Imatinib attenuates inflammation and vascular leak in a clinically relevant two-hit model of acute lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 11, 2015, Pages L1294-L1304

  Rizzo, Alicia N ^a,b   Sammani, Saad ^a   Esquinca, Adilene E ^a   Jacobson, Jeffrey R ^a   Garcia, Joe G N ^c   Letsiou, Eleftheria ^a   Dudek, Steven M ^a,b  

^a UNIVERSITY OF ILLINOIS HOSPITAL AND HEALTH SCIENCES SYSTEM   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Acute lung injury; Acute respiratory distress syndrome; Endothelium; Imatinib; Lipopolysaccharide; Mechanical ventilation; NF B

Indexed keywords

IMATINIB; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; PROTECTIVE AGENT; TUMOR NECROSIS FACTOR;

ACUTE LUNG INJURY; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL COUNT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENDOTHELIUM CELL; HISTOLOGY; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; LUNG PARENCHYMA; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSCRIPTION INITIATION; TREATMENT OUTCOME; VENTILATOR INDUCED LUNG INJURY; ADVERSE EFFECTS; ANIMAL; ARTIFICIAL VENTILATION; BIOLOGICAL MODEL; BIOSYNTHESIS; BRONCHOALVEOLAR LAVAGE FLUID; C57BL MOUSE; CELL NUCLEUS; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; INFLAMMATION; LUNG; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PULMONARY ARTERY; VASCULARIZATION; VENTILATOR-INDUCED LUNG INJURY;

ACUTE LUNG INJURY; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL NUCLEUS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HUMANS; IMATINIB MESYLATE; INFLAMMATION; LIPOPOLYSACCHARIDES; LUNG; MALE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; NF-KAPPA B; PHOSPHORYLATION; PROTECTIVE AGENTS; PULMONARY ARTERY; RESPIRATION, ARTIFICIAL; TUMOR NECROSIS FACTOR-ALPHA; VENTILATOR-INDUCED LUNG INJURY;

EID: 84949499436     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00031.2015     Document Type: Article

References (52)

