Differential and opposing effects of imatinib on LPS- and ventilator-induced lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 3, 2015, Pages L259-L269

  Letsiou, E ^a   Rizzo, A N ^a   Sammani, S ^a   Naureckas, P ^a   Jacobson, J R ^a   Garcia, J G N ^b   Dudek, S M ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

ARDS; Arg; C Abl; Endothelium; Imatinib; LPS; Permeability; Stretch; VILI

Indexed keywords

ABELSON KINASE; ARGININE; ENDOTOXIN; IMATINIB; INTERLEUKIN 6; INTERLEUKIN 8; SMALL INTERFERING RNA; VASCULAR CELL ADHESION MOLECULE 1; VASCULAR ENDOTHELIAL CADHERIN; ALPHA FETOPROTEIN; ALPHA-FETOPROTEIN RELATED PROTEIN, MOUSE; ANTIINFLAMMATORY AGENT; BENZAMIDE DERIVATIVE; CYTOKINE; LIPOPOLYSACCHARIDE; PIPERAZINE DERIVATIVE; PYRIMIDINE DERIVATIVE;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE EXACERBATION; DOWN REGULATION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INFLAMMATION; LUNG ENDOTHELIUM; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIDAL VOLUME; VENTILATOR INDUCED LUNG INJURY; ANIMAL; BIOMECHANICS; BIOSYNTHESIS; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL CULTURE; DRUG EFFECTS; DRUG SCREENING; IMMUNOLOGY; LUNG; METABOLISM; PHYSIOLOGICAL STRESS; VASCULAR ENDOTHELIUM; VASCULARIZATION; VENTILATOR-INDUCED LUNG INJURY;

ALPHA-FETOPROTEINS; ANIMALS; ANTI-INFLAMMATORY AGENTS; BENZAMIDES; BIOMECHANICAL PHENOMENA; CAPILLARY PERMEABILITY; CELLS, CULTURED; CYTOKINES; DRUG EVALUATION, PRECLINICAL; ENDOTHELIUM, VASCULAR; HUMANS; IMATINIB MESYLATE; LIPOPOLYSACCHARIDES; LUNG; MALE; MICE, INBRED C57BL; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-ABL; PYRIMIDINES; STRESS, PHYSIOLOGICAL; VENTILATOR-INDUCED LUNG INJURY;

EID: 84933047245     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00323.2014     Document Type: Article

References (63)

