Role of protein kinase G in barrier-protective effects of cGMP in human pulmonary artery endothelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 290, Issue 5, 2006, Pages

  Moldobaeva, Aigul ^a   Welsh Servinsky, Laura E ^a   Shimoda, Larissa A ^a   Stephens, R Scott ^a   Verin, Alexander D ^a,c   Tuder, Rubin M ^b   Pearse, David B ^a,d  

^a Division of Pulmonary and Critical Care Medicine   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d JOHNS HOPKINS BAYVIEW MEDICAL CENTER   (United States)

Author keywords

Acute lung injury; cAMP; Hydrogen peroxide; Pulmonary edema

Indexed keywords

8 (4 CHLOROPHENYLTHIO) CYCLIC GMP; CADHERIN; CALCIUM; CYCLIC GMP DEPENDENT PROTEIN KINASE; PHOSPHOPROTEIN; SERINE DERIVATIVE; VIRUS PROTEIN;

ADENOVIRUS; ARTICLE; CALCIUM CELL LEVEL; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CELL PROTECTION; CONTROLLED STUDY; CYTOSKELETON; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; GENE TRANSFER; HUMAN; HUMAN CELL; LUNG ALVEOLUS EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; STRESS FIBER;

ADENOVIRIDAE; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENDOTHELIUM, VASCULAR; HUMANS; PULMONARY ARTERY; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 33646592587     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00434.2005     Document Type: Article

References (54)