1. Ventilation with lower tidal volumes compared with traditional tidal volumes for acute lung injury, and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 342: 1301-1308, 2000.
2. Adzemovic MZ, Zeitelhofer M, Eriksson U, Olsson T, Nilsson I. Imatinib ameliorates neuroinflammation in a rat model of multiple sclerosis by enhancing blood-brain barrier integrity and by modulating the peripheral immune response. PLoS One 8: e56586, 2013.
3. Akashi N, Matsumoto I, Tanaka Y, Inoue A, Yamamoto K, Umeda N, Hayashi T, Goto D, Ito S, Sekiguchi K, Sumida T. Comparative suppressive effects of tyrosine kinase inhibitors imatinib and nilotinib in models of autoimmune arthritis. Mod Rheumatol 21: 267-275, 2011.
4. Aman J, Peters MJ, Weenink C, van Nieuw Amerongen GP, Vonk Noordegraaf A. Reversal of vascular leak with imatinib. Am J Respir Crit Care Med 188: 1171-1173, 2013.
5. Aman J, van Bezu J, Damanafshan A, Huveneers S, Eringa EC, Vogel SM, Groeneveld AB, Vonk Noordegraaf A, van Hinsbergh VW, van Nieuw Amerongen GP. Effective treatment of edema and endothelial barrier dysfunction with imatinib. Circulation 126: 2728-2738, 2012.
6. Cao C, Leng Y, Huang W, Liu X, Kufe D. Glutathione peroxidase 1 is regulated by the c-Abl and Arg tyrosine kinases. J Biol Chem 278: 39609-39614, 2003.
7. Cao C, Leng Y, Kufe D. Catalase activity is regulated by c-Abl and Arg in the oxidative stress response. J Biol Chem 278: 29667-29675, 2003.
8. Carnevale-Schianca F, Gallo S, Rota-Scalabrini D, Sangiolo D, Fiz-zotti M, Caravelli D, Capaldi A, Anselmetti G, Palesandro E, D'Ambrosio L, Coha V, Obert R, Aglietta M, Grignani G. Complete resolution of life-threatening bleomycin-induced pneumonitis after treatment with imatinib mesylate in a patient with Hodgkin's lymphoma: hope for severe chemotherapy-induced toxicity? J Clin Oncol 29: e691-693, 2011.
9. Chen A, Lee SM, Gao B, Shannon S, Zhu Z, Fang D. c-Abl-mediated tyrosine phosphorylation of the T-bet DNA-binding domain regulates CD4+ T-cell differentiation and allergic lung inflammation. Mol Cell Biol 31: 3445-3456, 2011.
10. Chislock EM, Pendergast AM. Abl family kinases regulate endothelial barrier function in vitro and in mice. PLoS One 8: e85231, 2013.
11. Chislock EM, Ring C, Pendergast AM. Abl kinases are required for vascular function, Tie2 expression, and angiopoietin-1-mediated survival. Proc Natl Acad Sci USA 110: 12432-12437, 2013.
12. Ciarcia R, Vitiello MT, Galdiero M, Pacilio C, Iovane V, d'Angelo D, Pagnini D, Caparrotti G, Conti D, Tomei V, Florio S, Giordano A. Imatinib treatment inhibit IL-6, IL-8, NF-KB and AP-1 production and modulate intracellular calcium in CML patients. J Cell Physiol 227: 2798-2803, 2012.
13. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF-kB and cytokine-inducible enhancers. FASEB J 9: 899-909, 1995.
14. Daniels CE, Wilkes MC, Edens M, Kottom TJ, Murphy SJ, Limper AH, Leof EB. Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Invest 114: 1308-1316, 2004.
15. de Ménorval MA, Mir LM, Fernández ML, Reigada R. Effects of dimethyl sulfoxide in cholesterol-containing lipid membranes: a comparative study of experiments in silico and with cells. PLoS One 7: e41733, 2012.
16. Druker BJ, Guilhot F, O'Brien SG, Gathmann I, Kantarjian H, Gattermann N, Deininger MW, Silver RT, Goldman JM, Stone RM, Cervantes F, Hochhaus A, Powell BL, Gabrilove JL, Rousselot P, Reiffers J, Cornelissen JJ, Hughes T, Agis H, Fischer T, Verhoef G, Shepherd J, Saglio G, Gratwohl A, Nielsen JL, Radich JP, Simonsson B, Taylor K, Baccarani M, So C, Letvak L, Larson RA, Investigators I. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355: 2408-2417, 2006.
17. Druker BJ, Talpaz M, Resta DJ, Peng B, Buchdunger E, Ford JM, Lydon NB, Kantarjian H, Capdeville R, Ohno-Jones S, Sawyers CL. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med 344: 1031-1037, 2001.
18. Dudek SM, Chiang ET, Camp SM, Guo Y, Zhao J, Brown ME, Singleton PA, Wang L, Desai A, Arce FT, Lal R, Van Eyk JE, Imam SZ, Garcia JG. Abl tyrosine kinase phosphorylates nonmuscle Myosin light chain kinase to regulate endothelial barrier function. Mol Biol Cell 21: 4042-4056, 2010.
19. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500, 2001.
20. Erickson SE, Martin GS, Davis JL, Matthay MA, Eisner MD, NIH NHLBI ARDS Network. Recent trends in acute lung injury mortality: 1996-2005. Crit Care Med 37: 1574-1579, 2009.
21. Garcia AN, Vogel SM, Komarova YA, Malik AB. Permeability of endothelial barrier: cell culture and in vivo models. Methods Mol Biol 763: 333-354, 2011.
22. Goldman JL, Sammani S, Kempf C, Saadat L, Letsiou E, Wang T, Moreno-Vinasco L, Rizzo AN, Fortman JD, Garcia JG. Pleiotropic effects of interleukin-6 in a “two-hit” murine model of acute respiratory distress syndrome. Pulm Circ 4: 280-288, 2014.
23. Goldsby R, Pulsipher M, Adams R, Coffin C, Albritton K, Wagner L. Unexpected pleural effusions in 3 pediatric patients treated with STI-571. J Pediatr Hematol Oncol 24: 694-695, 2002.
24. Held HD, Boettcher S, Hamann L, Uhlig S. Ventilation-induced chemo-kine and cytokine release is associated with activation of nuclear factor-kappaB and is blocked by steroids. Am J Respir Crit Care Med 163: 711-716, 2001.
