Deguelin attenuates reperfusion injury and improves outcome after orthotopic lung transplantation in the rat

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Paulus, Patrick ^a   Ockelmann, Pia ^a   Tacke, Sabine ^b   Karnowski, Nora ^c   Ellinghaus, Peter ^c   Scheller, Bertram ^a   Holfeld, Johannes ^d   Urbschat, Anja ^a   Zacharowski, Kai ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c BAYER PHARMA AG   (Germany)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CD68 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; DEGUELIN; GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR 1; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 4; INTERLEUKIN 6; VASCULOTROPIN A;

ADVERSE OUTCOME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL HYPOXIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; CXCR4 GENE; DOWN REGULATION; EDEMA; ENDOTHELIAL DYSFUNCTION; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; ICAM 1 GENE; IMMUNOMODULATION; IN VITRO STUDY; INFLAMMATION; LUNG ALVEOLUS CELL; LUNG TRANSPLANTATION; MALE; MONOCYTE; NONHUMAN; RAT; REPERFUSION INJURY; SHORT TERM SURVIVAL; SURVIVAL RATE; UPREGULATION; VEGF A GENE;

ANIMALS; INTERCELLULAR ADHESION MOLECULE-1; LUNG TRANSPLANTATION; MALE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CXCR4; REPERFUSION INJURY; ROTENONE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84862665618     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039265     Document Type: Article

References (62)

