Phosphoinositide 3-kinase, Src, and Akt modulate acute ventilation-induced vascular permeability increases in mouse lungs

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 293, Issue 1, 2007, Pages

  Miyahara, Takashige ^a,b   Hamanaka, Kazutoshi ^a,b   Weber, David S ^a   Drake, Douglas A ^a   Anghelescu, Mircea ^a,b   Parker, James C ^a,b  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

^b UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

catenin; Adherens junction; Capillary permeability

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ALBUMIN; BETA CATENIN; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINOSITIDE 3 KINASE INHIBITOR; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; SERINE; STEROID RECEPTOR COACTIVATOR 1; THREONINE; TYROSINE; UNCLASSIFIED DRUG;

ALBUMIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; C57BL 6 MOUSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; LUNG; LUNG BLOOD VESSEL; LUNG PRESSURE; LUNG VENTILATION; MALE; MECHANICAL STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BETA CATENIN; CAPILLARY PERMEABILITY; FILTRATION; LUNG; MALE; MICE; MICE, INBRED C57BL; ORGAN SIZE; PHOSPHORYLATION; PRESSURE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS PP60(C-SRC); PULMONARY VENTILATION; TIME FACTORS; VASCULAR RESISTANCE;

EID: 34447105081     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00279.2005     Document Type: Article

References (78)

