Erythropoietin inhibits respiratory epithelial cell apoptosis in a model of acute lung injury

European Respiratory Journal

Volumn 33, Issue 6, 2009, Pages 1403-1414

  MacRedmond, R ^a,b   Singhera, G K ^a   Dorscheid, D R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ST PAUL S HOSPITAL   (Canada)

Author keywords

Acute respiratory distress syndrome; Critically ill; Fas Fas ligand; Polymorphonuclear cells

Indexed keywords

ERYTHROPOIETIN; ERYTHROPOIETIN ANTIBODY; ERYTHROPOIETIN RECEPTOR; FAS ANTIBODY; FAS ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL XL; RECOMBINANT ERYTHROPOIETIN; SMALL INTERFERING RNA;

ACUTE LUNG INJURY; APOPTOSIS; ARTICLE; BRONCHUS MUCOSA; CELL CULTURE; CELL DEATH; CELL INTERACTION; CELL PROTECTION; CONTROLLED STUDY; CROSS LINKING; DRUG INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; NEUTROPHIL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN INDUCTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REGULATORY MECHANISM; RESPIRATORY EPITHELIUM;

ACUTE LUNG INJURY; ANALYSIS OF VARIANCE; ANTIGENS, CD95; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; COCULTURE TECHNIQUES; EPITHELIAL CELLS; ERYTHROPOIETIN; ERYTHROPOIETIN, RECOMBINANT; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSFECTION; UP-REGULATION;

EID: 69249145231     PISSN: 09031936     EISSN: 13993003     Source Type: Journal    
DOI: 10.1183/09031936.00084608     Document Type: Article

References (59)

1. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000; 342: 1334-1349.
2. Matthay MA, Flori HR, Conner ER, et al. Alveolar epithelial fluid transport: basic mechanisms and clinical relevance. Proc Assoc Am Physicians 1998; 110: 496-505.
3. Greene KE, Wright JR, Steinberg KP, et al. Serial changes in surfactant-associated proteins in lung and serum before and after onset of ARDS. Am J Respir Crit Care Med 1999; 160: 1843-1850.
4. Ware LB, Matthay MA. Alveolar fluid clearance is impaired in the majority of patients with acute lung injury and the acute respiratory distress syndrome. Am J Respir Crit Care Med 2001; 163: 1376-1383.
5. Bachofen M, Weibel ER. Structural alterations of lung parenchyma in the adult respiratory distress syndrome. Clin Chest Med 1982; 3: 35-56.
6. Bardales RH, Xie SS, Schaefer RF, et al. Apoptosis is a major pathway responsible for the resolution of type II pneumocytes in acute lung injury. Am J Pathol 1996; 149: 845-852.
7. Vernooy JH, Dentener MA, van Suylen RJ, et al. Intratracheal instillation of lipopolysaccharide in mice induces apoptosis in bronchial epithelial cells: no role for tumor necrosis factor-α and infiltrating neutrophils. Am J Respir Cell Mol Biol 2001; 24: 569-576.
8. Kitamura Y, Hashimoto S, Mizuta N, et al. Fas/FasL-dependent apoptosis of alveolar cells after lipopolysaccharide-induced lung injury in mice. Am J Respir Crit Care Med 2001; 163: 762-769.
9. Matute-Bello G, Liles WC, Steinberg KP, et al. Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS). J Immunol 1999; 163: 2217-2225.
10. Albertine KH, Soulier MF, Wang Z, et al. Fas and fas ligand are up-regulated in pulmonary edema fluid and lung tissue of patients with acute lung injury and the acute respiratory distress syndrome. Am J Pathol 2002; 161: 1783-1796.
11. Hagimoto N, Kuwano K, Miyazaki H, et al. Induction of apoptosis and pulmonary fibrosis in mice in response to ligation of Fas antigen. Am J Respir Cell Mol Biol 1997; 17: 272-278.
12. Matute-Bello G, Winn RK, Jonas M, et al. Fas (CD95) induces alveolar epithelial cell apoptosis in vivo: implications for acute pulmonary inflammation. Am J Pathol 2001; 158: 153-161.
13. Matute-Bello G, Winn RK, Martin TR, et al. Sustained lipopolysaccharide-induced lung inflammation in mice is attenuated by functional deficiency of the Fas/Fas ligand system. Clin Diagn Lab Immunol 2004; 11: 358-361.
14. Chong ZZ, Kang JQ, Maiese K. Erythropoietin: cytoprotection in vascular and neuronal cells. Curr Drug Targets Cardiovasc Haematol Disord 2003; 3: 141-154.
15. Silva M, Benito A, Sanz C, et al. Erythropoietin can induce the expression of bcl-x(L) through Stat5 in erythropoietin-dependent progenitor cell lines. J Biol Chem 1999; 274: 22165-22169.
16. Kashii Y, Uchida M, Kirito K, et al. A member of Forkhead family transcription factor, FKHRL1, is one of the downstream molecules of phosphatidylinositol 3-kinase-Akt activation pathway in erythropoietin signal transduction. Blood 2000; 96: 941-949.
17. Maiese K, Li F, Chong ZZ. New avenues of exploration for erythropoietin. JAMA 2005; 293: 90-95.
18. Gray TE, Guzman K, Davis CW, et al. Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 1996; 14: 104-112.
19. Hamann KJ, Dorscheid DR, Ko FD, et al. Expression of Fas (CD95) and FasL (CD95L) in human airway epithelium. Am J Respir Cell Mol Biol 1998; 19: 537-542.
20. Bonfoco E, Krainc D, Ankarcrona M, et al. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 1995; 92: 7162-7166.
21. Terui Y, Furukawa Y, Kikuchi J, et al. Apoptosis during HL-60 cell differentiation is closely related to a G0/G1 cell cycle arrest. J Cell Physiol 1995; 164: 74-84.
22. Dorscheid DR, Wojcik KR, Sun S, et al. Apoptosis of airway epithelial cells induced by corticosteroids. Am J Respir Crit Care Med 2001; 164: 1939-1947.
23. Patchell BJ, Wojcik KR, Yang TL, et al. Glycosylation and annexin II cell surface translocation mediate airway epithelial wound repair. Am J Physiol Lung Cell Mol Physiol 2007; 293: L354-L363.
24. Davani EY, Dorscheid DR, Lee CH, et al. Novel regulatory mechanism of cardiomyocyte contractility involving ICAM-1 and the cytoskeleton. Am J Physiol Heart Circ Physiol 2004; 287: H1013-H1022.
25. Lester RD, Jo M, Campana WM, et al. Erythropoietin promotes MCF-7 breast cancer cell migration by an ERK/mitogen-activated protein kinase-dependent pathway and is primarily responsible for the increase in migration observed in hypoxia. J Biol Chem 2005; 280: 39273-39277.
26. Calfee CS, Matthay MA. Nonventilatory treatments for acute lung injury and ARDS. Chest 2007; 131: 913-920.
27. Dagnon K, Pacary E, Commo F, et al. Expression of erythropoietin and erythropoietin receptor in non-small cell lung carcinomas. Clin Cancer Res 2005; 11: 993-999.
28. Juul SE, Yachnis AT, Christensen RD. Tissue distribution of erythropoietin and erythropoietin receptor in the developing human fetus. Early Hum Dev 1998; 52: 235-249.
29. Weiss G, Goodnough LT. Anemia of chronic disease. N Engl J Med 2005; 352: 1011-1023.
