Erythropoietin Reduces Acute Lung Injury and Multiple Organ Failure/Dysfunction Associated to a Scald-Burn Inflammatory Injury in the Rat

Inflammation

Volumn 38, Issue 1, 2015, Pages 312-326

  Rocha, Joao ^a   Eduardo Figueira, Maria ^a   Barateiro, Andreia ^a   Fernandes, Adelaide ^a   Brites, Dora ^a   Pinto, Rui ^a   Freitas, Marisa ^b   Fernandes, Eduarda ^b   Mota Filipe, Helder ^a   Sepodes, Bruno ^a  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

acute lung injury; burn; erythropoietin; inflammation; multiple organ dysfunction

Indexed keywords

ALBUMIN; CASPASE 3; CYTOPROTECTIVE AGENT; DRUG THERAPY; GELATINASE B; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; PHARMACOLOGY; PROTEIN KINASE B; RECOMBINANT ERYTHROPOIETIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ACUTE LUNG INJURY; ALBUMIN BLOOD LEVEL; ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BURNS; CELL PROTECTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG EFFECTS; DRUG THERAPY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INFLAMMATION; KIDNEY FAILURE; LIVER FAILURE; LUNG INSUFFICIENCY; LUNG LAVAGE; MALE; METABOLISM; MULTIPLE ORGAN FAILURE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOLOGY; PHYSIOLOGY; POLYMORPHONUCLEAR CELL; PROTEIN BLOOD LEVEL; RAT; RESPIRATORY BURST; SCALD; THERMAL INJURY; WISTAR RAT;

ACUTE LUNG INJURY; ANIMALS; BURNS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EFFECTS; DRUG THERAPY; EPOETIN ALFA; HUMANS; INFLAMMATION; MALE; METABOLISM; MULTIPLE ORGAN FAILURE; NEUTROPHILS; PATHOLOGY; PHARMACOLOGY; PHYSIOLOGY; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; RESPIRATORY BURST; THERAPEUTIC USE;

RATTUS;

EID: 84964211290     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-014-0035-7     Document Type: Article

References (64)

