Journal of Surgical Research
Volume 157, Issue 1 , Pages 30-42 , November 2009

Cell-Cell Junctions and Vascular Endothelial Growth Factor in Rat Lung as Affected by Ischemia/Reperfusion and Preconditioning With Inhaled Nitric Oxide

Received 25 March 2008

References 

  1. dePerrot M, Liu M, Waddell TK, et al. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med. 2003;167:490
  2. Seal JB, Gewertz BL. Vascular dysfunction in ischemia-reperfusion injury. Ann Vasc Surg. 2005;19:572
  3. Bazzoni G, Dejana E. Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis. Physiol Rev. 2004;84:869
  4. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86:279
  5. Yamada S, Pokutta S, Drees F, et al. Deconstructing the cadherin-catenin-actin complex. Cell. 2005;123:889
  6. Goto T, Ishizaka A, Kobayashi F, et al. Importance of tumor necrosis factor-alpha cleavage process in post-transplantation lung injury in rats. Am J Respir Crit Care Med. 2004;170:1239
  7. Godzich M, Hodnett M, Frank JA, et al. Activation of the stress protein response prevents the development of pulmonary edema by inhibiting VEGF cell signaling in a model of lung ischemia-reperfusion injury in rats. FASEB J. 2006;20:1519
  8. Pasupathy S, Homer-Vanniasinkam S. Ischaemic preconditioning protects against ischaemia/reperfusion injury: Emerging concepts. Eur J Vasc Endovasc Surg. 2005;29:106
  9. Downey JM, Davis AM, Cohen MV. Signaling pathways in ischemic preconditioning. Heart Fail Rev. 2007;12:181
  10. Cohen MV, Yang XM, Downey JM. Nitric oxide is a preconditioning mimetic and cardioprotectant and is the basis of many available infarct-sparing strategies. Cardiovasc Res. 2006;70:231
  11. Fujino S, Nagahiro I, Triantafillou AN, et al. Inhaled nitric oxide at the time of harvest improves early lung allograft function. Ann Thorac Surg. 1997;63:1383
  12. Guery B, Neviere R, Viget N, et al. Inhaled NO preadministration modulates local and remote ischemia-reperfusion organ injury in a rat model. J Appl Physiol. 1999;87:47
  13. Schütte H, Witzenrath M, Mayer K, et al. Short-term “preconditioning” with inhaled nitric oxide protects rabbit lungs against ischemia-reperfusion injury. Transplantation. 2001;72:1363
  14. Waldow T, Alexiou K, Witt W, et al. Protection of lung tissue against ischemia/reperfusion injury by preconditioning with inhaled nitric oxide in an in situ pig model of normothermic pulmonary ischemia. Nitric Oxide. 2004;10:195
  15. Waldow T, Alexiou K, Witt W, et al. Attenuation of reperfusion-induced systemic inflammation by preconditioning with nitric oxide in an in situ porcine model of normothermic lung ischemia. Chest. 2004;125:2253
  16. Gómez CB, del Valle HF, Bertolotti A, et al. Effects of short-term inhaled nitric oxide on interleukin-8 release after single-lung transplantation in pigs. J Heart Lung Transplant. 2005;24:714
  17. Vyas-Read S, Shaul PW, Yuhanna IS, et al. Nitric oxide attenuates epithelial – mesenchymal transition in alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol. 2007;293:212
  18. Moldobaeva A, Welsh-Servinsky LE, Shimoda LA, et al. Role of protein kinase G in barrier-protective effects of cGMP in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol. 2006;290:919
  19. Voelkel NF, Vandivier RW, Tuder RM. Vascular endothelial growth factor in the lung. Am J Physiol Lung Cell Mol Physiol. 2006;290:209
  20. Waldow T, Witt W, Ulmer A, et al. Preconditioning by inhaled nitric oxide prevents hyperoxic and ischemia/reperfusion injury in rat lungs. Pulmon Pharmacol Ther. 2007;21:418
  21. Patterson CE, Rhoades RA, Garcia JG. Evans blue dye as a marker of albumin clearance in cultured endothelial monolayer and isolated lung. J Appl Physiol. 1992;72:865
  22. Waldow T, Witt W, Weber E, et al. Nitric oxide donor-induced persistent inhibition of cell adhesion protein expression and NFkappaB activation in endothelial cells. Nitric Oxide. 2006;15:103
  23. Calautti E, Cabodi S, Stein PL, et al. Tyrosine phosphorylation and Src family kinases control keratinocyte cell-cell adhesion. J Cell Biol. 1998;141:1449
  24. Predescu D, Vogel SM, Malik AB. Functional and morphological studies of protein transcytosis in continuous endothelia. Am J Physiol Lung Cell Mol Physiol. 2004;287:L895
  25. Mei JM, Borchert GL, Donald SP, Phang JM. Matrix metalloproteinase(s) mediate(s) NO-induced dissociation of β-catenin from membrane bound E-cadherin and formation of nuclear β-catenin/LEF-1 complex. Carcinogenesis. 2002;23:2119
  26. González D, Herrera B, Beltrán A, et al. Nitric oxide disrupts VE-cadherin complex in murine microvascular endothelial cells. Biochem Biophys Res Commun. 2003;304:113
  27. You D, Waeckel L, Ebrahimian TG, et al. Increase in vascular permeability and vasodilation are critical for proangiogenic effects of stem cell therapy. Circulation. 2006;114:328
  28. Safdar Z, Wang P, Ichimura H, et al. Hyperosmolarity enhances the lung capillary barrier. J Clin Invest. 2003;112:1541
  29. Godzich M, Hodnett M, Frank JA, et al. Activation of the stress protein response prevents the development of pulmonary edema by inhibiting VEGF cell signaling in a model of lung ischemia-reperfusion injury in rats. FASEB J. 2006;20:757