1. Alexander JS, Alexander BC, Eppihimer LA, Goodyear N, Haque R, Davis CP, Kalogeris TJ, Carden DL, Zhu YN, and Kevil CG. Inflammatory mediators induce sequestration of VE-cadherin in cultured human endothelial cells. Inflammation 24: 99-113, 2000.
2. Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, and Gerbes AL. Prevention of Kupffer cell-induced oxidant injury in rat liver by atrial natriuretic peptide. Am J Physiol Gastrointest Liver Physiol 276: G1137-G1144, 1999.
3. Bilzer M, Witthaut R, Paumgartner G, and Gerbes AL. Prevention of ischemia/reperfusion injury in the rat liver by atrial natriuretic peptide. Gastroenterology 106: 143-151, 1994.
4. Chiche JD, Schlutsmeyer SM, Bloch DB, de la Monte SM, Roberts JD Jr, Filippov G, Janssens SP, Rosenzweig A, and Bloch KD. Adenovirus-mediated gene transfer of cGMP-dependent protein kinase increases the sensitivity of cultured vascular smooth muscle cells to the antiproliferative and pro-apoptotic effects of nitric oxide/cGMP. J Biol Chem 273: 34263-34271, 1998.
5. Chitaley K, Chen L, Galler A, Walter U, Daum G, and Clowes AW. Vasodilator-stimulated phosphoprotein is a substrate for protein kinase C. FEBS Lett 556: 211-215, 2004.
6. Clements RT, Minnear FL, Singer HA, Keller RS, and Vincent PA. RhoA and Rho-kinase dependent and independent signals mediate TGF-β-induced pulmonary endothelial cytoskeletal reorganization and permeability. Am J Physiol Lung Cell Mol Physiol 288: L294-L306, 2005.
7. Comerford KM, Lawrence DW, Synnestvedt K, Levi BP, and Colgan SP. Role of vasodilator-stimulated phosphoprotein in PKA-induced changes in endothelial junctional permeability. FASEB J 16: 583-585, 2002.
8. 2+ by atriopeptin and 8-bromo-cyclic GMP is mediated by cyclic GMP-dependent protein kinase. J Biol Chem 264: 1146-1155, 1989.
9. Diwan AH, Thompson WJ, Lee AK, and Strada SJ. Cyclic GMP-dependent protein kinase activity in rat pulmonary microvascular endothelial cells. Biochem Biophys Res Commun 202: 728-735, 1994.
10. Draijer R, Atsma DE, van der Laarse A, and van Hinsbergh VW. cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Regulation via different pathways in human aortic and umbilical vein endothelial cells. Circ Res 76: 199-208, 1995.
11. Draijer R, Vaandrager AB, Nolte C, de Jonge HR, Walter U, and van Hinsbergh VW. Expression of cGMP-dependent protein kinase I and phosphorylation of its substrate, vasodilator-stimulated phosphoprotein, in human endothelial cells of different origin. Circ Res 77: 897-905, 1995.
12. Feil R, Gappa N, Rutz M, Schlossmann J, Rose CR, Konnerth A, Brummer S, Kuhbandner S, and Hofmann F. Functional reconstitution of vascular smooth muscle cells with cGMP-dependent protein kinase I isoforms. Circ Res 90: 1080-1086, 2002.
13. Fischer TA, Palmetshofer A, Gambaryan S, Butt E, Jassoy C, Walter U, Sopper S, and Lohmann SM. Activation of cGMP-dependent protein kinase Iβ inhibits interleukin 2 release and proliferation of T cell receptor-stimulated human peripheral T cells. J Biol Chem 276: 5967-5974, 2000.
14. Gainor JP, Morton CA, Roberts JT, Vincent PA, and Minnear FL. Platelet-conditioned medium increases endothelial electrical resistance independently of cAMP/PKA and cGMP/PKG. Am J Physiol Heart Circ Physiol 281: H1992-H2001, 2001.
15. 2-induced endothelial barrier dysfunction: mechanisms of protection. Am J Physiol Lung Cell Mol Physiol 280: L116-L126, 2001.
16. Harbeck B, Huttelmaier S, Schluter K, Jockusch BM, and Illenberger S. Phosphorylation of the vasodilator-stimulated phosphoprotein regulates its interaction with actin. J Biol Chem 275: 30817-30825, 2000.
17. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, and Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95: 2509-2514, 1998.
18. Holschermann H, Noll T, Hempel A, and Piper HM. Dual role of cGMP in modulation of macromolecule permeability of aortic endothelial cells. Am J Physiol Heart Circ Physiol 272: H91-H98, 1997.
19. Hou Y, Lascola J, Dulin NO, Ye RD, and Browning DD. Activation of cGMP-dependent protein kinase by protein kinase C. J Biol Chem 278: 16706-16712, 2003.
20. Inserte J, Garcia-Dorado D, Agullo L, Paniagua A, and Soler-Soler J. Urodilatin limits acute reperfusion injury in the isolated rat heart. Cardiovasc Res 45: 351-359, 2000.
21. Kevil CG, Ohno N, Gute DC, Okayama N, Robinson SA, Chaney E, and Alexander JS. Role of cadherin internalization in hydrogen peroxide-mediated endothelial permeability. Free Radic Biol Med 24: 1015-1022, 1998.
22. 2- mediated permeability. II. Importance of tyrosine phosphatase and kinase activity. Am J Physiol Cell Physiol 281: C1940-C1947, 2001.
23. Kubes P. Nitric oxide affects microvascular permeability in the intact and inflamed vasculature. Microcirculation 2: 235-244, 1995.
24. Kwan HY, Huang Y, and Yao X. Store-operated calcium entry in vascular endothelial cells is inhibited by cGMP via a protein kinase G-dependent mechanism. J Biol Chem 275: 6758-6763, 2000.
25. Kwan HY, Huang Y, and Yao X. Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. Proc Natl Acad Sci USA 101: 2625-2630, 2004.
26. Lofton CE, Baron DA, Heffner JE, Currie MG, and Newman WH. Atrial natriuretic peptide inhibits oxidant-induced increases in endothelial permeability. J Mol Cell Cardiol 23: 919-927, 1991.
27. Lofton CE, Newman WH, and Currie MG. Atrial natriuretic peptide regulation of endothelial permeability is mediated by cGMP. Biochem Biophys Res Commun 172: 793-799, 1990.
