Table of Contents Author Guidelines Submit a Manuscript
Disease Markers
Volume 2016 (2016), Article ID 3501373, 20 pages
http://dx.doi.org/10.1155/2016/3501373
Review Article

A Pathophysiologic Approach to Biomarkers in Acute Respiratory Distress Syndrome

1CHU Clermont-Ferrand, Intensive Care Unit, Department of Perioperative Medicine, Estaing University Hospital, 63000 Clermont-Ferrand, France
2Clermont Université, Université d’Auvergne, EA 7281, R2D2, 63000 Clermont-Ferrand, France
3Department of Medical Biochemistry and Molecular Biology, CHU Clermont-Ferrand, 63000 Clermont-Ferrand, France

Received 2 December 2015; Accepted 10 January 2016

Academic Editor: George Perry

Copyright © 2016 Raiko Blondonnet et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. V. M. Ranieri, G. D. Rubenfeld, P. T. Thompson et al., “Acute respiratory distress syndrome: the Berlin definition,” The Journal of the American Medical Association, vol. 307, no. 23, pp. 2526–2533, 2012. View at Publisher · View at Google Scholar
  2. L. B. Ware and M. A. Matthay, “The acute respiratory distress syndrome,” The New England Journal of Medicine, vol. 342, no. 18, pp. 1334–1349, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Brun-Buisson, C. Minelli, G. Bertolini et al., “Epidemiology and outcome of acute lung injury in European intensive care units,” Intensive Care Medicine, vol. 30, no. 1, pp. 51–61, 2004. View at Publisher · View at Google Scholar
  4. G. D. Rubenfeld, E. Caldwell, E. Peabody et al., “Incidence and outcomes of acute lung injury,” The New England Journal of Medicine, vol. 353, no. 16, pp. 1685–1693, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. D. W. Dowdy, M. P. Eid, C. R. Dennison et al., “Quality of life after acute respiratory distress syndrome: a meta-analysis,” Intensive Care Medicine, vol. 32, no. 8, pp. 1115–1124, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. C. S. Calfee, M. D. Eisner, L. B. Ware et al., “Trauma-associated lung injury differs clinically and biologically from acute lung injury due to other clinical disorders,” Critical Care Medicine, vol. 35, no. 10, pp. 2243–2250, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. C. S. Calfee, D. R. Janz, G. R. Bernard et al., “Distinct molecular phenotypes of direct versus indirect ARDS in single and multi-center studies,” Chest, vol. 147, no. 6, pp. 1539–1548, 2015. View at Publisher · View at Google Scholar
  8. P. Tejera, N. J. Meyer, F. Chen et al., “Distinct and replicable genetic risk factors for acute respiratory distress syndrome of pulmonary or extrapulmonary origin,” Journal of Medical Genetics, vol. 49, no. 11, pp. 671–680, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. M. A. Matthay, G. A. Zimmerman, C. Esmon et al., “Future research directions in acute lung injury: summary of a National Heart, Lung, and Blood Institute Working Group,” American Journal of Respiratory and Critical Care Medicine, vol. 167, no. 7, pp. 1027–1035, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. J. P. Reilly, S. Bellamy, M. G. S. Shashaty et al., “Heterogeneous phenotypes of acute respiratory distress syndrome after major trauma,” Annals of the American Thoracic Society, vol. 11, no. 5, pp. 728–736, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Puybasset, P. Cluzel, N. Chao et al., “A computed tomography scan assessment of regional lung volume in acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 158, no. 5, pp. 1644–1655, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. J.-M. Constantin, S. Grasso, G. Chanques et al., “Lung morphology predicts response to recruitment maneuver in patients with acute respiratory distress syndrome,” Critical Care Medicine, vol. 38, no. 4, pp. 1108–1117, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. C. S. Calfee, K. Delucchi, P. E. Parsons, B. T. Thompson, L. B. Ware, and M. A. Matthay, “Subphenotypes in acute respiratory distress syndrome: latent class analysis of data from two randomised controlled trials,” The Lancet Respiratory Medicine, vol. 2, no. 8, pp. 611–620, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Marshall, G. Bellingan, and G. Laurent, “The acute respiratory distress syndrome: fibrosis in the fast lane,” Thorax, vol. 53, no. 10, pp. 815–817, 1998. View at Publisher · View at Google Scholar
  15. R. B. Henderson, J. A. R. Hobbs, M. Mathies, and N. Hogg, “Rapid recruitment of inflammatory monocytes is independent of neutrophil migration,” Blood, vol. 102, no. 1, pp. 328–335, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. H. M. Marriott and D. H. Dockrell, “The role of the macrophage in lung disease mediated by bacteria,” Experimental Lung Research, vol. 33, no. 10, pp. 493–505, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. L. J. M. Cross and M. A. Matthay, “Biomarkers in acute lung injury: insights into the pathogenesis of acute lung injury,” Critical Care Clinics, vol. 27, no. 2, pp. 355–377, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. H. K. Gaggin and J. L. Januzzi, “Biomarkers and diagnostics in heart failure,” Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease, vol. 1832, no. 12, pp. 2442–2450, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. E. Christenson and R. H. Christenson, “The role of cardiac biomarkers in the diagnosis and management of patients presenting with suspected acute coronary syndrome,” Annals of Laboratory Medicine, vol. 33, no. 5, pp. 309–318, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. L. B. Ware, T. Koyama, Z. Zhao et al., “Biomarkers of lung epithelial injury and inflammation distinguish severe sepsis patients with acute respiratory distress syndrome,” Critical Care, vol. 17, no. 5, article R253, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. A. Matthay, L. B. Ware, and G. A. Zimmerman, “The acute respiratory distress syndrome,” The Journal of Clinical Investigation, vol. 122, no. 8, pp. 2731–2740, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Shirasawa, N. Fujiwara, S. Hirabayashi et al., “Receptor for advanced glycation end-products is a marker of type I lung alveolar cells,” Genes to Cells, vol. 9, no. 2, pp. 165–174, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Neeper, A. M. Schmidt, J. Brett et al., “Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins,” The Journal of Biological Chemistry, vol. 267, no. 21, pp. 14998–15004, 1992. View at Google Scholar · View at Scopus
  24. M. Jabaudon, E. Futier, L. Roszyk, V. Sapin, B. Pereira, and J. Constantin, “Association between intraoperative ventilator settings and plasma levels of soluble receptor for advanced glycation end-products in patients without pre-existing lung injury,” Respirology, vol. 20, no. 7, pp. 1131–1138, 2015. View at Publisher · View at Google Scholar
  25. L. G. Dobbs, R. F. Gonzalez, L. Allen, and D. K. Froh, “HTI56, an integral membrane protein specific to human alveolar type I cells,” Journal of Histochemistry & Cytochemistry, vol. 47, pp. 129–137, 1999. View at Google Scholar
  26. L. G. Dobbs, M. C. Williams, and R. Gonzalez, “Monoclonal antibodies specific to apical surfaces of rat alveolar type I cells bind to surfaces of cultured, but not freshly isolated, type II cells,” Molecular Cell Research, vol. 970, no. 2, pp. 146–156, 1988. View at Publisher · View at Google Scholar · View at Scopus