1. Abram CL, Courtneidge SA. Src family tyrosine kinases and growth factor signaling. Exp Cell Res 254: 1-13, 2000.
2. Andjelic S, Hsia C, Suzuki H, Kadowaki T, Koyasu S, Liou HC. Phosphatidylinositol 3-kinase and NF-kappa B/Rel are at the divergence of CD40-mediated proliferation and survival pathways. J Immunol 165: 3860-3867, 2000.
3. Awolesi MA, Widmann MD, Sessa WC, Sumpio BE. Cyclic strain increases endothelial nitric oxide synthase activity. Surgery 116: 439-444, 1995.
4. Becker PM, Verin AD, Booth MA, Liu F, Birukova A, Garcia JGN. Differential regulation of diverse physiological responses to VEGF in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 281: L1500-L1511, 2001.
5. Bhattacharya J, Nakahara K, Staub NC. Effect of edema on pulmonary blood flow in the isolated perfused dog lung lobe. J Appl Physiol 48: 444-449, 1980.
6. Bhattacharya S, Sen N, Yiming MT, Patel R, Parthasarathi K, Quadri S, Issekutz AC, Bhattacharya J. High tidal volume ventilation induces proinflammatory signaling in rat lung endothelium. Am J Respir Cell Mol Biol 28: 218-224, 2003.
7. Birukov KG, Csortos C, Marzilli L, Dudek S, Ma SF, Bresnick AR, Verin AD, Cotter RJ, Garcia JGN. Differential regulation of alternatively spliced endothelial cell myosin light chain kinase isoforms by p60Src. J Biol Chem 276: 8567-8573, 2001.
8. Bogatcheva NV, Garcia JG, Verin AD. Role of tyrosine kinase signaling in endothelial cell barrier regulation. Vasc Pharmacol 39: 201-212, 2002.
9. Broccard AF, Feihl F, Vannay C, Markert M, Hotchkiss J, Schaller MD. Effects of L-NAME and inhaled nitric oxide on ventilator-induced lung injury in isolated, perfused rabbit lungs. Crit Care Med 32: 1872-1878, 2004.
10. Brower RG, Matthay MA, Morris A, Schoenfeld D, Thompson BT. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and respiratory distress syndrome. N Engl J Med 342: 1301-1308, 2000.
11. Cantley LC. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657, 2002.
12. Choi WI, Quinn DA, Park KM, Moufarrej RK, Jafari B, Syrkina O, Bonventre JV, Hales CA. Systemic microvascular leak in an in vivo rat model of ventilator-induced lung injury. Am J Respir Crit Care Med 167: 1627-1632, 2003.
13. Cioffi DL, Moore TM, Schaack J, Creighton JR, Cooper DM, Stevens T. Dominant regulation of interendothelial cell gap formation by calcium-inhibited type 6 adenylyl cyclase. J Cell Biol 157: 1267-1278, 2002.
14. Cohen AW, Carbajal JM, Schaeffer RC Jr. VEGF stimulates tyrosine phosphorylation of β-catenin and small-pore endothelial barrier dysfunction. Am J Physiol Heart Circ Physiol 277: H2038-H2049, 1999.
15. Danciu TE, Adam RM, Naruse K, Freeman MR, Hauschka PV. Calcium regulates the PI3K-Akt pathway in stretched osteoblasts. FEBS Lett 536: 193-197, 2003.
16. Deane JA, Fruman DA. Phosphoinositide 3-kinase: diverse roles in immune cell activation. Annu Rev Immunol 22: 563-598, 2004.
17. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
18. Drake RE, Gabel JC. Comparison of techniques to measure pulmonary capillary filtration coefficients in dogs. Microvasc Res 21: 133-141, 1981.
19. Drake RE, Smith JH, Gabel JC. Estimation of the filtration coefficient in intact dog lungs. Am J Physiol Heart Circ Physiol 238: H430-H438, 1980.
20. Dreyfuss D, Ricard JD, Saumon G. On the physiologic and clinical relevance of lung-borne cytokines during ventilator-induced lung injury. Am J Respir Crit Care Med 167: 1467-1471, 2003.
21. 2-terminal kinase by increasing NO production in response to shear stress. J Appl Physiol 91: 1574-1581, 2001.
22. Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 277: 32124-32132, 2002.
23. Han B, Bai XH, Lodyga M, Xu J, Yang BB, Keshavjee S, Post M, Liu M. Conversion of mechanical force into biochemical signaling. J Biol Chem 279: 54793-54801, 2004.
24. Karni R, Gus Y, Dor Y, Meyuhas O, Levitzki A. Active Src elevates the expression of (beta)-catenin by enhancement of cap-dependent translation. Mol Cell Biol 25: 5031-5039, 2005.
25. Kevil CG, Payne DK, Mire E, Alexander JS. Vascular permeability factor/vascular endothelial cell growth factor-mediated permeability occurs through disorganization of endothelial junctional proteins. J Biol Chem 273: 15099-15103, 1998.
26. Kuebler WM, Uhlig U, Goldmann T, Schael G, Kerem A, Exner K, Martin C, Vollmer E, Uhlig S. Stretch activates nitric oxide production in pulmonary vascular endothelial cells in situ. Am J Respir Crit Care Med 168: 1391-1398, 2001.