28. Lohmann SM and Walter U. Tracking functions of cGMP-dependent protein kinases (cGK). Front Biosci 10: 1313-1328, 2005.
29. Lum H, Jaffe HA, Schulz IT, Masood A, RayChaudhury A, and Green RD. Expression of PKA inhibitor (PKI) gene abolishes cAMP-mediated protection to endothelial barrier dysfunction. Am J Physiol Cell Physiol 277: C580-C588, 1999.
30. MacMillan-Crow LA, Murphy-Ullrich JE, and Lincoln TM. Identifi-cation and possible localization of cGMP-dependent protein kinase in bovine aortic endothelial cells. Biochem Biophys Res Commun 201: 531-537, 1994.
31. Munzel T, Feil R, Mulsch A, Lohmann SM, Hofmann F, and Walter U. Physiology and pathophysiology of vascular signaling controlled by cyclic guanosine 3′,5′-cyclic monophosphate-dependent protein kinase. Circulation 108: 2172-2183, 2003.
32. Norwood N, Moore TM, Dean DA, Bhattacharjee R, Li M, and Stevens T. Store-operated calcium entry and increased endothelial cell permeability. Am J Physiol Lung Cell Mol Physiol 279: L815-L824, 2000.
33. Oliver JA. Endothelium-derived relaxing factor contributes to the regulation of endothelial permeability. J Cell Physiol 151: 506-511, 1992.
34. Pearse DB and Becker PM. Effect of time and vascular pressure on permeability and cyclic nucleotides in ischemic lungs. Am J Physiol Heart Circ Physiol 279: H2077-H2084, 2000.
35. Pearse DB, Shimoda LA, Verin AD, Bogatcheva N, Moon C, Ronnett GV, Welsh LE, and Becker PM. Effect of cGMP on lung microvascular endothelial barrier dysfunction following hydrogen peroxide. Endothelium 10: 309-317, 2003.
36. Pearse DB, Wagner EM, and Permutt S. Effect of ventilation on vascular permeability and cyclic nucleotide concentrations in ischemic sheep lungs. J Appl Physiol 86: 123-132, 1999.
37. Pinsky DJ, Naka Y, Chowdhury NC, Liao H, Oz MC, Michler RE, Kubaszewski E, Malinski T, and Stern DM. The nitric oxide/cyclic GMP pathway in organ transplantation: critical role in successful lung preservation. Proc Natl Acad Sci USA 91: 12086-12090, 1994.
38. Price CJ and Brindle NP. Vasodilator-stimulated phosphoprotein is involved in stress-fiber and membrane ruffle formation in endothelial cells. Arterioscler Thromb Vasc Biol 20: 2051-2056, 2000.
39. + channels by cGMP in pulmonary vascular endothelial cells. Am J Physiol Lung Cell Mol Physiol 283: L297-L304, 2002.
40. Siflinger-Birnboim A, Goligorsky MS, Del Vecchio PJ, and Malik AB. Activation of protein kinase C pathway contributes to hydrogen peroxide-induced increase in endothelial permeability. Lab Invest 67: 24-30, 1992.
41. 2-induced increase in endothelial permeability. Am J Physiol Lung Cell Mol Physiol 270: L973-L978, 1996.
42. Smolenski A, Bachmann C, Reinhard K, Honig-Liedl P, Jarchau T, Hoschuetzky H, and Walter U. Analysis and regulation of vasodilator-stimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 273: 20029-20035, 1998.
43. Smolenski A, Burkhardt AM, Eigenthaler M, Butt E, Gambaryan S, Lohmann SM, and Walter U. Functional analysis of cGMP-dependent protein kinases I and II as mediators of NO/cGMP effects. Naunyn Schmiedebergs Arch Pharmacol 358: 134-139, 1998.
44. Suttorp N, Hippenstiel S, Fuhrmann M, Krull M, and Podzuweit T. Role of nitric oxide and phosphodiesterase isoenzyme II for reduction of endothelial hyperpermeability. Am J Physiol Cell Physiol 270: C778-C785, 1996.
45. Thomas MK, Francis SH, and Corbin JD. Characterization of a purified bovine lung cGMP-binding cGMP phosphodiesterase. J Biol Chem 265: 14964-14970, 1990.
46. Usatyuk PV and Natarajan V. Regulation of reactive oxygen species-induced endothelial cell-cell and cell-matrix contacts by focal adhesion kinase and adherens junction proteins. Am J Physiol Lung Cell Mol Physiol 289: L999-L1010, 2005.
47. Van Hinsbergh VW and van Nieuw Amerongen GP. Intracellular signalling involved in modulating human endothelial barrier function. J Anat 200: 549-560, 2002.
48. 2+/calmodulin-dependent phosphatase 2B in thrombin-induced endothelial cell contractile responses. Am J Physiol Lung Cell Mol Physiol 275: L788-L799, 1998.
49. Westendorp RG, Draijer R, Meinders AE, and van Hinsbergh VW. Cyclic-GMP-mediated decrease in permeability of human umbilical and pulmonary artery endothelial cell monolayers. J Vasc Res 31: 42-51, 1994.
50. Wojciak-Stothard B, Tsang LYF, and Haworth SG. Rac and Rho play opposing roles in the regulation of hypoxia/reoxygenation-induced permeability changes in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 288: L749-L760, 2005.
51. Wong D, Dorovini-Zis K, and Vincent SR. Cytokines, nitric oxide, and cGMP modulate the permeability of an in vitro model of the human blood-brain barrier. Exp Neurol 190: 446-455, 2004.
52. Wu S, Moore TM, Brough GH, Whitt SR, Chinkers M, Li M, and Stevens T. Cyclic nucleotide-gated channels mediate membrane depolarization following activation of store-operated calcium entry in endothelial cells. J Biol Chem 275: 18887-18896, 2000.
53. Wyatt TA, Lincoln TM, and Pryzwansky KB. Vimentin is transiently co-localized with and phosphorylated by cyclic GMP-dependent protein kinase in formyl-peptide-stimulated neutrophils. J Biol Chem 266: 21274-21280, 1991.
54. Zhang J, Xia SL, Block ER, and Patel JM. NO upregulation of a cyclic nucleotide-gated channel contributes to calcium elevation in endothelial cells. Am J Physiol Cell Physiol 283: C1080-C1089, 2002.