  27. I. W. Cheng, L. B. Ware, K. E. Greene, T. J. Nuckton, M. D. Eisner, and M. A. Matthay, “Prognostic value of surfactant proteins A and D in patients with acute lung injury,” Critical Care Medicine, vol. 31, no. 1, pp. 20–27, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Agrawal, H. Zhuo, S. Brady et al., “Pathogenetic and predictive value of biomarkers in patients with ALI and lower severity of illness: results from two clinical trials,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 303, no. 8, pp. L634–L639, 2012. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Sato, M. E. J. Callister, S. Mumby et al., “KL-6 levels are elevated in plasma from patients with acute respiratory distress syndrome,” European Respiratory Journal, vol. 23, no. 1, pp. 142–145, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. R. M. Determann, A. A. N. M. Royakkers, J. J. Haitsma et al., “Plasma levels of surfactant protein D and KL-6 for evaluation of lung injury in critically ill mechanically ventilated patients,” BMC Pulmonary Medicine, vol. 10, article 6, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Broeckaert and A. Bernard, “Clara cell secretory protein (CC16): characteristics and perspectives as lung peripheral biomarker,” Clinical and Experimental Allergy, vol. 30, no. 4, pp. 469–475, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. R. Cartin-Ceba, R. D. Hubmayr, R. Qin et al., “Predictive value of plasma biomarkers for mortality and organ failure development in patients with acute respiratory distress syndrome,” Journal of Critical Care, vol. 30, no. 1, pp. 219.e1–219.e7, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Eklund and P. Saharinen, “Angiopoietin signaling in the vasculature,” Experimental Cell Research, vol. 319, no. 9, pp. 1271–1280, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. S. Calfee, D. Gallagher, J. Abbott, B. T. Thompson, and M. A. Matthay, “Plasma angiopoietin-2 in clinical acute lung injury: prognostic and pathogenetic significance,” Critical Care Medicine, vol. 40, no. 6, pp. 1731–1737, 2012. View at Publisher · View at Google Scholar · View at Scopus
  35. M. L. Dustin, R. Rothlein, A. K. Bhan, C. A. Dinarello, and T. A. Springer, “Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1),” The Journal of Immunology, vol. 137, no. 1, pp. 245–254, 1986. View at Google Scholar
  36. R. P. McEver, “Selectins: lectins that initiate cell adhesion under flow,” Current Opinion in Cell Biology, vol. 14, no. 5, pp. 581–586, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. D. Osaka, Y. Shibata, K. Kanouchi et al., “Soluble endothelial selectin in acute lung injury complicated by severe pneumonia,” International Journal of Medical Sciences, vol. 8, no. 4, pp. 302–308, 2011. View at Google Scholar · View at Scopus
  38. M. Shibuya, “Vascular endothelial growth factor and its receptor system: physiological functions in angiogenesis and pathological roles in various diseases,” Journal of Biochemistry, vol. 153, no. 1, pp. 13–19, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. L. B. Ware, R. J. Kaner, R. G. Crystal et al., “VEGF levels in the alveolar compartment do not distinguish between ARDS and hydrostatic pulmonary oedama,” European Respiratory Journal, vol. 26, no. 1, pp. 101–105, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. L. B. Ware, M. D. Eisner, B. T. Thompson, P. E. Parsons, and M. A. Matthay, “Significance of von Willebrand factor in septic and nonseptic patients with acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 170, no. 7, pp. 766–772, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. A. J. Reininger, “Function of von Willebrand factor in haemostasis and thrombosis,” Haemophilia, vol. 14, supplement 5, pp. 11–26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. M. S. Bajaj and S. M. Tricomi, “Plasma levels of the three endothelial-specific proteins von Willebrand factor, tissue factor pathway inhibitor, and thrombomodulin do not predict the development of acute respiratory distress syndrome,” Intensive Care Medicine, vol. 25, no. 11, pp. 1259–1266, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. J. Tzu and M. P. Marinkovich, “Bridging structure with function: structural, regulatory, and developmental role of laminins,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 2, pp. 199–214, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Torii, K.-I. Iida, Y. Miyazaki et al., “Higher concentrations of matrix metalloproteinases in bronchoalveolar lavage fluid of patients with adult respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 1, pp. 43–46, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. E. G. Cleary and M. A. Gibson, “Elastic tissue, elastin and elastin associated microfibrils,” in Extracellular Matrix, vol. 2, pp. 95–140, Harwood Academic Publishers, Amsterdam, The Netherlands, 1996. View at Google Scholar
  46. D. E. McClintock, B. Starcher, M. D. Eisner et al., “Higher urine desmosine levels are associated with mortality in patients with acute lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 291, no. 4, pp. L566–L571, 2006. View at Publisher · View at Google Scholar
  47. J. Hästbacka, R. Linko, T. Tervahartiala et al., “Serum MMP-8 and TIMP-1 in critically ill patients with acute respiratory failure: TIMP-1 is associated with increased 90-day mortality,” Anesthesia & Analgesia, vol. 118, no. 4, pp. 790–798, 2014. View at Publisher · View at Google Scholar · View at Scopus
  48. A. H. Hergrueter, K. Nguyen, and C. A. Owen, “Matrix metalloproteinases: all the RAGE in the acute respiratory distress syndrome,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 300, no. 4, pp. L512–L515, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. N. Yamakawa, T. Uchida, M. A. Matthay, and K. Makita, “Proteolytic release of the receptor for advanced glycation end products from in vitro and in situ alveolar epithelial cells,” The American Journal of Physiology— Lung Cellular and Molecular Physiology, vol. 300, no. 4, pp. L516–L525, 2011. View at Google Scholar
  50. T. Strowig, J. Henao-Mejia, E. Elinav, and R. Flavell, “Inflammasomes in health and disease,” Nature, vol. 481, no. 7381, pp. 278–286, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Makabe, M. Kojika, G. Takahashi et al., “Interleukin-18 levels reflect the long-term prognosis of acute lung injury and acute respiratory distress syndrome,” Journal of Anesthesia, vol. 26, no. 5, pp. 658–663, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Cohen, “The immunopathogenesis of sepsis,” Nature, vol. 420, no. 6917, pp. 885–891, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Bouros, M. G. Alexandrakis, K. M. Antoniou et al., “The clinical significance of serum and bronchoalveolar lavage inflammatory cytokines in patients at risk for Acute Respiratory Distress Syndrome,” BMC Pulmonary Medicine, vol. 4, article 6, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. P. E. Parsons, M. A. Matthay, L. B. Ware, and M. D. Eisner, “Elevated plasma levels of soluble TNF receptors are associated with morbidity and mortality in patients with acute lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 288, no. 3, pp. L426–L431, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. G. U. Meduri, S. Headley, G. Kohler et al., “Persistent elevation of inflammatory cytokines predicts a poor outcome in ARDS: plasma IL-1β and IL-6 levels are consistent and efficient predictors of outcome over time,” Chest, vol. 107, no. 4, pp. 1062–1073, 1995. View at Publisher · View at Google Scholar · View at Scopus
  56. P. E. Parsons, M. Moss, J. L. Vannice, E. E. Moore, F. A. Moore, and J. E. Repine, “Circulating IL-1ra and IL-10 levels are increased but do not predict the development of acute respiratory distress syndrome in at-risk patients,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 4, pp. 1469–1473, 1997. View at Publisher · View at Google Scholar · View at Scopus
  57. M. A. Kovach, K. A. Stringer, R. Bunting et al., “Microarray analysis identifies IL-1 receptor type 2 as a novel candidate biomarker in patients with acute respiratory distress syndrome,” Respiratory Research, vol. 16, article 29, 2015. View at Publisher · View at Google Scholar
  58. R. G. Brower, P. N. Lanken, N. MacIntyre et al., “Higher versus lower positive end-expiratory pressures in patients with the acute respiratory distress syndrome,” The New England Journal of Medicine, vol. 351, no. 4, pp. 327–336, 2004. View at Publisher · View at Google Scholar · View at Scopus