1. Dahiya, P. 2009. Burns as a model of SIRS. Frontiers in Bioscience 1(14): 4962–4967.
2. Dancey, D.R., J. Hayes, M. Gomez, D. Schouten, J. Fish, W. Peters, A.S. Slutsky, and T.E. Stewart. 1999. ARDS in patients with thermal injury. Intensive Care Medicine 25(11): 1231–1236.
3. Herridge, M.S., A.M. Cheung, C.M. Tansey, A. Matte-Martyn, N. Diaz-Granados, F. Al-Saidi, A.B. Cooper, C.B. Guest, C.D. Mazer, S. Mehta, T.E. Stewart, A. Barr, D. Cook, A.S. Slutsky, and Canadian Critical Care Trials Group. 2003. One-year outcomes in survivors of the acute respiratory distress syndrome. New England Journal of Medicine 348(8): 683–693.
4. Rodriguez, J.L., C.G. Miller, W.L. Garner, G.O. Till, P. Guerrero, N.P. Moore, M. Corridore, D.P. Normolle, D.J. Smith, and D.G. Remick. 1993. Correlation of the local and systemic cytokine response with clinical outcome following thermal injury. The Journal of Trauma 34(5): 684–694.
5. Ipaktchi, K., A. Mattar, A.D. Niederbichler, L.M. Hoesel, S. Vollmannshauser, M.R. Hemmila, G.L. Su, D.G. Remick, S.C. Wang, and S. Arbabi. 2006. Attenuating burn wound inflammatory signaling reduces systemic inflammation and acute lung injury. The Journal of Immunology 177(11): 8065–8071.
6. Edens, H.A., and C.A. Parkos. 2003. Neutrophil transendothelial migration and alteration in vascular permeability: focus on neutrophil-derived azurocidin. Current Opinion in Hematology 10(1): 25–30.
7. Fry, D.E. 2012. Sepsis, systemic inflammatory response, and multiple organ dysfunction: the mystery continues. The American Journal of Surgery 78(1): 1–8.
8. Helm, R.E., J.P. Gold, T.K. Rosengart, J.A. Zelano, O.W. Isom, and K.H. Krieger. 1993. Erythropoietin in cardiac surgery. Journal of Cardiac Surgery 8(5): 579–606.
9. Broxmeyer, H.E. 2013. Erythropoietin: multiple targets, actions, and modifying influences for biological and clinical consideration. The Journal of Experimental Medicine 210(2): 205–208.
10. Nairz, M., T. Sonnweber, A. Schroll, I. Theurl, and G. Weiss. 2012. The pleiotropic effects of erythropoietin in infection and inflammation. Microbes and Infection 14(3): 238–246.
11. Maiese, K., Z.Z. Chong, and Y.C. Shang. 2008. Raves and risks for erythropoietin. Cytokine & Growth Factor Reviews 19(2): 145–155.
12. Maiese, K., F. Li, and Z.Z. Chong. 2005. New avenues of exploration for erythropoietin. JAMA: The Journal of the American Medical Association 293(1): 90–95.
13. Digicaylioglu, M., S. Bichet, H.H. Marti, R.H. Wenger, L.A. Rivas, C. Bauer, and M. Gassmann. 1995. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proceedings of the National Academy of Sciences of the United States of America 92(9): 3717–3720.
14. Lacombe, C., and P. Mayeux. 1999. The molecular biology of erythropoietin. Nephrology, Dialysis, Transplantation 14(2): 22–28.
15. McCook, O., M. Georgieff, A. Scheuerle, P. Möller, C. Thiemermann, and P. Radermacher. 2012. Erythropoietin in the critically ill: do we ask the right questions? Critical Care 16(5): 319.
16. MacRedmond, R., G.K. Singhera, and D.R. Dorscheid. 2009. Erythropoietin inhibits respiratory epithelial cell apoptosis in a model of acute lung injury. The European Respiratory Journal 33(6): 1403–1414.
17. Coleman, T., and M. Brines. 2004. Science review: recombinant human erythropoietin in critical illness: a role beyond anemia? Critical Care 8(5): 337–341.
18. Thiemermann, C. 2007. Beneficial effects of erythropoietin in preclinical models of shock and organ failure. Critical Care 11(3): 132.
