Early activation of pro-fibrotic WNT5A in sepsis-induced acute lung injury

Critical Care

Volumn 18, Issue 5, 2014, Pages

  Villar, Jesús ^a   Cabrera Benítez, Nuria E ^a,b   Ramos Nuez, Angela ^a,b   Flores, Carlos ^a,d   García Hernández, Sonia ^e   Valladares, Francisco ^a,e   López Aguilar, Josefina ^a,f   Blanch, Lluís ^a,f   Slutsky, Arthur S ^c,g  

^a INSTITUTO DE SALUD CARLOS III   (Spain)

^b HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^c ST MICHAEL'S HOSPITAL   (Canada)

^d HOSPITAL UNIVERSITARIO NUESTRA SEÑORA DE CANDELARIA   (Spain)

^e UNIVERSIDAD DE LA LAGUNA   (Spain)

^f Hospital Universitari Parc Taulí   (Spain)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; COLLAGEN; CYCLIN D1; MATRILYSIN; VASCULOTROPIN; WNT5A PROTEIN; WNT PROTEIN; WNT5A PROTEIN, RAT;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHUS MUCOSA; CONTROLLED STUDY; GENE TARGETING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG BIOPSY; LUNG FIBROBLAST; MALE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RAT; SEPSIS; UPREGULATION; VALIDATION PROCESS; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; COMPLICATION; FIBROSIS; METABOLISM; PATHOLOGY; RESPIRATORY TRACT MUCOSA; SPRAGUE DAWLEY RAT;

ACUTE LUNG INJURY; ANIMALS; CELLS, CULTURED; FIBROSIS; HUMANS; MALE; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUCOSA; SEPSIS; WNT PROTEINS;

EID: 84964696664     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/s13054-014-0568-z     Document Type: Article

References (48)