  59. P. E. Parsons, M. D. Eisner, B. T. Thompson et al., “Lower tidal volume ventilation and plasma cytokine markers of inflammation in patients with acute lung injury,” Critical Care Medicine, vol. 33, no. 1, pp. 1–6, 2005. View at Publisher · View at Google Scholar · View at Scopus
  60. D. F. Fiorentino, A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra, “IL-10 inhibits cytokine production by activated macrophages,” Journal of Immunology, vol. 147, no. 11, pp. 3815–3822, 1991. View at Google Scholar · View at Scopus
  61. L. Armstrong and A. B. Millar, “Relative production of tumour necrosis factor and interleukin 10 in adult respiratory distress syndrome,” Thorax, vol. 52, no. 5, pp. 442–446, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. M. J. Cohen, K. Brohi, C. S. Calfee et al., “Early release of high mobility group box nuclear protein 1 after severe trauma in humans: role of injury severity and tissue hypoperfusion,” Critical Care, vol. 13, no. 6, article R174, 2009. View at Publisher · View at Google Scholar
  63. T. Nakamura, E. Sato, N. Fujiwara, Y. Kawagoe, S. Maeda, and S.-I. Yamagishi, “Increased levels of soluble receptor for advanced glycation end products (sRAGE) and high mobility group box 1 (HMGB1) are associated with death in patients with acute respiratory distress syndrome,” Clinical Biochemistry, vol. 44, no. 8-9, pp. 601–604, 2011. View at Publisher · View at Google Scholar · View at Scopus
  64. T. R. Martin, G. D. Rubenfeld, J. T. Ruzinski et al., “Relationship between soluble CD14, lipopolysaccharide binding protein, and the alveolar inflammatory response in patients with acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 155, no. 3, pp. 937–944, 1997. View at Publisher · View at Google Scholar · View at Scopus
  65. J. Villar, L. Pérez-Méndez, E. Espinosa et al., “Serum lipopolysaccharide binding protein levels predict severity of lung injury and mortality in patients with severe sepsis,” PLoS ONE, vol. 4, no. 8, Article ID e6818, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. C. Sittipunt, K. P. Steinberg, J. T. Ruzinski et al., “Nitric oxide and nitrotyrosine in the lungs of patients with acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 2, pp. 503–510, 2001. View at Publisher · View at Google Scholar · View at Scopus
  67. L. B. Ware, J. A. Magarik, N. Wickersham et al., “Low plasma citrulline levels are associated with acute respiratory distress syndrome in patients with severe sepsis,” Critical Care, vol. 17, article R10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  68. E. K. Bajwa, U. A. Khan, J. L. Januzzi, M. N. Gong, B. T. Thompson, and D. C. Christiani, “Plasma C-reactive protein levels are associated with improved outcome in ARDS,” Chest, vol. 136, no. 2, pp. 471–480, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. S. H. Hoeboer, H. M. Oudemans-van Straaten, and A. B. J. Groeneveld, “Albumin rather than C-reactive protein may be valuable in predicting and monitoring the severity and course of acute respiratory distress syndrome in critically ill patients with or at risk for the syndrome after new onset fever,” BMC Pulmonary Medicine, vol. 15, article 22, 2015. View at Publisher · View at Google Scholar
  70. I. R. Doyle, C. Hermans, A. Bernard, T. E. Nicholas, and A. D. Bersten, “Clearance of clara cell secretory protein 16 (CC16) and surfactant proteins A and B from blood in acute respiratory failure,” American Journal of Respiratory and Critical Care Medicine, vol. 158, no. 5, pp. 1528–1535, 1998. View at Publisher · View at Google Scholar · View at Scopus
  71. L. B. Ware, J. A. Bastarache, and L. Wang, “Coagulation and fibrinolysis in human acute lung injury—new therapeutic targets?” Keio Journal of Medicine, vol. 54, no. 3, pp. 142–149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. P. Prabhakaran, L. B. Ware, K. E. White, M. T. Cross, M. A. Matthay, and M. A. Olman, “Elevated levels of plasminogen activator inhibitor-1 in pulmonary edema fluid are associated with mortality in acute lung injury,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 285, no. 1, pp. L20–L28, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. L. B. Ware, X. Fang, and M. A. Matthay, “Protein C and thrombomodulin in human acute lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 285, no. 3, pp. L514–L521, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Sapru, C. S. Calfee, K. D. Liu et al., “Plasma soluble thrombomodulin levels are associated with mortality in the acute respiratory distress syndrome,” Intensive Care Medicine, vol. 41, pp. 470–478, 2015. View at Publisher · View at Google Scholar · View at Scopus
  75. A. Koutsi, A. Papapanagiotou, and A. G. Papavassiliou, “Thrombomodulin: from haemostasis to inflammation and tumourigenesis,” International Journal of Biochemistry and Cell Biology, vol. 40, no. 9, pp. 1669–1673, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. E. M. Conway, “Thrombomodulin and its role in inflammation,” Seminars in Immunopathology, vol. 34, no. 1, pp. 107–125, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. W. Ruf and M. Riewald, “Tissue factor-dependent coagulation protease signaling in acute lung injury,” Critical Care Medicine, vol. 31, no. 4, pp. S231–S237, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Xue, Z. Sun, M. Shao et al., “Diagnostic and prognostic utility of tissue factor for severe sepsis and sepsis-induced acute lung injury,” Journal of Translational Medicine, vol. 13, article 172, 2015. View at Publisher · View at Google Scholar
  79. J. A. Bastarache, S. C. Sebag, J. K. Clune et al., “Low levels of tissue factor lead to alveolar haemorrhage, potentiating murine acute lung injury and oxidative stress,” Thorax, vol. 67, no. 12, pp. 1032–1039, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Mumby, L. Ramakrishnan, T. W. Evans, M. J. D. Griffiths, and G. J. Quinlan, “Methemoglobin-induced signaling and chemokine responses in human alveolar epithelial cells,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 306, no. 1, pp. L88–L100, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. A. Fein, R. F. Grossman, J. G. Jones et al., “The value of edema fluid protein measurement in patients with pulmonary edema,” The American Journal of Medicine, vol. 67, no. 1, pp. 32–38, 1979. View at Publisher · View at Google Scholar · View at Scopus
  82. L. B. Ware, R. D. Fremont, J. A. Bastarache, C. S. Calfee, and M. A. Matthay, “Determining the aetiology of pulmonary oedema by the oedema fluid-to-plasma protein ratio,” European Respiratory Journal, vol. 35, no. 2, pp. 331–337, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. D. R. Thickett, L. Armstrong, S. J. Christie, and A. B. Millar, “Vascular endothelial growth factor may contribute to increased vascular permeability in acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 9, pp. 1601–1605, 2001. View at Publisher · View at Google Scholar · View at Scopus
  84. Y. Abadie, F. Bregeon, L. Papazian et al., “Decreased VEGF concentration in lung tissue and vascular injury during ARDS,” European Respiratory Journal, vol. 25, no. 1, pp. 139–146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  85. T. J. Desai and W. V. Cardoso, “Growth factors in lung development and disease: friends or foe?” Respiratory Research, vol. 3, article 2, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Maitre, S. Boussat, D. Jean et al., “Vascular endothelial growth factor synthesis in the acute phase of experimental and clinical lung injury,” European Respiratory Journal, vol. 18, no. 1, pp. 100–106, 2001. View at Publisher · View at Google Scholar · View at Scopus