  30. Parker JC, Stevens T, Randall J, et al. Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am J Physiol Lung Cell Physiol. 2006;291:L30
  31. Wang F, Daugherty B, Keise LL, et al. Heterogeneity of claudin expression by alveolar epithelial cells. Am J Respir Cell Mol Biol. 2003;29:62
  32. González-Mariscal L, Betanzos A, Nava P, et al. Tight junction proteins. Prog Biophys Mol Biol. 2003;81:1
  33. Lum H, Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol. 2001;280:C719
  34. Bush KT, Tsukamoto T, Nigam SK. Selective degradation of E-cadherin and dissolution of E-cadherin-catenin complexes in epithelial ischemia. Am J Physiol Renal Physiol. 2000;278:F847
  35. Lampugnani MG, Corada M, Caveda L, et al. The molecular organization of endothelial cell to cell junctions: Differential association of plakoglobin, β-catenin, and α-catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol. 1995;129:203
  36. Scott JA, Yap AS. Cinderella no longer: α-catenin steps out of cadherin's shadow. J Cell Sci. 2006;119:4599
  37. Nelson WJ, Nusse R. Convergence of Wnt, β-catenin, and cadherin pathways. Science. 2004;303:1483
  38. Dugo L, Collin M, Thiemermann C. Glycogen synthase kinase 3β as a target for the therapy of shock and inflammation. Shock. 2007;27:113
  39. Clevers H. Wnt/β-catenin signaling in development and disease. Cell. 2006;127:469
  40. Miyahara T, Hamanaka K, Weber DS, et al. Phosphoinositide 3-kinase, Src, and Akt modulate acute ventilation-induced vascular permeability increases in mouse lungs. Am J Physiol Lung Cell Mol Physiol. 2007;293:L11
  41. Liu F, Schaphorst KL, Verin AD, et al. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: Potential role of glycogen synthase kinase-3β. FASEB J. 2002;16:950
  42. Failor KL, Desyatnikov Y, Finger LA, et al. Glucocorticoid-induced degradation of GSK3 protein is triggered by Sgk and Akt signaling and controls beta-catenin dynamics and tight junction formation in mammery epithelial tumor cells. Mol Endocrinol. 2007;21:2403
  43. Prévotat L, Filomenko R, Solary E, et al. Nitric oxide-induced down-regulation of β-catenin in colon cancer cells by a proteasome-independent specific pathway. Gastroenterology. 2006;131:1142
  44. Katsube T, Tsuji H, Onoda M. Nitric oxide attenuates hydrogen peroxide-induced barrier disruption and protein tyrosine phosphorylation in monolayers of intestinal epithelial cell. Biochim Biophys Acta. 2007;1773:794
  45. Keck PJ, Hauser SD, Krivi G, et al. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science. 1989;246:1309
  46. Monacci WT, Merrill MJ, Oldfield EH. Expression of vascular permeability factor/vascular endothelial growth factor in normal rat tissues. Am J Physiol. 1993;264:C995
  47. Kaner RJ, Crystal RG. Compartmentalization of vascular endothelial growth factor to the epithelial surface of the human lung. Mol Med. 2001;7:240
  48. Thickett DR, Armstrong L, Millar AB. A role for vascular endothelial growth factor in acute and resolving lung injury. Am J Respir Crit Care Med. 2002;166:1332
  49. Esser S, Lampugnani MG, Corada M, et al. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111:1853
  50. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol. 2006;11:1223
  51. Becker PM, Alcasabas A, Yu A, et al. Oxygen-independent upregulation of vascular endothelial growth factor and vascular barrier dysfunction during ventilated pulmonary ischemia in isolated ferret lungs. Am J Respir Cell Mol Biol. 2000;22:272
  52. Tuder RM, Flook BE, Voelkel NF. Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. J Clin Invest. 1995;95:1798
  53. Balasubramaniam V, Tang JR, Maxey A, et al. Mild hypoxia impairs alveolarization in the endothelial nitric oxide synthase-deficient mouse. Am J Physiol Lung Cell Mol Physiol. 2003;284:L964
  54. Ekekezie II, Thibeault DW, Rezaikhaligh MH, et al. Endostatin and vascular endothelial cell growth factor (VEGF) in piglet lungs: Effect of inhaled nitric oxide and hyperoxia. Pediatr Res. 2003;53:440
  55. Lopez E, Boucherat O, Franco-Montoya ML, et al. Nitric oxide donor restores lung growth factor and receptor expression in hyperoxia-exposed rat pups. Am J Respir Cell Mol Biol. 2006;34:738
  56. Liu Y, Christou H, Morita T, et al. Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5′ enhancer. J Biol Chem. 1998;273:15257
  57. Adhikari NKJ, Burns KEA, Friedrich JO, et al. Effect of nitric oxide on oxygenation and mortality in acute lung injury: Systematic review and meta-analysis. Br Med J. 2007;334:779
  58. Ferguson ND. Inhaled nitric oxide for acute respiratory distress syndrome. Theoretical promise of benefit does not translate to improvements in morbidity and mortality. Br Med J. 2007;334:757
  59. Lahm T, Crisostomo PR, Markel TA, et al. The critical role of vascular endothelial growth factor in pulmonary vascular remodeling after lung injury. Shock. 2007;28:4
  60. Maharaj AS, D'Amore PA. Roles for VEGF in the adult. Microvasc Res. 2007;74:100

PII: S0022-4804(08)00525-8

doi: 10.1016/j.jss.2008.07.042

Journal of Surgical Research
Volume 157, Issue 1 , Pages 30-42 , November 2009

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