25. Hotchkiss RS, Karl IE. The pathophysiology and treatment of sepsis. N Engl J Med 348: 138-150, 2003.
26. Hägerkvist R, Sandler S, Mokhtari D, Welsh N. Amelioration of diabetes by imatinib mesylate (Gleevec): role of ß-cell NF-kB activation and anti-apoptotic preconditioning. FASEB J 21: 618-628, 2007.
27. Kim IK, Rhee CK, Yeo CD, Kang HH, Lee DG, Lee SH, Kim JW. Effect of tyrosine kinase inhibitors, imatinib and nilotinib, in murine lipopolysaccharide-induced acute lung injury during neutropenia recovery. CritCare 17: R114, 2013.
28. Ko YA, Yang MC, Huang HT, Hsu CM, Chen LW. NF-kB activation in myeloid cells mediates ventilator-induced lung injury. Respir Res 14: 69, 2013.
29. Letsiou E, Rizzo AN, Sammani S, Naureckas P, Jacobson JR, Garcia JG, Dudek SM. Differential and opposing effects of imatinib on LPS- and ventilator-induced lung injury. Am J Physiol Lung Cell Mol Physiol 308: L259-L269, 2015.
30. Li LF, Yu L, Quinn DA. Ventilation-induced neutrophil infiltration depends on c-Jun N-terminal kinase. Am J Respir Crit Care Med 169: 518-524, 2004.
31. Lin SM, Lin HC, Lee KY, Huang CD, Liu CY, Wang CH, Kuo HP. Ventilator-induced injury augments interleukin-1beta production and neu-trophil sequestration in lipopolysaccharide-treated lungs. Shock 28: 453-460, 2007.
32. Liu YY, Liao SK, Huang CC, Tsai YH, Quinn DA, Li LF. Role for nuclear factor-kappaB in augmented lung injury because of interaction between hyperoxia and high stretch ventilation. Transl Res 154: 228-240, 2009.
33. Moitra J, Sammani S, Garcia JG. Re-evaluation of Evans Blue dye as a marker of albumin clearance in murine models of acute lung injury. Transl Res 150: 253-265, 2007.
34. Mokhtari D, Li T, Lu T, Welsh N. Effects of Imatinib Mesylate (Gleevec) on human islet NF-kappaB activation and chemokine production in vitro. PLoS One 6: e24831, 2011.
35. Ning QM, Wang XR. Activations of mitogen-activated protein kinase and nuclear factor-kappaB by mechanical stretch result in ventilation-induced lung injury. Med Hypotheses 68: 356-360, 2007.
36. Overbeek MJ, van Nieuw Amerongen GP, Boonstra A, Smit EF, Vonk-Noordegraaf A. Possible role of imatinib in clinical pulmonary veno-occlusive disease. Eur Respir J 32: 232-235, 2008.
37. Peng B, Lloyd P, Schran H. Clinical pharmacokinetics of imatinib. Clin Pharmacokinet 44: 879-894, 2005.
38. Pugin J. Molecular mechanisms of lung cell activation induced by cyclic stretch. Crit Care Med 31: S200-S206, 2003.
39. Rix U, Hantschel O, Dürnberger G, Remsing Rix LL, Planyavsky M, Fernbach NV, Kaupe I, Bennett KL, Valent P, Colinge J, Köcher T, Superti-Furga G. Chemical proteomic profiles of the BCR-ABL inhibitors imatinib, nilotinib, and dasatinib reveal novel kinase and nonkinase targets. Blood 110: 4055-4063, 2007.
40. Sakurai H, Chiba H, Miyoshi H, Sugita T, Toriumi W. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J Biol Chem 274: 30353-30356, 1999.
41. Scheinfeld N. Imatinib mesylate and dermatology part 2: a review of the cutaneous side effects of imatinib mesylate. J Drugs Dermatol 5: 228-231, 2006.
42. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, Grimminger F. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 115: 2811-2821, 2005.
43. Shu YS, Tao W, Miao QB, Zhu YB, Yang YF. Improvement of ventilation-induced lung injury in a rodent model by inhibition of inhibitory kB kinase. J Trauma Acute Care Surg 76: 1417-1424, 2014.
44. Slutsky AS, Ranieri VM. Ventilator-induced lung injury. N Engl J Med 369: 2126-2136, 2013.
45. Stephens RS, Servinsky LE, Rentsendorj O, Kolb TM, Pfeifer A, Pearse DB. Protein kinase G increases antioxidant function in lung microvascular endothelial cells by inhibiting the c-Abl tyrosine kinase. Am J Physiol Cell Physiol 306: C559-C569, 2014.
46. Su EJ, Fredriksson L, Geyer M, Folestad E, Cale J, Andrae J, Gao Y, Pietras K, Mann K, Yepes M, Strickland DK, Betsholtz C, Eriksson U, Lawrence DA. Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat Med 14: 731-737, 2008.
47. Tan SY, Kan E, Lim WY, Chay G, Law JH, Soo GW, Bukhari NI, Segarra I. Metronidazole leads to enhanced uptake of imatinib in brain, liver and kidney without affecting its plasma pharmacokinetics in mice. J Pharm Pharmacol 63: 918-925, 2011.
48. Uhlig U, Haitsma JJ, Goldmann T, Poelma DL, Lachmann B, Uhlig S. Ventilation-induced activation of the mitogen-activated protein kinase pathway. Eur Respir J 20: 946-956, 2002.
49. Wadgaonkar R, Linz-McGillem L, Zaiman AL, Garcia JG. Endothe-lial cell myosin light chain kinase (MLCK) regulates TNFalpha-induced NFkappaB activity. J Cell Biochem 94: 351-364, 2005.
50. Wang L, Chiang ET, Simmons JT, Garcia JG, Dudek SM. FTY720-induced human pulmonary endothelial barrier enhancement is mediated by c-Abl. Eur Respir J 38: 78-88, 2011.
51. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349, 2000.
52. Wolf AM, Wolf D, Rumpold H, Ludwiczek S, Enrich B, Gastl G, Weiss G, Tilg H. The kinase inhibitor imatinib mesylate inhibits TNF-alpha production in vitro and prevents TNF-dependent acute hepatic inflammation. Proc Natl Acad Sci USA 102: 13622-13627, 2005.