19. Brines, M., N.S. Patel, P. Villa, C. Brines, T. Mennini, M. De Paola, Z. Erbayraktar, S. Erbayraktar, B. Sepodes, C. Thiemermann, P. Ghezzi, M. Yamin, C.C. Hand, Q.W. Xie, T. Coleman, and A. Cerami. 2008. Nonerythropoietic, tissue-protective peptides derived from the tertiary structure of erythropoietin. Proceedings of the National Academy of Sciences of the United States of America 105(31): 10925–10930.
20. Maio, R., B. Sepodes, N.S. Patel, C. Thiemermann, H. Mota-Filipe, and P. Costa. 2011. Erythropoietin preserves the integrity and quality of organs for transplantation after cardiac death. Shock 35(2): 126–133.
21. Sepodes, B., R. Maio, R. Pinto, E. Sharples, P. Oliveira, M. McDonald, M. Yaqoob, C. Thiemermann, and H. Mota-Filipe. 2006. Recombinant human erythropoietin protects the liver from hepatic ischemia- reperfusion injury in the rat. Transplant International 19(11): 919–926.
22. Ratilal, B.O., M.M. Arroja, J.P. Rocha, A.M. Fernandes, A.P. Barateiro, D.M. Brites, R.M. Pinto, B.M. Sepodes, and H.D. Mota-Filipe. 2014. Neuroprotective effects of erythropoietin pretreatment in a rodent model of transient middle cerebral artery occlusion. Journal of Neurosurgery 121(1): 55–62.
23. Freitas, M., G. Porto, J.L. Lima, and E. Fernandes. 2008. Isolation and activation of human neutrophils in vitro. The importance of the anticoagulant used during blood collection. Clinical Biochemistry 41(7–8): 570–575.
24. Freitas, M., G. Porto, J.L. Lima, and E. Fernandes. 2009. Optimization of experimental settings for the analysis of human neutrophils oxidative burst in vitro. Talanta 78(4–5): 1476–1483.
25. Freitas, M., J.L. Lima, and E. Fernandes. 2009. Optical probes for detection and quantification of neutrophils’ oxidative burst. A review. Analytica Chimica Acta 649(1): 8–23.
26. Fernandes, E., D. Costa, A.P. Marques, R.L. Reis, and J.L.F.C. Lima. 2006. Inhibition of human neutrophil oxidative burst by pyrazolone derivatives. Free Radical Biology and Medicine 40(4): 632–640.
27. Fischer, A.E., K.A. Jacobson, J. Rose, and R. Zeller. 2008. Hematoxylin and eosin staining of tissue and cell sections. CSH protocols 2008:pdb.prot4986.
28. Schreiber, E., P. Matthias, M.M. Müller, and W. Schaffner. 1989. Rapid detection of octamer binding proteins with ‘mini-extracts’, prepared from a small number of cells. Nucleic Acids Research 17(15): 6419.
29. Fernandes, A., A.S. Falcão, R.F. Silva, A.C. Gordo, M.J. Gama, M.A. Brito, and D. Brites. 2006. Inflammatory signalling pathways involved in astroglial activation by unconjugated bilirubin. Journal of Neurochemistry 96(6): 1667–1679.
30. Barateiro, A., A.R. Vaz, S.L. Silva, A. Fernandes, and D. Brites. 2012. ER stress, mitochondrial dysfunction and calpain/JNK activation are involved in oligodendrocyte precursor cell death by unconjugated bilirubin. NeuroMolecular Medicine 14(4): 285–302.
31. Silva, S.L., A.R. Vaz, A. Barateiro, A.S. Falcão, A. Fernandes, M.A. Brito, R.F. Silva, and D. Brites. 2010. Features of bilirubin-induced reactive microglia: from phagocytosis to inflammation. Neurobiology of Disease 40(3): 663–675.
32. Abdullahi, A., S. Amini-Nik, and M.G. Jeschke. 2014. Animal models in burn research. Cellular and Molecular Life Sciences
33. Brachkova, M.I., P. Marques, J. Rocha, B. Sepodes, M.A. Duarte, and J.F. Pinto. 2011. Alginate films containing Lactobacillus plantarum as wound dressing for prevention of burn infection. Journal of Hospital Infection 79(4): 375–377.
34. Jeschke, M.G., R. Einspanier, D. Klein, and K.W. Jauch. 2002. Insulin attenuates the systemic inflammatory response to thermal trauma. Molecular Medicine 8(8): 443–450.