27. Kuebler WM, Ying X, Singh B, Issekutz AC, Bhattacharya J. Pressure is proinflammatory in lung venular capillaries. J Clin Invest 104: 495-502, 1999.
28. 2. J Biol Chem 272: 16709-16712, 1997.
29. 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.
30. Lionetti V, Lisi A, Patrucco E, De Giuli P, Milazzo MG, Ceci S, Wymann M, Lena A, Gremigni V, Fanelli V, Hirsch E, Ranieri VM. Lack of phosphoinositide 3-kinase-gamma attenuates ventilator-induced lung injury. Crit Care Med 34: 134-141, 2006.
31. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, Day RM, Bogatcheva N, Bottaro DP, Garcia JG. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J 16: 950-962, 2002.
32. Liu M, Qin Y, Liu J, Tanswell AK, Post M. Mechanical strain induces pp60Src activation and translocation to cytoskeleton in fetal rat lung cells. J Biol Chem 271: 7066-7071, 1996.
33. 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.
34. Lu YB, Parkyn L, Otterbein LE, Kureishi Y, Walsh K, Ray A, Ray P. Activated Akt protects the lung from oxidant-induced injury and delays death of mice. J Exp Med 193: 545-549, 2001.
35. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86: 279-367, 2006.
36. Miyahara T, Shibamoto T, Wang HG, Koizumi T, Honda T, Kubo K, Sekiguchi M, Koyama S. Lecithinized superoxide dismutase attenuates phorbol myristate acetate-induced injury in isolated dog lung. Eur J Pharmacol 344: 231-239, 1998.
37. Monick MM, Carter AB, Robeff P, Flaherty DM, Peterson MW, Hunninghake GW. LPS activates PKB (AKT) in a PI 3-kinase-dependent manner resulting in stabilization and nuclear accumulation of beta catenin. FASEB J 15: A706, 2001.
38. Monick MM, Robeff P, Carter AB, Flaherty DM, Hunninghake GW. Activation of PI 3-kinase by LPS results in inactivation of GSK-3 and nuclear accumulation of beta catenin. Mol Biol Cell 11: 247A, 2000.
39. Mucha DR, Myers CL, Schaeffer RC Jr. Endothelial contraction and monolayer hyperpermeability are regulated by Src kinase. Am J Physiol Heart Circ Physiol 284: H994-H1002, 2003.
40. Muir AL, Hall DL, Despas P, Hogg JC. Distribution of blood flow in the lungs in acute pulmonary edema in dogs. J Appl Physiol 33: 763-769, 1972.
41. Muir AL, Hogg JC, Naimark A, Hall DL, Chernecki W. Effect of alveolar liquid on distribution of blood flow in dog lungs. J Appl Physiol 39: 885-890, 1975.
42. Naruse K, Sai X, Yokoyama N, Sokabe M. Uni-axial cyclic stretch induces c-src activation and translocation in human endothelial cells via SA channel activation. FEBS Lett 441: 111-115, 1998.
43. Parker JC. Inhibitors of myosin light chain kinase, phosphodiesterase and calmodulin attenuate ventilator induced lung injury. J Appl Physiol 89: 2241-2248, 2000.
44. Parker JC, Gillespie MN, Taylor AE, Martin SL. Capillary filtration coefficient, vascular resistance and compliance in isolated mouse lungs. J Appl Physiol 87: 1421-1427, 1999.
45. Parker JC, Ivey C, Tucker A. Gadolinium prevents high airway pressure induced permeability increases in isolated rat lungs. J Appl Physiol 84: 1113-1118, 1998.
46. Parker JC, Ivey CL. Isoproterenol attenuates high vascular pressure-induced permeability increases in isolated rat lungs. J Appl Physiol 83: 1962-1967, 1998.
47. Parker JC, Ivey CL, Tucker A. Phosphotyrosine phosphatase and tyrosine inhibition modulate airway pressure-induced lung injury. J Appl Physiol 85: 1753-1761, 1998.
48. Parker JC, Townsley MI. Evaluation of lung injury in rats and mice. Am J Physiol Lung Cell Mol Physiol 286: L231-L246, 2004.
49. Parker JC, Townsley MI, Cartledge JT. Lung edema increases transvascular filtration rate but not filtration coefficient. J Appl Physiol 66: 1553-1560, 1989.
50. Parker JC, Yoshikawa S. Vascular segmental permeabilities at high peak inflation pressure in isolated rat lungs. Am J Physiol Lung Cell Mol Physiol 283: L1203-L1209, 2002.
51. Peng X, Abdulnour RE, Sammani S, Ma SF, Han EJ, Hasan EJ, Tuder R, Garcia JGN, Hassoun PM. Inducible nitric oxide synthase contributes to ventilator-induced lung injury. Am J Respir Crit Care Med 172: 470-479, 2005.
52. Puri KD, Doggett TA, Huang CY, Douangpanya J, Hayflick JS, Turner M, Penninger J, Diacovo TG. The role of endothelial PI3K(gamma) activity in neutrophil trafficking. Blood 106: 150-157, 2005.