1. 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
2. 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
3. Amma H, Naruse K, Ishiguro N, Sokabe M. Involvement of reactive oxygen species in cyclic stretch-induced NF-B activation in human fibroblast cells. Br J Pharmacol 145: 364–373, 2005
4. Baron F, Turhan AG, Giron-Michel J, Azzarone B, Bentires-Alj M, Bours V, Bourhis JH, Chouaib S, Caignard A. Leukemic target susceptibility to natural killer cytotoxicity: relationship with BCR-ABL expression. Blood 99: 2107–2113, 2002
5. Berlin AA, Lukacs NW. Treatment of cockroach allergen asthma model with imatinib attenuates airway responses. Am J Respir Crit Care Med 171: 35–39, 2005
6. Birukov KG, Jacobson JR, Flores AA, Ye SQ, Birukova AA, Verin AD, Garcia JG. Magnitude-dependent regulation of pulmonary endothelial cell barrier function by cyclic stretch. Am J Physiol Lung Cell Mol Physiol 285: L785–L797, 2003
7. Birukova AA, Tian Y, Meliton A, Leff A, Wu T, Birukov KG. Stimulation of Rho signaling by pathologic mechanical stretch is a “second hit” to Rho-independent lung injury induced by IL-6. Am J Physiol Lung Cell Mol Physiol 302: L965–L975, 2012
8. Birukova AA, Wu T, Tian Y, Meliton A, Sarich N, Tian X, Leff A, Birukov KG. Iloprost improves endothelial barrier function in lipopolysaccharide- induced lung injury. Eur Respir J 41: 165–176, 2013
9. Bradley WD, Koleske AJ. Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J Cell Sci 122: 3441–3454, 2009
10. Chatterjee A, Snead C, Yetik-Anacak G, Antonova G, Zeng J, Catravas JD. Heat shock protein 90 inhibitors attenuate LPS-induced endothelial hyperpermeability. Am J Physiol Lung Cell Mol Physiol 294: L755–L763, 2008
11. Chislock EM, Pendergast AM. Abl family kinases regulate endothelial barrier function in vitro and in mice. PLoS One 8: e85231, 2013
12. 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
13. 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
14. Colicelli J. ABL tyrosine kinases: evolution of function, regulation, and specificity. Sci Signal 3: re6, 2010
15. Contreras M, Ansari B, Curley G, Higgins BD, Hassett P, O’Toole D, Laffey JG. Hypercapnic acidosis attenuates ventilation-induced lung injury by a nuclear factor-B-dependent mechanism. Crit Care Med 40: 2622–2630, 2012
16. Dejana E, Orsenigo F. Endothelial adherens junctions at a glance. J Cell Sci 126: 2545–2549, 2013
17. Dos Santos CC, Slutsky AS. Invited review: mechanisms of ventilatorinduced lung injury: a perspective. J Appl Physiol 89: 1645–1655, 2000
18. Dos Santos LV, Lima JP, Abdalla KC, Bragagnoli AC, Santos FA, Dos Anjos Jacome A, Porto FE. Imatinib-induced bone edema: case report and review of literature. J Natl Compr Canc Netw 11: 1187–1191, 2013
19. 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
20. 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
21. Esmaeli B, Diba R, Ahmadi MA, Saadati HG, Faustina MM, Shepler TR, Talpaz M, Fraunfelder R, Rios MB, Kantarjian H. Periorbital oedema and epiphora as ocular side effects of imatinib mesylate (Gleevec). Eye 18: 760–762, 2004
22. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108: 689–701, 2001
23. Gavard J. Breaking the VE-cadherin bonds. FEBS Lett 583: 1–6, 2009
24. Gawlak G, Tian Y, O’Donnell JJ 3rd, Tian X, Birukova AA, Birukov KG. Paxillin mediates stretch-induced Rho signaling and endothelial permeability via assembly of paxillin-p42/44MAPK-GEF-H1 complex. FASEB J 28: 3249–3260, 2014
25. Greuber EK, Smith-Pearson P, Wang J, Pendergast AM. Role of ABL family kinases in cancer: from leukaemia to solid tumours. Nat Rev Cancer 13: 559–571, 2013
26. Guilhot F. Indications for imatinib mesylate therapy and clinical management. Oncologist 9: 271–281, 2004
27. Halbertsma FJ, Vaneker M, Scheffer GJ, van der Hoeven JG. Cytokines and biotrauma in ventilator-induced lung injury: a critical review of the literature. Neth J Med 63: 382–392, 2005
28. Held HD, Boettcher S, Hamann L, Uhlig S. Ventilation-induced chemokine and cytokine release is associated with activation of nuclear factor-B and is blocked by steroids. Am J Respir Crit Care Med 163: 711–716, 2001
29. Hernández SE, Krishnaswami M, Miller AL, Koleske AJ. How do Abl family kinases regulate cell shape and movement? Trends Cell Biol 14: 36–44, 2004
30. Inoh H, Ishiguro N, Sawazaki S, Amma H, Miyazu M, Iwata H, Sokabe M, Naruse K. Uni-axial cyclic stretch induces the activation of transcription factor nuclear factor B in human fibroblast cells. FASEB J 16: 405–407, 2002
31. Iwaki M, Ito S, Morioka M, Iwata S, Numaguchi Y, Ishii M, Kondo M, Kume H, Naruse K, Sokabe M, Hasegawa Y. Mechanical stretch enhances IL-8 production in pulmonary microvascular endothelial cells. Biochem Biophys Res Commun 389: 531–536, 2009
