonary ischemia-reperfusion injury. , 2009, American journal of respiratory cell and molecular biology.

[47]  Yoshiro Kobayashi The role of chemokines in neutrophil biology. , 2008, Frontiers in bioscience : a journal and virtual library.

[48]  D. Sheppard,et al.  Integrin αvβ5 Regulates Lung Vascular Permeability and Pulmonary Endothelial Barrier Function , 2007 .

[49]  D. Sheppard,et al.  Integrin alphavbeta5 regulates lung vascular permeability and pulmonary endothelial barrier function. , 2007, American journal of respiratory cell and molecular biology.

[50]  A. Zarbock,et al.  Alveolar macrophage activation is a key initiation signal for acute lung ischemia-reperfusion injury. , 2006, American journal of physiology. Lung cellular and molecular physiology.

[51]  David R. Jones,et al.  Ischemia-reperfusion injury after lung transplantation increases risk of late bronchiolitis obliterans syndrome. , 2002, The Annals of thoracic surgery.

[52]  J. T. Cope,et al.  Lung transplant reperfusion injury involves pulmonary macrophages and circulating leukocytes in a biphasic response. , 2001, The Journal of thoracic and cardiovascular surgery.

[53]  C. Valeri,et al.  Pathophysiology of ischaemia reperfusion injury: Central role of the neutrophil , 1991, The British journal of surgery.