  87. Z. Borok, S. I. Danto, L. L. Dimen, X.-L. Zhang, and R. L. Lubman, “Na+-K+-ATPase expression in alveolar epithelial cells: upregulation of active ion transport by KGF,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 274, no. 1, pp. L149–L158, 1998. View at Google Scholar · View at Scopus
  88. L. B. Ware and M. A. Matthay, “Keratinocyte and hepatocyte growth factors in the lung: Roles in lung development, inflammation, and repair,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 282, no. 5, pp. L924–L940, 2002. View at Publisher · View at Google Scholar · View at Scopus
  89. V. Galani, E. Tatsaki, M. Bai et al., “The role of apoptosis in the pathophysiology of Acute Respiratory Distress Syndrome (ARDS): an up-to-date cell-specific review,” Pathology Research and Practice, vol. 206, no. 3, pp. 145–150, 2010. View at Publisher · View at Google Scholar · View at Scopus
  90. R. C. Pires-Neto, M. M. B. Morales, T. Lancas et al., “Expression of acute-phase cytokines, surfactant proteins, and epithelial apoptosis in small airways of human acute respiratory distress syndrome,” Journal of Critical Care, vol. 28, no. 1, pp. 111.e9–111.e15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. D. Talmor, T. Sarge, A. Legedza et al., “Cytokine release following recruitment maneuvers,” Chest, vol. 132, no. 5, pp. 1434–1439, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. J. M. Walter, J. Wilson, and L. B. Ware, “Biomarkers in acute respiratory distress syndrome: from pathobiology to improving patient care,” Expert Review of Respiratory Medicine, vol. 8, no. 5, pp. 573–586, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. C. S. Calfee, K. Delucchi, P. E. Parsons, B. T. Thompson, L. B. Ware, and M. A. Matthay, “Latent class models identify two subphenotypes in respiratory distress syndrome with differential response to positive end-expiratory pressure,” Annals of the American Thoracic Society, vol. 12, supplement 1, p. S77, 2015. View at Publisher · View at Google Scholar
  94. V. Newman, R. F. Gonzalez, M. A. Matthay, and L. G. Dobbs, “A novel alveolar type I cell-specific biochemical marker of human acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 161, no. 3, pp. 990–995, 2000. View at Publisher · View at Google Scholar · View at Scopus
  95. A. M. Schmidt, S. D. Yan, S. F. Yan, and D. M. Stern, “The biology of the receptor for advanced glycation end products and its ligands,” Biochimica et Biophysica Acta (BBA)—Molecular Cell Research, vol. 1498, no. 2-3, pp. 99–111, 2000. View at Publisher · View at Google Scholar · View at Scopus
  96. T. Uchida, M. Shirasawa, L. B. Ware et al., “Receptor for advanced glycation end-products is a marker of type I cell injury in acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 173, no. 9, pp. 1008–1015, 2006. View at Publisher · View at Google Scholar · View at Scopus
  97. M. T. Kuipers, T. van der Poll, M. J. Schultz, and C. W. Wieland, “Bench-to-bedside review: damage-associated molecular patterns in the onset of ventilator-induced lung injury,” Critical Care, vol. 15, no. 6, article 235, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. T. Uchida, M. Shirasawa, L. B. Ware et al., “Receptor for advanced glycation end-products is a marker of type I cell injury in acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 173, no. 9, pp. 1008–1015, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. C. S. Calfee, L. B. Ware, M. D. Eisner et al., “Plasma receptor for advanced glycation end products and clinical outcomes in acute lung injury,” Thorax, vol. 63, no. 12, pp. 1083–1089, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Jabaudon, E. Futier, L. Roszyk et al., “Soluble form of the receptor for advanced glycation end products is a marker of acute lung injury but not of severe sepsis in critically ill patients,” Critical Care Medicine, vol. 39, no. 3, pp. 480–488, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. M. Jabaudon, R. Blondonnet, L. Roszyk et al., “Soluble RAGE predicts impaired alveolar fluid clearance in acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 192, no. 2, 2015. View at Publisher · View at Google Scholar
  102. M. D. Johnson, J. H. Widdicombe, L. Allen, P. Barbry, and L. G. Dobbs, “Alveolar epithelial I cells contain transport proteins and transport sodium, supporting an active role for type I cells in regulation of lung liquid homeostasis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 1966–1971, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. L. E. Hanford, J. J. Enghild, Z. Valnickova et al., “Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE),” The Journal of Biological Chemistry, vol. 279, no. 48, pp. 50019–50024, 2004. View at Publisher · View at Google Scholar · View at Scopus
  104. C. Cheng, K. Tsuneyama, R. Kominami et al., “Expression profiling of endogenous secretory receptor for advanced glycation end products in human organs,” Modern Pathology, vol. 18, no. 10, pp. 1385–1396, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. J. Brett, A. M. Schmidt, S. D. Yan et al., “Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues,” The American Journal of Pathology, vol. 143, no. 6, pp. 1699–1712, 1993. View at Google Scholar · View at Scopus
  106. L. E. Hanford, C. L. Fattman, L. M. Schaefer, J. J. Enghild, Z. Valnickova, and T. D. Oury, “Regulation of receptor for advanced glycation end products during bleomycin-induced lung injury,” American Journal of Respiratory Cell and Molecular Biology, vol. 29, no. 3, pp. S77–S81, 2003. View at Google Scholar · View at Scopus
  107. J. M. Englert, L. E. Hanford, N. Kaminski et al., “A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis,” The American Journal of Pathology, vol. 172, no. 3, pp. 583–591, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. A. M. Schmidt, S. D. Yan, S. F. Yan, and D. M. Stern, “The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses,” The Journal of Clinical Investigation, vol. 108, no. 7, pp. 949–955, 2001. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Jabaudon, R. Blondonnet, L. Roszyk et al., “Soluble forms and ligands of the receptor for advanced glycation end-products in patients with acute respiratory distress syndrome: an observational prospective study,” PLoS ONE, vol. 10, no. 8, Article ID e0135857, 2015. View at Publisher · View at Google Scholar
  110. C. A. Downs, L. H. Kreiner, N. M. Johnson, L. A. Brown, and M. N. Helms, “Receptor for advanced glycation end-products regulates lung fluid balance via protein kinase C-gp91phox signaling to epithelial sodium channels,” American Journal of Respiratory Cell and Molecular Biology, vol. 52, no. 1, pp. 75–87, 2015. View at Publisher · View at Google Scholar
  111. R. Briot, J. A. Frank, T. Uchida, J. W. Lee, C. S. Calfee, and M. A. Matthay, “Elevated levels of the receptor for advanced glycation end products, a marker of alveolar epithelial type i cell injury, predict impaired alveolar fluid clearance in isolated perfused human lungs,” Chest, vol. 135, no. 2, pp. 269–275, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. J.-M. Constantin, “Impact of Inflammation Biomarkers on the Acute Respiratory Distress Syndrome (ARDS) Definition,” (NCT01161901), https://clinicaltrials.gov/ct2/show/NCT01161901?term=constantin+clermont&rank=5.
  113. M. Jabaudon, N. Hamroun, L. Roszyk et al., “Effects of a recruitment maneuver on plasma levels of soluble RAGE in patients with diffuse acute respiratory distress syndrome: a prospective randomized crossover study,” Intensive Care Medicine, vol. 41, no. 5, pp. 846–855, 2015. View at Publisher · View at Google Scholar
  114. M. Jabaudon, “Predictive Values of Plasma Soluble RAGE Levels and RAGE Polymorphisms for the Onset of Acute Respiratory Distress Syndrome in Critically Ill Patients (PrediRAGE Study),” in: ClinicalTrials.gov, 2014, http://clinicaltrials.gov/show/NCT02070536.