1. Trulock EP, Christie JD, Edwards LB, Boucek MM, Aurora P, et al. (2007) Registry of the International Society for Heart and Lung Transplantation: twenty-fourth official adult lung and heart-lung transplantation report-2007. J Heart Lung Transplant 26: 782-795.
2. Souilamas R, (2009) Donor lung availability in the 21st century. Bull Acad Natl Med 193: 1589-1597; discussion 1597-1589.
3. Boucek MM, Aurora P, Edwards LB, Taylor DO, Trulock EP, et al. (2007) Registry of the International Society for Heart and Lung Transplantation: tenth official pediatric heart transplantation report-2007. J Heart Lung Transplant 26: 796-807.
4. Wohlschlager J, Sommerwerck U, Jonigk D, Rische J, Baba HA, et al. (2011) [Lung transplantation and rejection. Basic principles, clinical aspects and histomorphology]. Pathologe 32: 104-112.
5. Kruger B, Krick S, Dhillon N, Lerner SM, Ames S, et al. (2009) Donor Toll-like receptor 4 contributes to ischemia and reperfusion injury following human kidney transplantation. Proc Natl Acad Sci U S A 106: 3390-3395.
6. Fang N, Casida JE, (1998) Anticancer action of cube insecticide: correlation for rotenoid constituents between inhibition of NADH:ubiquinone oxidoreductase and induced ornithine decarboxylase activities. Proc Natl Acad Sci U S A 95: 3380-3384.
7. Hail N Jr, Lotan R, (2004) Apoptosis induction by the natural product cancer chemopreventive agent deguelin is mediated through the inhibition of mitochondrial bioenergetics. Apoptosis 9: 437-447.
8. Navarro A, Bandez MJ, Gomez C, Repetto MG, Boveris A, (2010) Effects of rotenone and pyridaben on complex I electron transfer and on mitochondrial nitric oxide synthase functional activity. J Bioenerg Biomembr 42: 405-412.
9. Loor G, Schumacker PT, (2008) Role of hypoxia-inducible factor in cell survival during myocardial ischemia-reperfusion. Cell Death Differ 15: 686-690.
10. Marx J, (2004) Cell biology. How cells endure low oxygen. Science 303: 1454-1456.
11. Pouyssegur J, Dayan F, Mazure NM, (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
12. Chen F, Kondo N, Sonobe M, Fujinaga T, Wada H, et al. (2008) Expression of endothelial cell-specific adhesion molecules in lungs after cardiac arrest. Interact Cardiovasc Thorac Surg 7: 437-440.
13. Winning S, Splettstoesser F, Fandrey J, Frede S, (2010) Acute hypoxia induces HIF-independent monocyte adhesion to endothelial cells through increased intercellular adhesion molecule-1 expression: the role of hypoxic inhibition of prolyl hydroxylase activity for the induction of NF-kappa B. J Immunol 185: 1786-1793.
14. Taghavi S, Abraham D, Riml P, Paulus P, Schafer R, et al. (2002) Co-expression of endothelin-1 and vascular endothelial growth factor mediates increased vascular permeability in lung grafts before reperfusion. J Heart Lung Transplant 21: 600-603.
15. Kazi AA, Lee WS, Wagner E, Becker PM, (2000) VEGF, fetal liver kinase-1, and permeability increase during unilateral lung ischemia. Am J Physiol Lung Cell Mol Physiol 279: L460-467.
16. Ten VS, Pinsky DJ, (2002) Endothelial response to hypoxia: physiologic adaptation and pathologic dysfunction. Curr Opin Crit Care 8: 242-250.
17. Paulus P, Jennewein C, Zacharowski K, (2011) Biomarkers of endothelial dysfunction: can they help us deciphering systemic inflammation and sepsis? Biomarkers 16: S11-21.
18. Bindewald K, Gunduz D, Hartel F, Peters SC, Rodewald C, et al. (2004) Opposite effect of cAMP signaling in endothelial barriers of different origin. Am J Physiol Cell Physiol 287: C1246-1255.
19. Brinkkoetter PT, Beck GC, Gottmann U, Loesel R, Schnetzke U, et al. (2006) Hypothermia-induced loss of endothelial barrier function is restored after dopamine pretreatment: role of p42/p44 activation. Transplantation 82: 534-542.
20. Hanusch C, Nowak K, Torlitz P, Gill IS, Song H, et al. (2008) Donor dopamine treatment limits pulmonary oedema and inflammation in lung allografts subjected to prolonged hypothermia. Transplantation 85: 1449-1455.
21. Kosieradzki M, Rowinski W, (2008) Ischemia/reperfusion injury in kidney transplantation: mechanisms and prevention. Transplant Proc 40: 3279-3288.
22. Abraham D, Krenn K, Seebacher G, Paulus P, Klepetko W, et al. (2004) Upregulated hypoxia-inducible factor-1 DNA binding activity to the vascular endothelial growth factor-A promoter mediates increased vascular permeability in donor lung grafts. Ann Thorac Surg 77: 1751-1755.
23. Krenn K, Klepetko W, Taghavi S, Paulus P, Aharinejad S, (2007) Vascular endothelial growth factor increases pulmonary vascular permeability in cystic fibrosis patients undergoing lung transplantation. Eur J Cardiothorac Surg 32: 35-41.
24. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, et al. (1996) Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 87: 3336-3343.
25. Clauss M, Gerlach M, Gerlach H, Brett J, Wang F, et al. (1990) Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. J Exp Med 172: 1535-1545.
26. Eltzschig HK, (2011) Targeting Hypoxia-induced Inflammation. Anesthesiology 114: 239-242.
27. Eltzschig HK, Carmeliet P, (2011) Hypoxia and inflammation. N Engl J Med 364: 656-665.
28. Grocott MP, Martin DS, Levett DZ, McMorrow R, Windsor J, et al. (2009) Arterial blood gases and oxygen content in climbers on Mount Everest. N Engl J Med 360: 140-149.
29. Semenza GL, (2007) Life with oxygen. Science 318: 62-64.
30. Mackel AM, DeLustro F, DeLustro B, Fudenberg HH, LeRoy EC, (1982) Immune response to connective tissue components of the basement membrane. Connect Tissue Res 10: 333-343.
31. Eckle T, Grenz A, Laucher S, Eltzschig HK, (2008) A2B adenosine receptor signaling attenuates acute lung injury by enhancing alveolar fluid clearance in mice. J Clin Invest 118: 3301-3315.
32. Schingnitz U, Hartmann K, Macmanus CF, Eckle T, Zug S, et al. (2010) Signaling through the A2B adenosine receptor dampens endotoxin-induced acute lung injury. J Immunol 184: 5271-5279.
33. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, et al. (1997) A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A 94: 4273-4278.
34. Ferrara N, (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77: 527-543.
35. Flamme I, Frohlich T, von Reutern M, Kappel A, Damert A, et al. (1997) HRF, a putative basic helix-loop-helix-PAS-domain transcription factor is closely related to hypoxia-inducible factor-1 alpha and developmentally expressed in blood vessels. Mech Dev 63: 51-60.
36. Lassus P, Turanlahti M, Heikkila P, Andersson LC, Nupponen I, et al. (2001) Pulmonary vascular endothelial growth factor and Flt-1 in fetuses, in acute and chronic lung disease, and in persistent pulmonary hypertension of the newborn. Am J Respir Crit Care Med 164: 1981-1987.
37. Aharinejad S, Schafer R, Krenn K, Zuckermann A, Schneider B, et al. (2007) Donor myocardial HIF-1alpha is an independent predictor of cardiac allograft dysfunction: a 7-year prospective, exploratory study. Am J Transplant 7: 2012-2019.
38. Abraham D, Taghavi S, Riml P, Paulus P, Hofmann M, et al. (2002) VEGF-A and-C but not-B mediate increased vascular permeability in preserved lung grafts. Transplantation 73: 1703-1706.
39. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292: C125-136.
40. Rodeheffer RJ, Naftel DC, Stevenson LW, Porter CB, Young JB, et al. (1996) Secular trends in cardiac transplant recipient and donor management in the United States, 1990 to 1994. A multi-institutional study. Cardiac Transplant Research Database Group. Circulation 94: 2883-2889.
41. Lee JC, Christie JD, (2011) Primary graft dysfunction. Clin Chest Med 32: 279-293.
42. Linfert D, Chowdhry T, Rabb H, (2009) Lymphocytes and ischemia-reperfusion injury. Transplant Rev (Orlando) 23: 1-10.
43. Peeters P, Vanholder R, (2008) Therapeutic interventions favorably influencing delayed and slow graft function in kidney transplantation: mission impossible? Transplantation 85: S31-37.
44. Koeppen M, Eckle T, Eltzschig HK, (2011) The hypoxia-inflammation link and potential drug targets. Curr Opin Anaesthesiol 24: 363-369.
45. Semenza GL, (2005) Pulmonary vascular responses to chronic hypoxia mediated by hypoxia-inducible factor 1. Proc Am Thorac Soc 2: 68-70.
46. Kannan KB, Colorado I, Reino D, Palange D, Lu Q, et al. (2011) Hypoxia-inducible factor plays a gut-injurious role in intestinal ischemia reperfusion injury. Am J Physiol Gastrointest Liver Physiol 300: G853-861.
47. Polosukhin VV, Cates JM, Lawson WE, Milstone AP, Matafonov AG, et al. (2011) Hypoxia-inducible factor-1 signalling promotes goblet cell hyperplasia in airway epithelium. J Pathol 224: 203-211.
48. Polosukhin VV, Lawson WE, Milstone AP, Egunova SM, Kulipanov AG, et al. (2007) Association of progressive structural changes in the bronchial epithelium with subepithelial fibrous remodeling: a potential role for hypoxia. Virchows Arch 451: 793-803.
49. Wang GL, Semenza GL, (1993) Desferrioxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood 82: 3610-3615.
50. Wang GL, Semenza GL, (1993) Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J Biol Chem 268: 21513-21518.
51. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, et al. (2001) HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. FASEB J 15: 2445-2453.
52. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, et al. (2005) Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105: 659-669.
53. Cursio R, Miele C, Filippa N, Van Obberghen E, Gugenheim J, (2008) Liver HIF-1 alpha induction precedes apoptosis following normothermic ischemia-reperfusion in rats. Transplant Proc 40: 2042-2045.
54. Jiang X, Khan MA, Tian W, Beilke J, Natarajan R, et al. (2011) Adenovirus-mediated HIF-1alpha gene transfer promotes repair of mouse airway allograft microvasculature and attenuates chronic rejection. J Clin Invest 121: 2336-2349.
55. Krebs R, Hollmen ME, Tikkanen JM, Wu Y, Hicklin DJ, et al. (2006) Vascular endothelial growth factor plays a major role in development of experimental obliterative bronchiolitis. Transplant Proc 38: 3266-3267.
56. Yamada M, Kubo H, Kobayashi S, Ishizawa K, He M, et al. (2011) The increase in surface CXCR4 expression on lung extravascular neutrophils and its effects on neutrophils during endotoxin-induced lung injury. Cell Mol Immunol 8: 305-314.
57. Liu G, Vogel SM, Gao X, Javaid K, Hu G, et al. (2011) Src phosphorylation of endothelial cell surface intercellular adhesion molecule-1 mediates neutrophil adhesion and contributes to the mechanism of lung inflammation. Arterioscler Thromb Vasc Biol 31: 1342-1350.
58. Hashimoto S, Yamada M, Motoyoshi K, Akagawa KS, (1997) Enhancement of macrophage colony-stimulating factor-induced growth and differentiation of human monocytes by interleukin-10. Blood 89: 315-321.
59. de Waal Malefyt R, Figdor CG, Huijbens R, Mohan-Peterson S, Bennett B, et al. (1993) Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes. Comparison with IL-4 and modulation by IFN-gamma or IL-10. J Immunol 151: 6370-6381.
60. Dominguez-Soto A, Sierra-Filardi E, Puig-Kroger A, Perez-Maceda B, Gomez-Aguado F, et al. (2011) Dendritic cell-specific ICAM-3-grabbing nonintegrin expression on M2-polarized and tumor-associated macrophages is macrophage-CSF dependent and enhanced by tumor-derived IL-6 and IL-10. J Immunol 186: 2192-2200.
61. Villalta SA, Deng B, Rinaldi C, Wehling-Henricks M, Tidball JG, (2011) IFN-gamma promotes muscle damage in the mdx mouse model of Duchenne muscular dystrophy by suppressing M2 macrophage activation and inhibiting muscle cell proliferation. J Immunol 187: 5419-5428.
62. Paulus P, Stanley ER, Schafer R, Abraham D, Aharinejad S, (2006) Colony-stimulating factor-1 antibody reverses chemoresistance in human MCF-7 breast cancer xenografts. Cancer Res 66: 4349-4356.