35. Matute-Bello, G., G. Downey, B.B. Moore, S.D. Groshong, M.A. Matthay, A.S. Slutsky, W.M. Kuebler, and Acute Lung Injury in Animals Study Group. 2011. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. American Journal of Respiratory Cell and Molecular Biology 44(5): 725–738.
36. Cuzzocrea, S., R. Di Paola, E. Mazzon, N.S. Patel, T. Genovese, C. Muià, C. Crisafulli, A.P. Caputi, and C. Thiemermann. 2006. Erythropoietin reduces the development of nonseptic shock induced by zymosan in mice. Critical Care Medicine 34(4): 1168–1177.
37. Tascilar, O., G.K. Cakmak, I.O. Tekin, A.U. Emre, B.H. Ucan, B. Bahadir, S. Acikgoz, O. Irkorucu, K. Karakaya, H. Balbaloglu, G. Kertis, H. Ankarali, and M. Comert. 2007. Protective effects of erythropoietin against acute lung injury in a rat model of acute necrotizing pancreatitis. World Journal of Gastroenterology 13(46): 6172–6182.
38. Coldewey, S.M., A.I. Khan, A. Kapoor, M. Collino, M. Rogazzo, M. Brines, A. Cerami, P. Hall, M. Sheaff, J.E. Kieswich, M.M. Yaqoob, N.S. Patel, and C. Thiemermann. 2013. Erythropoietin attenuates acute kidney dysfunction in murine experimental sepsis by activation of the β-common receptor. Kidney International 84(3): 482–490.
39. Khan, A.I., S.M. Coldewey, N.S. Patel, M. Rogazzo, M. Collino, M.M. Yaqoob, P. Radermacher, A. Kapoor, and C. Thiemermann. 2013. Erythropoietin attenuates cardiac dysfunction in experimental sepsis in mice via activation of the β-common receptor. Disease Models & Mechanisms 6(4): 1021–1030.
40. Nandra, K.K., M. Collino, M. Rogazzo, R. Fantozzi, N.S. Patel, and C. Thiemermann. 2013. Pharmacological preconditioning with erythropoietin attenuates the organ injury and dysfunction induced in a rat model of hemorrhagic shock. Disease Models & Mechanisms 6(3): 701–709.
41. Patel, N.S., K.K. Nandra, and C. Thiemermann. 2012. Bench-to-bedside review: erythropoietin and its derivatives as therapies in critical care. Critical Care 16(4): 229.
42. Mullonkal, C.J., and L.H. Toledo-Pereyra. 2007. Akt in ischemia and reperfusion. Journal of Investigative Surgery 20(3): 195–203.
43. Pap, M., and G.M. Cooper. 1998. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-Kinase/Akt cell survival pathway. The Journal of Biological Chemistry 273(32): 19929–199932.
44. Frame, S., and P. Cohen. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochemical Journal 359(Pt 1): 1–16.
45. Eldar-Finkelman, H., and E.G. Krebs. 1997. Phosphorylation of insulin receptor substrate 1 by glycogen synthase kinase 3 impairs insulin action. Proceedings of the National Academy of Sciences of the United States of America 94(18): 9660–9664.
46. Dugo, L., M. Collin, D.A. Allen, N.S. Patel, I. Bauer, E.M. Mervaala, M. Louhelainen, S.J. Foster, M.M. Yaqoob, and C. Thiemermann. 2005. GSK-3beta inhibitors attenuate the organ injury/dysfunction caused by endotoxemia in the rat. Critical Care Medicine 33(9): 1903–1912.
47. Dugo, L., M. Collin, D.A. Allen, O. Murch, S.J. Foster, M.M. Yaqoob, and C. Thiemermann. 2006. Insulin reduces the multiple organ injury and dysfunction caused by coadministration of lipopolysaccharide and peptidoglycan independently of blood glucose: role of glycogen synthase kinase-3beta inhibition. Critical Care Medicine 34(5): 1489–1496.
48. Bao, Z., S. Lim, W. Liao, Y. Lin, C. Thiemermann, B.P. Leung, and W.S. Wong. 2007. Glycogen synthase kinase-3beta inhibition attenuates asthma in mice. American Journal of Respiratory and Critical Care Medicine 176(5): 431–438.