32. 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. Crit Care 17: R114, 2013
33. Ko YA, Yang MC, Huang HT, Hsu CM, Chen LW. NF-B activation in myeloid cells mediates ventilator-induced lung injury. Respir Res 14: 69, 2013
34. Liu M, Tanswell AK, Post M. Mechanical force-induced signal transduction in lung cells. Am J Physiol Lung Cell Mol Physiol 277: L667–L683, 1999
35. Ma SF, Xie L, Pino-Yanes M, Sammani S, Wade MS, Letsiou E, Siegler J, Wang T, Infusino G, Kittles RA, Flores C, Zhou T, Prabhakar BS, Moreno-Vinasco L, Villar J, Jacobson JR, Dudek SM, Garcia JG. Type 2 deiodinase and host responses of sepsis and acute lung injury. Am J Respir Cell Mol Biol 45: 1203–1211, 2011
36. Maniatis NA, Kotanidou A, Catravas JD, Orfanos SE. Endothelial pathomechanisms in acute lung injury. Vascul Pharmacol 49: 119–133, 2008
37. Matthay MA, Ware LB, Zimmerman GA. The acute respiratory distress syndrome. J Clin Invest 122: 2731–2740, 2012
38. McClelland CM, Harocopos GJ, Custer PL. Periorbital edema secondary to imatinib mesylate. Clin Ophthalmol 4: 427–431, 2010
39. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279–367, 2006
40. Moen MD, McKeage K, Plosker GL, Siddiqui MA. Imatinib: a review of its use in chronic myeloid leukaemia. Drugs 67: 299–320, 2007
41. Moreno-Vinasco L, Quijada H, Sammani S, Siegler J, Letsiou E, Deaton R, Saadat L, Zaidi RS, Messana J, Gann PH, Machado RF, Ma W, Camp SM, Wang T, Garcia JG. Nicotinamide phosphoribosyltransferase inhibitor is a novel therapeutic candidate in murine models of inflammatory lung injury. Am J Respir Cell Mol Biol 51: 223–228, 2014
42. Muller WA. Mechanisms of transendothelial migration of leukocytes. Circ Res 105: 223–230, 2009
43. Nagar B. c-Abl tyrosine kinase and inhibition by the cancer drug imatinib (Gleevec/STI-571). J Nutr 137: 1518S–1523S; discussion 1548S, 2007
44. Ning Q, Wang X. Role of Rel A and IB of nuclear factor B in the release of interleukin-8 by cyclic mechanical strain in human alveolar type II epithelial cells A549. Respirology 12: 792–798, 2007
45. Okuda K, Weisberg E, Gilliland DG, Griffin JD. ARG tyrosine kinase activity is inhibited by STI571. Blood 97: 2440–2448, 2001
46. Ostro D, Lipton J. Unusual fluid retention with imatinib therapy for chronic myeloid leukemia. Leuk Lymphoma 48: 195–196, 2007
47. Peacock JG, Couch BA, Koleske AJ. The Abl and Arg non-receptor tyrosine kinases regulate different zones of stress fiber, focal adhesion, and contractile network localization in spreading fibroblasts. Cytoskeleton (Hoboken) 67: 666–675, 2010
48. Pendergast AM. The Abl family kinases: mechanisms of regulation and signaling. Adv Cancer Res 85: 51–100, 2002
49. Plataki M, Hubmayr RD. The physical basis of ventilator-induced lung injury. Expert Rev Respir Med 4: 373–385, 2010
50. Rhee CK, Lee SH, Yoon HK, Kim SC, Lee SY, Kwon SS, Kim YK, Kim KH, Kim TJ, Kim JW. Effect of nilotinib on bleomycin-induced acute lung injury and pulmonary fibrosis in mice. Respiration 82: 273–287, 2011
51. 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
52. Schouten M, Wiersinga WJ, Levi M, van der Poll T. Inflammation, endothelium, and coagulation in sepsis. J Leukoc Biol 83: 536–545, 2008
53. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, Richards DR, McDonald-Smith GP, Gao H, Hennessy L, Finnerty CC, Lopez CM, Honari S, Moore EE, Minei JP, Cuschieri J, Bankey PE, Johnson JL, Sperry J, Nathens AB, Billiar TR, West MA, Jeschke MG, Klein MB, Gamelli RL, Gibran NS, Brownstein BH, Miller- Graziano C, Calvano SE, Mason PH, Cobb JP, Rahme LG, Lowry SF, Maier RV, Moldawer LL, Herndon DN, Davis RW, Xiao W, Tompkins RG. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 110: 3507–3512, 2013
54. Sirvent A, Benistant C, Roche S. Cytoplasmic signalling by the c-Abl tyrosine kinase in normal and cancer cells. Biol Cell 100: 617–631, 2008
55. Slutsky AS, Ranieri VM. Ventilator-induced lung injury. N Engl J Med 369: 2126–2136, 2013
56. 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
57. Sun Y, Hu G, Zhang X, Minshall RD. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res 105: 676–685, 615 p. following 685, 2009
58. 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
59. 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
60. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 342: 1334–1349, 2000
61. Wolf AM, Wolf D, Rumpold H, Ludwiczek S, Enrich B, Gastl G, Weiss G, Tilg H. The kinase inhibitor imatinib mesylate inhibits TNF_ production in vitro and prevents TNF-dependent acute hepatic inflammation. Proc Natl Acad Sci USA 102: 13622–13627, 2005
62. Woodring PJ, Hunter T, Wang JY. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J Cell Sci 116: 2613–2626, 2003
63. Zandy NL, Playford M, Pendergast AM. Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci USA 104: 17686–17691, 2007.