  115. J. Bhattacharya and M. A. Matthay, “Regulation and repair of the alveolar-capillary barrier in acute lung injury,” Annual Review of Physiology, vol. 75, pp. 593–615, 2013. View at Publisher · View at Google Scholar · View at Scopus
  116. I. Frerking, A. Günther, W. Seeger, and U. Pison, “Pulmonary surfactant: functions, abnormalities and therapeutic options,” Intensive Care Medicine, vol. 27, no. 11, pp. 1699–1717, 2001. View at Publisher · View at Google Scholar · View at Scopus
  117. D. G. Ashbaugh, D. B. Bigelow, T. L. Petty, and B. E. Levine, “Acute respiratory distress in adults,” The Lancet, vol. 2, no. 7511, pp. 319–323, 1967. View at Google Scholar · View at Scopus
  118. I. R. Doyle, A. D. Bersten, and T. E. Nicholas, “Surfactant proteins-A and -B are elevated in plasma of patients with acute respiratory failure,” American Journal of Respiratory and Critical Care Medicine, vol. 156, no. 4, pp. 1217–1229, 1997. View at Publisher · View at Google Scholar · View at Scopus
  119. K. E. Greene, S. Ye, R. J. Mason, and P. E. Parsons, “Serum surfactant protein-A levels predict development of ARDS in at-risk patients,” Chest, vol. 116, supplement 1, pp. 90S–91S, 1999. View at Publisher · View at Google Scholar · View at Scopus
  120. A. D. Bersten, T. Hunt, T. E. Nicholas, and I. R. Doyle, “Elevated plasma surfactant protein-B predicts development of acute respiratory distress syndrome in patients with acute respiratory failure,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 4, pp. 648–652, 2001. View at Publisher · View at Google Scholar · View at Scopus
  121. A. Ishizaka, T. Matsuda, K. H. Albertine et al., “Elevation of KL-6, a lung epithelial cell marker, in plasma and epithelial lining fluid in acute respiratory distress syndrome,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 286, no. 6, pp. L1088–L1094, 2004. View at Publisher · View at Google Scholar · View at Scopus
  122. N. Nathani, G. D. Perkins, W. Tunnicliffe, N. Murphy, M. Manji, and D. R. Thickett, “Kerbs von Lungren 6 antigen is a marker of alveolar inflammation but not of infection in patients with acute respiratory distress syndrome,” Critical Care, vol. 12, article R12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. T. Kondo, N. Hattori, N. Ishikawa et al., “KL-6 concentration in pulmonary epithelial lining fluid is a useful prognostic indicator in patients with acute respiratory distress syndrome,” Respiratory Research, vol. 12, article 32, 2011. View at Publisher · View at Google Scholar · View at Scopus
  124. R. Lucas, A. D. Verin, S. M. Black, and J. D. Catravas, “Regulators of endothelial and epithelial barrier integrity and function in acute lung injury,” Biochemical Pharmacology, vol. 77, no. 12, pp. 1763–1772, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Binnie, J. L. Tsang, and C. C. dos Santos, “Biomarkers in acute respiratory distress syndrome,” Current Opinion in Critical Care, vol. 20, no. 1, pp. 47–55, 2014. View at Publisher · View at Google Scholar
  126. S. Tsigkos, M. Koutsilieris, and A. Papapetropoulos, “Angiopoietins in angiogenesis and beyond,” Expert Opinion on Investigational Drugs, vol. 12, no. 6, pp. 933–941, 2003. View at Publisher · View at Google Scholar · View at Scopus
  127. U. Fiedler, Y. Reiss, M. Scharpfenecker et al., “Angiopoietin-2 sensitizes endothelial cells to TNF-α and has a crucial role in the induction of inflammation,” Nature Medicine, vol. 12, no. 2, pp. 235–239, 2006. View at Publisher · View at Google Scholar · View at Scopus
  128. V. Bhandari and J. A. Elias, “The role of angiopoietin 2 in hyperoxia-induced acute lung injury,” Cell Cycle, vol. 6, no. 9, pp. 1049–1052, 2007. View at Publisher · View at Google Scholar · View at Scopus
  129. N. J. Meyer, M. Li, R. Feng et al., “ANGPT2 genetic variant is associated with trauma-associated acute lung injury and altered plasma angiopoietin-2 isoform ratio,” American Journal of Respiratory and Critical Care Medicine, vol. 183, no. 10, pp. 1344–1353, 2011. View at Publisher · View at Google Scholar · View at Scopus
  130. A. Agrawal, M. A. Matthay, K. N. Kangelaris et al., “Plasma angiopoietin-2 predicts the onset of acute lung injury in critically ill patients,” American Journal of Respiratory and Critical Care Medicine, vol. 187, no. 7, pp. 736–742, 2013. View at Publisher · View at Google Scholar · View at Scopus
  131. T. Wada, S. Jesmin, S. Gando et al., “The role of angiogenic factors and their soluble receptors in acute lung injury (ALI)/ acute respiratory distress syndrome (ARDS) associated with critical illness,” Journal of Inflammation, vol. 10, article 6, 2013. View at Publisher · View at Google Scholar
  132. T. Ong, D. E. McClintock, R. H. Kallet, L. B. Ware, M. A. Matthay, and K. D. Liu, “Ratio of angiopoietin-2 to angiopoietin-1 as a predictor of mortality in acute lung injury patients,” Critical Care Medicine, vol. 38, no. 9, pp. 1845–1851, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. K. A. Roebuck and A. Finnegan, “Regulation of intercellular adhesion molecule-1 (CD54) gene expression,” Journal of Leukocyte Biology, vol. 66, no. 6, pp. 876–888, 1999. View at Google Scholar · View at Scopus
  134. E. R. Conner, L. B. Ware, G. Modin, and M. A. Matthay, “Elevated pulmonary edema fluid concentrations of soluble intercellular adhesion molecule-1 in patients with acute lung injury: biological and clinical significance,” Chest, vol. 116, pp. 83S–84S, 1999. View at Publisher · View at Google Scholar · View at Scopus
  135. C. S. Calfee, M. D. Eisner, P. E. Parsons et al., “Soluble intercellular adhesion molecule-1 and clinical outcomes in patients with acute lung injury,” Intensive Care Medicine, vol. 35, no. 2, pp. 248–257, 2009. View at Publisher · View at Google Scholar · View at Scopus
  136. P. Agouridakis, D. Kyriakou, M. G. Alexandrakis et al., “The predictive role of serum and bronchoalveolar lavage cytokines and adhesion molecules for acute respiratory distress syndrome development and outcome,” Respiratory Research, vol. 3, article 25, 2002. View at Publisher · View at Google Scholar · View at Scopus
  137. H. R. Flori, L. B. Ware, D. Glidden, and M. A. Matthay, “Early elevation of plasma soluble intercellular adhesion molecule-1 in pediatric acute lung injury identifies patients at increased risk of death and prolonged mechanical ventilation,” Pediatric Critical Care Medicine, vol. 4, no. 3, pp. 315–321, 2003. View at Publisher · View at Google Scholar · View at Scopus
  138. A. Sousa, F. Raposo, S. Fonseca et al., “Measurement of cytokines and adhesion molecules in the first 72 hours after severe trauma: association with severity and outcome,” Disease Markers, vol. 2015, Article ID 747036, 8 pages, 2015. View at Publisher · View at Google Scholar
  139. S. Gando, T. Kameue, N. Matsuda et al., “Combined activation of coagulation and inflammation has an important role in multiple organ dysfunction and poor outcome after severe trauma,” Thrombosis and Haemostasis, vol. 88, no. 6, pp. 943–949, 2002. View at Google Scholar · View at Scopus
  140. K. Xing, S. Murthy, W. C. Liles, and J. M. Singh, “Clinical utility of biomarkers of endothelial activation in sepsis-a systematic review,” Critical Care, vol. 16, article R7, 2012. View at Publisher · View at Google Scholar · View at Scopus