49. Jellestad, L., T. Fink, S. Pradarutti, D. Kubulus, B. Wolf, I. Bauer, C. Thiemermann, and H. Rensing. 2014. Inhibition of glycogen synthase kinase (GSK)-3-β improves liver microcirculation and hepatocellular function after hemorrhagic shock. European Journal of Pharmacology 724: 175–184.
50. Burger, D., A. Xenocostas, and Q.P. Feng. 2009. Molecular basis of cardioprotection by erythropoietin. Current Molecular Pharmacology 1: 56–69.
51. Nishihara, M., T. Miura, T. Miki, J. Sakamoto, M. Tanno, H. Kobayashi, Y. Ikeda, K. Ohori, A. Takahashi, and K. Shimamoto. 2006. Erythropoietin affords additional cardioprotection to preconditioned hearts by enhanced phosphorylation of glycogen synthase kinase-3 beta. American Journal of Physiology. Heart and Circulatory Physiology 291(2): H748–H755.
52. Chateauvieux, S., C. Grigorakaki, F. Morceau, M. Dicato, and M. Diederich. 2011. Erythropoietin, erythropoiesis and beyond. Biochemical Pharmacology 82(10): 1291–1303.
53. Kilic, E., U. Kilic, J. Soliz, C.L. Bassetti, M. Gassmann, and D.M. Hermann. 2005. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 19(14): 2026–2028.
54. Yamaguchi, H., J.L. Hsu, and M.C. Hung. 2012. Regulation of ubiquitination-mediated protein degradation by survival kinases in cancer. Frontiers in Oncology 2: 15.
55. Chen, C., X. Fang, Y. Wang, Y. Li, D. Wang, X. Zhao, C. Bai, and X. Wang. 2011. Preventive and therapeutic effects of phosphoinositide 3-kinase inhibitors on acute lung injury. Chest 140(2): 391–400.
56. Yum, H.K., J. Arcaroli, J. Kupfner, R. Shenkar, J.M. Penninger, T. Sasaki, K.Y. Yang, J.S. Park, and E. Abraham. 2001. Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. Journal of Immunology 167(11): 6601–6608.
57. Lionetti, V., A. Lisi, E. Patrucco, P. De Giuli, M.G. Milazzo, S. Ceci, M. Wymann, A. Lena, V. Gremigni, V. Fanelli, E. Hirsch, and V.M. Ranieri. 2006. Lack of phosphoinositide 3-kinase-gamma attenuates ventilator-induced lung injury. Critical Care Medicine 34(1): 134–141.
58. Miyahara, T., K. Hamanaka, D.S. Weber, D.A. Drake, M. Anghelescu, and J.C. Parker. 2007. Phosphoinositide 3-kinase, Src, and Akt modulate acute ventilation-induced vascular permeability increases in mouse lungs. American Journal of Physiology - Lung Cellular and Molecular Physiology 293(1): L11–L21.
59. Corwin, H.L., A. Gettinger, R.G. Pearl, M.P. Fink, M.M. Levy, M.J. Shapiro, M.J. Corwin, and T. Colton. 2002. Efficacy of recombinant human erythropoietin in critically ill patients: a randomized controlled trial. JAMA: The Journal of the American Medical Association 288: 2827–2835.
60. Corwin, H.L., A. Gettinger, T.C. Fabian, A. May, R.G. Pearl, S. Heard, R. An, P.J. Bowers, P. Burton, M.A. Klausner, and M.J. Corwin. 2007. Efficacy and safety of epoetin alfa in critically ill patients. The New England Journal of Medicine 357: 965–976.
61. Corwin, H.L. 2007. Erythropoietin use in critically ill patients: forest and trees. CMAJ:Canadian Medical Association Journal 177(7): 747–749.
62. Kakavas, S., T. Demestiha, P. Vasileiou, and T. Xanthos. 2011. Erythropoetin as a novel agent with pleiotropic effects against acute lung injury. European Journal of Clinical Pharmacology 67(1): 1–9.
63. Walden, A.P., J.D. Young, and E. Sharples. 2010. Bench to bedside: a role for erythropoietin in sepsis. Critical Care 14(4): 227.
64. Patel, N.S., M. Collino, M.M. Yaqoob, and C. Thiemermann. 2011. Erythropoietin in the intensive care unit: beyond treatment of anemia. Annals of Intensive Care 1: 40.