30. Frede S, Fandrey J, Pagel H, et al. Erythropoietin gene expression is suppressed after lipopolysaccharide or interleukin-1β injections in rats. Am J Physiol 1997; 273: R1067-R1071.
31. La Ferla K, Reimann C, Jelkmann W, et al. Inhibition of erythropoietin gene expression signaling involves the transcription factors GATA-2 and NF-κB. FASEB J 2002; 16: 1811-1813.
32. Jelkmann W. Proinflammatory cytokines lowering erythropoietin production. J Interferon Cytokine Res 1998; 18: 555-559.
33. Grasso G, Sfacteria A, Passalacqua M, et al. Erythropoietin and erythropoietin receptor expression after experimental spinal cord injury encourages therapy by exogenous erythropoietin. Neurosurgery 2005; 56: 821-827.
34. Hashimoto S, Kobayashi A, Kooguchi K, et al. Upregulation of two death pathways of perforin/granzyme and FasL/Fas in septic acute respiratory distress syndrome. Am J Respir Crit Care Med 2000; 161: 237-243.
35. Matute-Bello G, Liles WC, Frevert CW, et al. Recombinant human Fas ligand induces alveolar epithelial cell apoptosis and lung injury in rabbits. Am J Physiol Lung Cell Mol Physiol 2001; 281: L328-L335.
36. Nakamura M, Matute-Bello G, Liles WC, et al. Differential response of human lung epithelial cells to fas-induced apoptosis. Am J Pathol 2004; 164: 1949-1958.
37. Tang PS, Tsang ME, Lodyga M, et al. Lipopolysaccharide accelerates caspase-independent but cathepsin B-dependent death of human lung epithelial cells. J Cell Physiol 2006; 209: 457-467.
38. Neff SB, Z'Graggen BR, Neff TA, et al. Inflammatory response of tracheobronchial epithelial cells to endotoxin. Am J Physiol Lung Cell Mol Physiol 2006; 290: L86-L96.
39. Yang S, Lin H, Diehl AM. Fatty liver vulnerability to endotoxin-induced damage despite NF-κB induction and inhibited caspase 3 activation. Am J Physiol Gastrointest Liver Physiol 2001; 281: G382-G392.
40. Scaffidi C, Fulda S, Srinivasan A, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998; 17: 1675-1687.
41. Breckenridge DG, Xue D. Regulation of mitochondrial membrane permeabilization by BCL-2 family proteins and caspases. Curr Opin Cell Biol 2004; 16: 647-652.
42. Zhande R, Karsan A. Erythropoietin promotes survival of primary human endothelial cells through PI3K-dependent, NF-κB-independent upregulation of Bcl-xL. Am J Physiol Heart Circ Physiol 2007; 292: H2467-H2474.
43. Johnson DW, Pat B, Vesey DA, et al. Delayed administration of darbepoetin or erythropoietin protects against ischemic acute renal injury and failure. Kidney Int 2006; 69: 1806-1813.
44. Kumral A, Genc S, Ozer E, et al. Erythropoietin downregulates bax and DP5 proapoptotic gene expression in neonatal hypoxic-ischemic brain injury. Biol Neonate 2006; 89: 205-210.
45. Walker DC, Behzad AR, Chu F. Neutrophil migration through preexisting holes in the basal laminae of alveolar capillaries and epithelium during streptococcal pneumonia. Microvasc Res 1995; 50: 397-416.
46. Jones HA, Clark RJ, Rhodes CG, et al. In vivo measurement of neutrophil activity in experimental lung inflammation. Am J Respir Crit Care Med 1994; 149: 1635-1639.
47. Serrao KL, Fortenberry JD, Owens ML, et al. Neutrophils induce apoptosis of lung epithelial cells via release of soluble Fas ligand. Am J Physiol Lung Cell Mol Physiol 2001; 280: L298-L305.
48. Suzuki T, Moraes TJ, Vachon E, et al. Proteinase-activated receptor-1 mediates elastase-induced apoptosis of human lung epithelial cells. Am J Respir Cell Mol Biol 2005; 33: 231-247.
49. Silva M, Grillot D, Benito A, et al. Erythropoietin can promote erythroid progenitor survival by repressing apoptosis through Bcl-XL and Bcl-2. Blood 1996; 88: 1576-1582.
50. Chong ZZ, Kang JQ, Maiese K. Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation of microglia, Akt1, Bad, and caspase-mediated pathways. Br J Pharmacol 2003; 138: 1107-1118.
51. Krafte-Jacobs B, Levetown ML, Bray GL, et al. Erythropoietin response to critical illness. Crit Care Med 1994; 22: 821-826.
52. Elliot JM, Virankabutra T, Jones S, et al. Erythropoietin mimics the acute phase response in critical illness. Crit Care 2003; 7: R35-R40.
53. Rogiers P, Zhang H, Leeman M, et al. Erythropoietin response is blunted in critically ill patients. Intensive Care Med 1997; 23: 159-162.
54. Corwin HL, Gettinger A, Fabian TC, et al. Efficacy and safety of epoetin-α in critically ill patients. N Engl J Med 2007; 357: 965-976.
55. Fischer U, Schulze-Osthoff K. Apoptosis-based therapies and drug targets. Cell Death Differ 2005; 12: Suppl. 1, 942-961.
56. Bohlius J, Wilson J, Seidenfeld J, et al. Erythropoietin or darbepoetin for patients with cancer. Cochrane Database Syst Rev 2006; 3: CD003407.
57. Lai SY, Grandis JR. Understanding the presence and function of erythropoietin receptors on cancer cells. J Clin Oncol 2006; 24: 4675-4676.
58. Ehrenreich H, Hasselblatt M, Dembowski C, et al. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 2002; 8: 495-505.
59. Lipsic E, van der Meer P, Voors AA, et al. A single bolus of a long-acting erythropoietin analogue darbepoetin-α in patients with acute myocardial infarction: a randomized feasibility and safety study. Cardiovasc Drugs Ther 2006; 20: 135-141.