  141. J. Boldt, M. Wollbrück, D. Kuhn, L. C. Linke, and G. Hempelmann, “Do plasma levels of circulating soluble adhesion molecules differ between surviving and nonsurviving critically ill patients?” Chest, vol. 107, no. 3, pp. 787–792, 1995. View at Publisher · View at Google Scholar · View at Scopus
  142. F. Sakamaki, A. Ishizaka, M. Handa et al., “Soluble form of P-selectin in plasma is elevated in acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 6, pp. 1821–1826, 1995. View at Publisher · View at Google Scholar · View at Scopus
  143. E. L. Burnham, M. Moss, F. Harris, and L. A. S. Brown, “Elevated plasma and lung endothelial selectin levels in patients with acute respiratory distress syndrome and a history of chronic alcohol abuse,” Critical Care Medicine, vol. 32, no. 3, pp. 675–679, 2004. View at Publisher · View at Google Scholar · View at Scopus
  144. K. Okajima, N. Harada, G. Sakurai et al., “Rapid assay for plasma soluble E-selectin predicts the development of acute respiratory distress syndrome in patients with systemic inflammatory response syndrome,” Translational Research, vol. 148, no. 6, pp. 295–300, 2006. View at Publisher · View at Google Scholar · View at Scopus
  145. A. R. L. Medford and A. B. Millar, “Vascular endothelial growth factor (VEGF) in acute lung injury (ALI) and acute respiratory distress syndrome (ARDS): paradox or paradigm?” Thorax, vol. 61, no. 7, pp. 621–626, 2006. View at Publisher · View at Google Scholar · View at Scopus
  146. M. Shibuya, “Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis,” Journal of Biochemistry and Molecular Biology, vol. 39, no. 5, pp. 469–478, 2006. View at Publisher · View at Google Scholar · View at Scopus
  147. R. J. Kaner, J. V. Ladetto, R. Singh, N. Fukuda, M. A. Matthay, and R. G. Crystal, “Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema,” American Journal of Respiratory Cell and Molecular Biology, vol. 22, no. 6, pp. 657–664, 2000. View at Publisher · View at Google Scholar · View at Scopus
  148. L. Azamfirei, S. Gurzu, R. Solomon et al., “Vascular endothelial growth factor: a possible mediator of endothelial activation in acute respiratory distress syndrome,” Minerva Anestesiologica, vol. 76, no. 8, pp. 609–616, 2010. View at Google Scholar · View at Scopus
  149. D. R. Thickett, L. Armstrong, and A. B. Millar, “A role for vascular endothelial growth factor in acute and resolving lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 166, no. 10, pp. 1332–1337, 2002. View at Publisher · View at Google Scholar · View at Scopus
  150. A. C. A. Carvalho, S. M. Bellman, V. J. Saullo, D. Quinn, and W. M. Zapol, “Altered factor VIII in acute respiratory failure,” The New England Journal of Medicine, vol. 307, no. 18, pp. 1113–1119, 1982. View at Publisher · View at Google Scholar · View at Scopus
  151. D. B. Rubin, J. P. Wiener-Kronish, J. F. Murray et al., “Elevated von Willebrand factor antigen is an early plasma predictor of acute lung injury in nonpulmonary sepsis syndrome,” Journal of Clinical Investigation, vol. 86, no. 2, pp. 474–480, 1990. View at Publisher · View at Google Scholar · View at Scopus
  152. M. Moss, L. Ackerson, M. K. Gillespie, F. A. Moore, E. E. Moore, and P. E. Parsons, “Von willebrand factor antigen levels are not predictive for the adult respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 1, pp. 15–20, 1995. View at Publisher · View at Google Scholar · View at Scopus
  153. A. K. Sabharwal, S. P. Bajaj, A. Ameri et al., “Tissue factor pathway inhibitor and von Willebrand factor antigen levels in adult respiratory distress syndrome and in a primate model of sepsis,” American Journal of Respiratory and Critical Care Medicine, vol. 151, no. 3 I, pp. 758–767, 1995. View at Publisher · View at Google Scholar · View at Scopus
  154. P. R. M. Rocco, C. Dos Santos, and P. Pelosi, “Lung parenchyma remodeling in acute respiratory distress syndrome,” Minerva Anestesiologica, vol. 75, no. 12, pp. 730–740, 2009. View at Google Scholar · View at Scopus
  155. B. C. Starcher, “Lung elastin and matrix,” Chest, vol. 117, no. 5, supplement 1, pp. 229S–234S, 2000. View at Google Scholar · View at Scopus
  156. G. M. Albaiceta, A. Gutierrez-Fernández, E. García-Prieto et al., “Absence or inhibition of matrix metalloproteinase-8 decreases ventilator-induced lung injury,” American Journal of Respiratory Cell and Molecular Biology, vol. 43, no. 5, pp. 555–563, 2010. View at Publisher · View at Google Scholar · View at Scopus
  157. S. E. G. Fligiel, T. Standiford, H. M. Fligiel et al., “Matrix metalloproteinases and matrix metalloproteinase inhibitors in acute lung injury,” Human Pathology, vol. 37, no. 4, pp. 422–430, 2006. View at Publisher · View at Google Scholar · View at Scopus
  158. M. Y. F. Kong, Y. Li, R. Oster, A. Gaggar, and J. P. Clancy, “Early elevation of matrix metalloproteinase-8 and -9 in pediatric ARDS is associated with an increased risk of prolonged mechanical ventilation,” PLoS ONE, vol. 6, no. 8, Article ID e22596, 2011. View at Publisher · View at Google Scholar · View at Scopus
  159. A. González-López and G. M. Albaiceta, “Repair after acute lung injury: molecular mechanisms and therapeutic opportunities,” Critical Care, vol. 16, no. 2, article 209, 2012. View at Publisher · View at Google Scholar · View at Scopus
  160. M. Bhatia and S. Moochhala, “Role of inflammatory mediators in the pathophysiology of acute respiratory distress syndrome,” Journal of Pathology, vol. 202, no. 2, pp. 145–156, 2004. View at Publisher · View at Google Scholar · View at Scopus
  161. L. A. Dada and J. I. Sznajder, “Hypoxic inhibition of alveolar fluid reabsorption,” in Hypoxia and the Circulation, pp. 159–168, Springer US, 2007. View at Google Scholar
  162. A. E. Postlethwaite and J. M. Seyer, “Stimulation of fibroblast chemotaxis by human recombinant tumor necrosis factor α (TNF-α) and a synthetic TNF-α31-68 peptide,” The Journal of Experimental Medicine, vol. 172, no. 6, pp. 1749–1756, 1990. View at Publisher · View at Google Scholar · View at Scopus
  163. P. F. Piguet, M. A. Collart, G. E. Grau, A.-P. Sappino, and P. Vassalli, “Requirement of tumour necrosis factor for development of silica-induced pulmonary fibrosis,” Nature, vol. 344, no. 6263, pp. 245–247, 1990. View at Publisher · View at Google Scholar · View at Scopus
  164. W. Y. Park, R. B. Goodman, K. P. Steinberg et al., “Cytokine balance in the lungs of patients with acute respiratory distress syndrome,” American Journal of Respiratory and Critical Care Medicine, vol. 164, no. 10, pp. 1896–1903, 2001. View at Publisher · View at Google Scholar · View at Scopus
  165. J. Pugin, B. Ricou, K. P. Steinberg, P. M. Suter, and T. R. Martin, “Proinflammatory activity in bronchoalveolar lavage fluids from patients with ARDS, a prominent role for interleukin-1,” American Journal of Respiratory and Critical Care Medicine, vol. 153, no. 6, pp. 1850–1856, 1996. View at Publisher · View at Google Scholar · View at Scopus
  166. G. U. Meduri, G. Kohler, S. Headley, E. Tolley, F. Stentz, and A. Postlethwaite, “Inflammatory cytokines in the BAL of patients with ARDS. Persistent elevation over time predicts poor outcome,” Chest, vol. 108, no. 5, pp. 1303–1314, 1995. View at Publisher · View at Google Scholar · View at Scopus