1. Ware LB, Matthay MA: The acute respiratory distress syndrome. N Engl J Med 2000, 342:1334-1349.
2. Villar J: What is the acute respiratory distress syndrome? Respir Care 2011, 56:1539-1545.
3. Villar J, Blanco J, Añón JM, Santos-Bouza A, Blanch L, Ambrós A, Gandía F, Carriedo D, Mosteiro F, Basaldúa S, Fernández RL, Kacmarek RM, ALIEN Network: The ALIEN study: incidence and outcome of acute respiratory distress syndrome in the era of lung protective ventilation. Intensive Care Med 2011, 37:1932-1941.
4. Angus DC, Linde-Zwirble WT, Lidicker J, Clermont G, Carcillo J, Pinsky MR: Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001, 29:1303-1310.
5. Shimabukuro DW, Sawa T, Gropper MA: Injury and repair in lung and airways. Crit Care Med 2003, 31:S524-S531.
6. Chesnutt AN, Matthay MA, Tibayan FA, Clark JG: Early detection of type III procollagen peptide in acute lung injury: pathogenetic and prognostic significance. Am J Respir Crit Care Med 1997, 156:840-845.
7. Horowitz JC, Cui Z, Moore TA, Meier TR, Reddy RC, Toews GB, Standiford TJ, Thannickal VJ: Constitutive activation of prosurvival signaling in alveolar mesenchymal cells isolated from patients with nonresolving acute respiratory distress syndrome. Am J Physiol Lung Cell Mol Physiol 2006, 290:L415-L425.
8. Marshall RP, Bellingan G, Webb S, Puddicombe A, Goldsack N, McAnulty RJ, Laurent GJ: Fibroproliferation occurs early in the acute respiratory distress syndrome and impacts on outcome. Am J Respir Crit Care Med 2000, 162:1783-1788.
9. Selman M, Pardo A: Idiopathic pulmonary fibrosis: an epithelial/ fibroblastic cross-talk disorder. Respir Res 2002, 3:31.
10. Konigshoff M, Kramer M, Balsara N, Wilhelm J, Amarie OV, Jahn A, Rose F, Fink L, Seeger W, Schaefer L, Günther A, Eickelberg O: WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J Clin Invest 2009, 119:772-787.
11. Pongracz JE, Stockley RA: Wnt signalling in lung development and diseases. Respir Res 2006, 7:15.
12. Crosby LM, Waters CM: Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol 2010, 298:L715-L731.
13. Staal FJ, Noort MM, Strous GJ, Clevers HC: Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep 2002, 3:63-68.
14. Morrisey EE: Wnt signaling and pulmonary fibrosis. Am J Pathol 2003, 162:1393-1397.
15. Nelson WJ, Nusse R: Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004, 303:1483-1487.
16. Konigshoff M, Balsara N, Pfaff EM, Kramer M, Chrobak I, Seeger W, Eickelberg O: Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLoS One 2008, 3:e2142.
17. Villar J, Cabrera N, Casula M, Flores C, Valladares F, Muros M, Blanch L, Slutsky AS, Kacmarek RM: Mechanical ventilation modulates Toll-like receptor signaling pathway in a sepsis-induced lung injury model. Intensive Care Med 2010, 36:1049-1057.
18. Koyama S, Sato E, Nomura H, Kubo K, Miura M, Yamashita T, Nagai S, Izumi T: The potential of various lipopolysaccharides to release IL-8 and G-CSF. Am J Physiol Lung Cell Mol Physiol 2000, 278:L658-L666.
19. Pugin J, Dunn-Siegrist I, Dufour J, Tissières P, Charles PE, Comte R: Cyclic stretch of human lung cells induces an acidification and promotes bacterial growth. Am J Respir Cell Mol Biol 2008, 38:362-370.
20. Boots AW, Gerloff K, Bartholomé R, van Berlo D, Ledermann K, Haenen GR, Bast A, van Schooten FJ, Albrecht C, Schins RP: Neutrophils augment LPS-mediated pro-inflammatory signaling in human lung epithelial cells. Biochim Biophys Acta 1823, 2012:1151-1162.
21. Fortis S, Spieth PM, Lu WY, Parotto M, Haitsma JJ, Slutsky AS, Zhong N, Mazer CD, Zhang H: Effects of anesthetic regimes on inflammatory responses in a rat model of acute lung injury. Intensive Care Med 2012, 38:1548-1555.
22. Cabrera-Benitez NE, Pérez-Roth E, Casula M, Ramos-Nuez A, Ríos-Luci C, Rodríguez-Gallego C, Sologuren I, Jakubkiene V, Slutsky AS, Padrón JM, Villar J: Anti-inflammatory activity of a novel family of aryl ureas compounds in an endotoxin-induced airway epithelial cell injury model. PLoS One 2012, 7:e48468.
23. He Z, Gao Y, Deng Y, Li W, Chen Y, Xing S, Zhao X, Ding J, Wang X: Lipopolysaccharide induces lung fibroblast proliferation through Toll-like receptor 4 signaling and the phosphoinositide3-kinase-Akt pathway. PLoS One 2012, 7:e35926.
24. Cohen M, Marchand-Adam S, Lecon-Malas V, Marchal-Somme J, Boutten A, Durand G, Crestani B, Dehoux M: HGF synthesis in human lung fibroblasts is regulated by oncostatin M. Am J Physiol Lung Cell Mol Physiol 2006, 290:L1097-L1103.
25. Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D, Warren JT, Bokesch H, Kenney S, Boyd MR: New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst 1990, 82:1107-1112.
26. Cabrera-Benitez NE, Parotto M, Post M, Han B, Spieth PM, Cheng WE, Valladares F, Villar J, Liu M, Sato M, Zhang H, Slutsky AS: Mechanical stress induces lung fibrosis by epithelial-mesenchymal transition. Crit Care Med 2012, 40:510-517.
27. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG: Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010, 8:e1000412.
28. Rittirsch D, Huber-Lang MS, Flierl MA, Ward PA: Immunodesign of experimental sepsis by cecal ligation and puncture. Nat Protoc 2009, 4:31-36.
29. Malkusch W, Rehn B, Bruch J: Advantages of Sirius Red staining for quantitative morphometric collagen measurements in lungs. Exp Lung Res 1995, 21:67-77.
30. Martínez-Galán L, del Puerto-Nevado L, Pérez-Rial S, Díaz-Gil JJ, González Mangado N, Peces-Barba G: Liver growth factor improves pulmonary fibrosis secondary to cadmium administration in rats. Arch Bronconeumol 2010, 46:20-26.
31. Aoki Y, Maeno T, Aoyagi K, Ueno M, Aoki F, Aoki N, Nakagawa J, Sando Y, Shimizu Y, Suga T, Arai M, Kurabayashi M: Pioglitazone, a peroxisome proliferator-activated receptor gamma ligand, suppresses bleomycininduced acute lung injury and fibrosis. Respiration 2009, 77:311-319.
32. Strieter RM, Belperio JA, Keane MP: Cytokines in innate host defense in the lung. J Clin Invest 2002, 109:699-705.
33. Cheng DS, Han W, Chen SM, Sherrill TP, Chont M, Park GY, Sheller JR, Polosukhin VV, Christman JW, Yull FE, Blackwell TS: Airway epithelium controls lung inflammation and injury through the NF-kappa B pathway. J Immunol 2007, 178:6504-6513.
34. Lin WJ, Yeh WC: Implication of Toll-like receptor and tumor necrosis factor alpha signalling in septic shock. Shock 2005, 24:206-209.
35. Koyama S, Sato E, Nomura H, Kubo K, Miura M, Yamashita T, Nagai S, Izumi T: The potential of various lipopolysaccharides to release monocyte chemotactic activity from lung epithelial cells and fibroblasts. Eur Respir J 1999, 14:545-552.
36. MacRedmond R, Singhera GK, Dorscheid DR: Erythropoietin inhibits respiratory epithelial cell apoptosis in a model of acute lung injury. Eur Respir J 2009, 33:1403-1414.
37. Stockmann C, Kerdiles Y, Nomaksteinsky M, Weidemann A, Takeda N, Doedens A, Torres-Collado AX, Iruela-Arispe L, Nizet V, Johnson RS: Loss of myeloid cell-derived vascular endothelial growth factor accelerates fibrosis. Proc Natl Acad Sci U S A 2010, 107:4329-4334.
38. Torgersen C, Moser P, Luckner G, Mayr V, Jochberger S, Hasibeder WR, Dünser MW: Macroscopic postmortem findings in 235 surgical intensive care patients with sepsis. Anesth Analg 2009, 108:1841-1847.
39. Cabrera-Benitez NE, Laffey JG, Parotto M, Spieth PM, Villar J, Zhang H, Slutsky AS: Mechanical ventilation-associated lung fibrosis in acute respiratory distress syndrome. Anesthesiology 2014, 121:189-198.
40. Ichikado K, Muranaka H, Gushima Y, Kotani T, Nader HM, Fujimoto K, Johkoh T, Iwamoto N, Kawamura K, Nagano J, Fukuda K, Hirata N, Yoshinaga T, Ichiyasu H, Tsumura S, Kohrogi H, Kawaguchi A, Yoshioka M, Sakuma T, Suga M: Fibroproliferative changes on high-resolution CT in the acute respiratory distress syndrome predict mortality and ventilator dependency: a prospective observational cohort study. BMJ Open 2012, 2:e000545.
41. Blumenthal A, Ehlers S, Lauber J, Buer J, Lange C, Goldmann T, Heine H, Brandt E, Reiling N: The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 2006, 108:965-973.
42. Königshoff M, Eickelberg O: WNT signaling in lung disease: a failure or a regeneration signal? Am J Respir Cell Mol Biol 2010, 42:21-31.
43. Vuga LJ, Ben-Yehudah A, Kovkarova-Naumovski E, Oriss T, Gibson KF, Feghali-Bostwick C, Kaminski N: WNT5A is a regulator of fibroblast proliferation and resistance to apoptosis. Am J Respir Cell Mol Biol 2009, 41:583-589.
44. Chilosi M, Poletti V, Zamò A, Lestani M, Montagna L, Piccoli P, Pedron S, Bertaso M, Scarpa A, Murer B, Cancellieri A, Maestro R, Semenzato G, Doglioni C: Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am J Pathol 2003, 162:1495-1502.
45. Rocco PR, Dos Santos C, Pelosi P: Lung parenchyma remodeling in acute respiratory distress syndrome. Minerva Anestesiol 2009, 75:730-740.
46. Zuo F, Kaminski N, Eugui E, Allard J, Yakhini Z, Ben-Dor A, Lollini L, Morris D, Kim Y, DeLustro B, Sheppard D, Pardo A, Selman M, Heller RA: Gene expression analysis reveals matrilysin as a key regulator of pulmonary fibrosis in mice and humans. Proc Natl Acad Sci USA 2002, 99:6292-6297.
47. Jenei V, Sherwood V, Howlin J, Linnskog R, Säfholm A, Axelsson L, Andersson T: A t-butyloxycarbonyl-modified Wnt5a-derived hexapeptide functions as a potent antagonist of Wnt5a-dependent melanoma cell invasion. Proc Natl Acad Sci USA 2009, 106:19473-19478.
48. Henderson WR Jr, Chi EY, Ye X, Nguyen C, Tien YT, Zhou B, Borok Z, Knight DA, Kahn M: Inhibition of Wnt/beta-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc Natl Acad Sci U S A 2010, 107:14309-14314.