53. Reyes-Reyes M, Mora N, Zentella A, Rosales C. Phosphatidylinositol 3-kinase mediates integrin-dependent NF-kappa B and MAPK activation through separate signaling pathways. J Cell Sci 114: 1579-1589, 2001.
54. Ricard JD, Dreyfuss D, Saumon G. Production of inflammatory cytokines in ventilator-induced lung injury: a reappraisal. Am J Respir Crit Care Med 163: 1176-1180, 2001.
55. Roura S, Miravet S, Piedra J, de Herreros AG, Dunach M. Regulation of E-cadherin/catenin association by tyrosine phosphorylation. J Biol Chem 274: 36734-36740, 1999.
56. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225, 2000.
57. Sedding DG, Hermsen J, Seay U, Eickelberg O, Kummer W, Schwencke C, Strasser RH, Tillmanns H, Braun-Dullaeus RC. Caveolin-1 facilitates mechanosensitive protein kinase B (Akt) signaling in vitro and in vivo. Circ Res 96: 635-642, 2005.
58. Shibamoto T, Parker JC, Taylor AE, Townsley MI. Derecruitment of filtration surface area in paraquat-injured isolated dog lungs. J Appl Physiol 68: 1581-1589, 1990.
59. Shiojima I, Walsh K. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90: 1243-1250, 2002.
60. Takenaka K, Nishimura Y, Nishiuma T, Sakashita A, Yamashita T, Kobayashi K, Satouchi M, Ishida T, Kawashima S, Yokoyama M. Ventilator-induced lung injury is reduced in transgenic mice that overexpress endothelial nitric oxide synthase. Am J Physiol Lung Cell Mol Physiol 290: L1078-L1086, 2006.
61. Tallquist MD, Soriano P, Klinghoffer RA. Growth factor signaling pathways in vascular development. Oncogene 18: 7917-7932, 1999.
62. Taylor AE, Parker JC. The interstitial spaces and lymph flow. In: Handbook of Physiology: The Respiratory System: Circulation and Nonrespiratory Function, edited by Fishman AP and Fisher AB. Bethesda, MD: Am. Physiol. Soc., 1985, p. 167-320.
63. Taylor AE, Parker JC, Kvietys PR, Perry MA. The pulmonary interstitium in capillary exchange. Ann NY Acad Sci 384: 146-165, 1982.
64. Taylor AE, Rehder K, Hyatt RE, Parker JC. Clinical respiratory physiology. Philadelphia, PA: Saunders, 1989.
65. Tinsley JH, Ustinova EE, Xu W, Yuan SY. Src-dependent, neutrophilmediated vascular hyperpermeability and β-catenin modification. Am J Physiol Cell Physiol 283: C1745-C1751, 2002.
66. Uhlig S, Uhlig U. Pharmacologic interventions in ventilator induced lung injury. Trends Pharmacol Sci 25: 592-600, 2004.
67. Uhlig U, Fehrenbach H, Lachmann RA, Goldmann T, Lachmann B, Vollmer E, Uhlig S. Phosphoinositide 3-OH kinase inhibition prevents ventilation-induced lung cell activation. Am J Respir Crit Care Med 169: 201-208, 2004.
68. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602, 2001.
69. Wainwright MS, Rossi J, Schavocky J, Crawford S, Steinhorn D, Velentza AV, Zasadzki M, Shirinsky V, Jia Y, Haiech J, Van Eldik LJ, Watterson DM. Protein kinase involved in lung injury susceptibility: evidence from enzyme isoform genetic knockout and in vivo inhibitor treatment. Proc Natl Acad Sci USA 100: 6233-6238, 2003.
70. West JB, Tsukimoto K, Mathieu Costello O, Prediletto R. Stress failure in pulmonary capillaries. J Appl Physiol 70: 1731-1742, 1991.
71. Yamamoto H, Teramoto H, Uetani K, Igawa K, Shimizu E. Stretch induces a growth factor in alveolar cells via protein kinase. Respir Physiol 127: 105-111, 2001.
72. Yano Y, Geibel J, Sumpio BE. Tyrosine phosphorylation of pp125FAK and paxillin in aortic endothelial cells induced by mechanical strain. Am J Physiol Cell Physiol 271: C635-C649, 1996.
73. Yiming MT, Parthasarathi K, Issekutz AC, Bhattacharya S. Sequence of endothelial signaling during lung expansion. Am J Respir Cell Mol Biol 33: 549-554, 2005.
74. Yoshikawa S, King JA, Lausch RN, Penton AM, Eyal FG, Parker JC. Acute ventilator-induced vascular permeability and cytokine responses in isolated and in situ mouse lungs. J Appl Physiol 97: 2190-2199, 2004.
75. 2 activity modulate acute ventilator-induced lung injury in mice. J Appl Physiol 98: 1264-1271, 2005.
76. Yoshikawa S, King JA, Reynolds SD, Stripp BR, Parker JC. Time and pressure dependence of transvascular Clara cell protein, albumin, and IgG transport during ventilator-induced lung injury in mice. Am J Physiol Lung Cell Mol Physiol 286: L604-L612, 2004.
77. Yuan SY. Protein kinase signaling in the modulation of microvascular permeability. Vasc Pharmacol 39: 213-223, 2002.
78. Yum HK, Arcaroli J, Kupfner J, Shenkar R, Penninger JM, Sasaki T, Yang KY, Park JS, Abraham E. Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. J Immunol 167: 6601-6608, 2001.