  167. R. Roten, M. Markert, F. Feihl, M.-D. Schaller, M.-C. Tagan, and C. Perret, “Plasma levels of tumor necrosis factor in the adult respiratory distress syndrome,” American Review of Respiratory Disease, vol. 143, no. 3, pp. 590–592, 1991. View at Publisher · View at Google Scholar · View at Scopus
  168. T. Dolinay, Y. S. Kim, J. Howrylak et al., “Inflammasome-regulated cytokines are critical mediators of acute lung injury,” American Journal of Respiratory and Critical Care Medicine, vol. 185, no. 11, pp. 1225–1234, 2012. View at Publisher · View at Google Scholar · View at Scopus
  169. D. McClintock, H. Zhuo, N. Wickersham, M. A. Matthay, and L. B. Ware, “Biomarkers of inflammation, coagulation and fibrinolysis predict mortality in acute lung injury,” Critical Care, vol. 12, no. 2, article R41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  170. R. P. Baughman, K. L. Gunther, M. C. Rashkin, D. A. Keeton, and E. N. Pattishall, “Changes in the inflammatory response of the lung during acute respiratory distress syndrome: prognostic indicators,” American Journal of Respiratory and Critical Care Medicine, vol. 154, no. 1, pp. 76–81, 1996. View at Publisher · View at Google Scholar · View at Scopus
  171. H. Schütte, J. Lohmeyer, S. Rosseau et al., “Bronchoalveolar and systemic cytokine profiles in patients with ARDS, severe pneumonia and cardiogenic pulmonary oedema,” European Respiratory Journal, vol. 9, no. 9, pp. 1858–1867, 1996. View at Publisher · View at Google Scholar · View at Scopus
  172. A. Kurdowska, E. J. Miller, J. M. Noble et al., “Anti-IL-8 autoantibodies in alveolar fluid from patients with the adult respiratory distress syndrome,” The Journal of Immunology, vol. 157, no. 6, pp. 2699–2706, 1996. View at Google Scholar · View at Scopus
  173. A. Kurdowska, J. M. Noble, I. S. Grant, C. R. Robertson, C. Haslett, and S. C. Donnelly, “Anti-interleukin-8 autoantibodies in patients at risk for acute respiratory distress syndrome,” Critical Care Medicine, vol. 30, no. 10, pp. 2335–2337, 2002. View at Publisher · View at Google Scholar · View at Scopus
  174. A. Krupa, H. Kato, M. A. Matthay, and A. K. Kurdowska, “Proinflammatory activity of anti-IL-8 autoantibody:IL-8 complexes in alveolar edema fluid from patients with acute lung injury,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 286, no. 6, pp. L1105–L1113, 2004. View at Publisher · View at Google Scholar · View at Scopus
  175. R. Fudala, A. Krupa, M. A. Matthay, T. C. Allen, and A. K. Kurdowska, “Anti-IL-8 autoantibody:IL-8 immune complexes suppress spontaneous apoptosis of neutrophils,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 293, no. 2, pp. L364–L374, 2007. View at Publisher · View at Google Scholar · View at Scopus
  176. M. A. Matthay and L. B. Ware, “Resolution of alveolar edema in acute respiratory distress syndrome. Physiology and biology,” American Journal of Respiratory and Critical Care Medicine, vol. 192, no. 2, pp. 124–125, 2015. View at Publisher · View at Google Scholar
  177. P. Ralph, I. Nakoinz, A. Sampson-Johannes et al., “IL-10, T lymphocyte inhibitor of human blood cell production of IL-1 and tumor necrosis factor,” The Journal of Immunology, vol. 148, no. 3, pp. 808–814, 1992. View at Google Scholar · View at Scopus
  178. M. Seitz, P. Loetscher, B. Dewald, H. Towbin, H. Gallati, and M. Baggiolini, “Interleukin-10 differentially regulates cytokine inhibitor and chemokine release from blood mononuclear cells and fibroblasts,” European Journal of Immunology, vol. 25, no. 4, pp. 1129–1132, 1995. View at Publisher · View at Google Scholar · View at Scopus
  179. C.-J. Lo, M. Fu, and H. G. Cryer, “Interleukin 10 inhibits alveolar macrophage production of inflammatory mediators involved in adult respiratory distress syndrome,” Journal of Surgical Research, vol. 79, no. 2, pp. 179–184, 1998. View at Publisher · View at Google Scholar · View at Scopus
  180. A. Sapru, J. L. Wiemels, J. S. Witte, L. B. Ware, and M. A. Matthay, “Acute lung injury and the coagulation pathway: potential role of gene polymorphisms in the protein C and fibrinolytic pathways,” Intensive Care Medicine, vol. 32, no. 9, pp. 1293–1303, 2006. View at Publisher · View at Google Scholar · View at Scopus
  181. V. Jalkanen, R. Yang, R. Linko et al., “SuPAR and PAI-1 in critically ill, mechanically ventilated patients,” Intensive Care Medicine, vol. 39, no. 3, pp. 489–496, 2013. View at Publisher · View at Google Scholar · View at Scopus
  182. L. B. Ware, M. A. Matthay, P. E. Parsons et al., “Pathogenetic and prognostic significance of altered coagulation and fibrinolysis in acute lung injury/acute respiratory distress syndrome,” Critical Care Medicine, vol. 35, no. 8, pp. 1821–1828, 2007. View at Publisher · View at Google Scholar · View at Scopus
  183. C. T. Esmon, “Inflammation and the activated protein C anticoagulant pathway,” Seminars in Thrombosis and Hemostasis, vol. 32, supplement 1, pp. 49–60, 2006. View at Publisher · View at Google Scholar · View at Scopus
  184. M. F. Nold, C. A. Nold-Petry, D. Fischer et al., “Activated protein C downregulates p38 mitogen-activated protein kinase and improves clinical parameters in an in-vivo model of septic shock,” Thrombosis and Haemostasis, vol. 98, no. 5, pp. 1118–1126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  185. T. Cheng, D. Liu, J. H. Griffin et al., “Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective,” Nature Medicine, vol. 9, no. 3, pp. 338–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  186. S. C. Christiaans, B. M. Wagener, C. T. Esmon, and J. F. Pittet, “Protein C and acute inflammation: a clinical and biological perspective,” The American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 305, no. 7, pp. L455–L466, 2013. View at Publisher · View at Google Scholar · View at Scopus
  187. J. A. Bastarache, L. Wang, T. Geiser et al., “The alveolar epithelium can initiate the extrinsic coagulation cascade through expression of tissue factor,” Thorax, vol. 62, no. 7, pp. 608–616, 2007. View at Publisher · View at Google Scholar · View at Scopus
  188. A. J. Ghio, J. H. Richards, K. M. Crissman, and J. D. Carter, “Iron disequilibrium in the rat lung after instilled blood,” Chest, vol. 118, no. 3, pp. 814–823, 2000. View at Publisher · View at Google Scholar · View at Scopus
  189. J. A. Bastarache, J. L. Wynn, and L. B. Ware, “Fanning the fire: can methemoglobin enhance neutrophil activation?” EBioMedicine, vol. 2, no. 3, pp. 184–185, 2015. View at Publisher · View at Google Scholar
  190. E. L. Burnham, W. J. Janssen, D. W. H. Riches, M. Moss, and G. P. Downey, “The fibroproliferative response in acute respiratory distress syndrome: mechanisms and clinical significance,” European Respiratory Journal, vol. 43, no. 1, pp. 276–285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  191. T. Geiser, K. Atabai, P.-H. Jarreau, L. B. Ware, J. Pugin, and M. A. Matthay, “Pulmonary edema fluid from patients with acute lung injury augments in vitro alveolar epithelial repair by an IL-1β-dependent mechanism,” American Journal of Respiratory and Critical Care Medicine, vol. 163, no. 6, pp. 1384–1388, 2001. View at Publisher · View at Google Scholar · View at Scopus
  192. K. Atabai, M. Ishigaki, T. Geiser, I. Ueki, M. A. Matthay, and L. B. Ware, “Keratinocyte growth factor can enhance alveolar epithelial repair by nonmitogenic mechanisms,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 283, no. 1, pp. L163–L169, 2002. View at Publisher · View at Google Scholar · View at Scopus
  193. M. Mura, C. C. dos Santos, D. Stewart, and M. Liu, “Vascular endothelial growth factor and related molecules in acute lung injury,” Journal of Applied Physiology, vol. 97, no. 5, pp. 1605–1617, 2004. View at Publisher · View at Google Scholar · View at Scopus
  194. C. Quesnel, S. Marchand-Adam, A. Fabre et al., “Regulation of hepatocyte growth factor secretion by fibroblasts in patients with acute lung injury,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 294, no. 2, pp. L334–L343, 2008. View at Publisher · View at Google Scholar
  195. S. Fan, Y. X. Ma, J.-A. Wang et al., “The cytokine hepatocyte growth factor/scatter factor inhibits apoptosis and enhances DNA repair by a common mechanism involving signaling through phosphatidyl inositol 3′ kinase,” Oncogene, vol. 19, no. 18, pp. 2212–2223, 2000. View at Publisher · View at Google Scholar · View at Scopus
  196. J.-B. Stern, L. Fierobe, C. Paugam et al., “Keratinocyte growth factor and hepatocyte growth factor in bronchoalveolar lavage fluid in acute respiratory distress syndrome patients,” Critical Care Medicine, vol. 28, no. 7, pp. 2326–2333, 2000. View at Google Scholar · View at Scopus
  197. G. M. Verghese, K. McCormick-Shannon, R. J. Mason, and M. A. Matthay, “Hepatocyte growth factor and keratinocyte growth factor in the pulmonary edema fluid of patients with acute lung injury: biologic and clinical significance,” American Journal of Respiratory and Critical Care Medicine, vol. 158, no. 2, pp. 386–394, 1998. View at Publisher · View at Google Scholar · View at Scopus
  198. M. A. Rahman, K. Sundaram, S. Mitra, M. A. Gavrilin, and M. D. Wewers, “Receptor interacting protein-2 plays a critical role in human lung epithelial cells survival in response to Fas-induced cell-death,” PLoS ONE, vol. 9, no. 3, Article ID e92731, 2014. View at Publisher · View at Google Scholar · View at Scopus
  199. A. D. Lopez, S. Avasarala, S. Grewal, A. K. Murali, and L. London, “Differential role of the Fas/Fas ligand apoptotic pathway in inflammation and lung fibrosis associated with reovirus 1/L-induced bronchiolitis obliterans organizing pneumonia and acute respiratory distress syndrome,” The Journal of Immunology, vol. 183, no. 12, pp. 8244–8257, 2009. View at Publisher · View at Google Scholar · View at Scopus
  200. G. Matute-Bello, W. C. Liles, K. P. Steinberg et al., “Soluble Fas ligand induces epithelial cell apoptosis in humans with acute lung injury (ARDS),” Journal of Immunology, vol. 163, no. 4, pp. 2217–2225, 1999. View at Google Scholar · View at Scopus
  201. M. Tanaka, T. Suda, T. Takahashi, and S. Nagata, “Expression of the functional soluble form of human Fas ligand in activated lymphocytes,” The EMBO Journal, vol. 14, no. 6, pp. 1129–1135, 1995. View at Google Scholar · View at Scopus
  202. K. H. Albertine, M. F. Soulier, Z. Wang 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,” The American Journal of Pathology, vol. 161, no. 5, pp. 1783–1796, 2002. View at Publisher · View at Google Scholar · View at Scopus
  203. J. Farjanel, D. J. Hartmann, B. Guidet, L. Luquel, and G. Offenstadt, “Four markers of collagen metabolism as possible indicators of disease in the adult respiratory distress syndrome,” American Review of Respiratory Disease, vol. 147, no. 5, pp. 1091–1099, 1993. View at Publisher · View at Google Scholar · View at Scopus
  204. A. N. Chesnutt, M. A. Matthay, F. A. Tibayan, and J. G. Clark, “Early detection of type iii procollagen peptide in acute lung injury: pathogenetic and prognostic significance,” American Journal of Respiratory and Critical Care Medicine, vol. 156, no. 3, pp. 840–845, 1997. View at Publisher · View at Google Scholar · View at Scopus
  205. J. G. Clark, J. A. Milberg, K. P. Steinberg, and L. D. Hudson, “Type III procollagen peptide in the adult respiratory distress syndrome: association of increased peptide levels in bronchoalveolar lavage fluid with increased risk for death,” Annals of Internal Medicine, vol. 122, no. 1, pp. 17–23, 1995. View at Publisher · View at Google Scholar · View at Scopus
  206. J.-M. Forel, C. Guervilly, S. Hraiech et al., “Type III procollagen is a reliable marker of ARDS-associated lung fibroproliferation,” Intensive Care Medicine, vol. 41, no. 1, pp. 1–11, 2015. View at Publisher · View at Google Scholar · View at Scopus
  207. C. M. Hendrickson, B. Crestani, and M. A. Matthay, “Biology and pathology of fibroproliferation following the acute respiratory distress syndrome,” Intensive Care Medicine, vol. 41, no. 1, pp. 147–150, 2015. View at Publisher · View at Google Scholar · View at Scopus
  208. L. B. Ware, T. Koyama, D. D. Billheimer et al., “Prognostic and pathogenetic value of combining clinical and biochemical indices in patients with acute lung injury,” Chest, vol. 137, no. 2, pp. 288–296, 2010. View at Publisher · View at Google Scholar · View at Scopus
  209. J.-M. Constantin and E. Futier, “Lung imaging in patients with acute respiratory distress syndrome: from an understanding of pathophysiology to bedside monitoring,” Minerva Anestesiologica, vol. 79, no. 2, pp. 176–184, 2013. View at Google Scholar · View at Scopus
  210. L. Puybasset, P. Gusman, J.-C. Muller, P. Cluzel, P. Coriat, and J.-J. Rouby, “Regional distribution of gas and tissue in acute respiratory distress syndrome. III. Consequences for the effects of positive end-expiratory pressure,” Intensive Care Medicine, vol. 26, no. 9, pp. 1215–1227, 2000. View at Publisher · View at Google Scholar · View at Scopus
  211. J.-M. Constantin, S. Jaber, E. Futier et al., “Respiratory effects of different recruitment maneuvers in acute respiratory distress syndrome,” Critical Care, vol. 12, article R50, 2008. View at Publisher · View at Google Scholar · View at Scopus
  212. J.-M. Constantin, S. Cayot-Constantin, L. Roszyk et al., “Response to recruitment maneuver influences net alveolar fluid clearance in acute respiratory distress syndrome,” Anesthesiology, vol. 106, no. 5, pp. 944–951, 2007. View at Publisher · View at Google Scholar · View at Scopus
  213. R. Mayeux, “Biomarkers: potential uses and limitations,” NeuroRx, vol. 1, no. 2, pp. 182–188, 2004. View at Publisher · View at Google Scholar · View at Scopus
  214. V. G. De Gruttola, P. Clax, D. L. DeMets et al., “Considerations in the evaluation of surrogate endpoints in clinical trials: summary of a National Institutes of Health Workshop,” Controlled Clinical Trials, vol. 22, no. 5, pp. 485–502, 2001. View at Publisher · View at Google Scholar · View at Scopus
  215. P. Ray, Y. L. Manach, B. Riou, and T. T. Houle, “Statistical evaluation of a biomarker,” Anesthesiology, vol. 112, no. 4, pp. 1023–1040, 2010. View at Publisher · View at Google Scholar · View at Scopus
  216. H. Gerlach and S. Toussaint, “Sensitive, specific, predictive… statistical basics: how to use biomarkers,” Critical Care Clinics, vol. 27, no. 2, pp. 215–227, 2011. View at Publisher · View at Google Scholar
  217. M. Bhargava and C. H. Wendt, “Biomarkers in acute lung injury,” Translational Research, vol. 159, no. 4, pp. 205–217, 2012. View at Publisher · View at Google Scholar · View at Scopus