PKA inhibits RhoA activation: A protection mechanism against endothelial barrier dysfunction

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 284, Issue 6 28-6, 2003, Pages

  Qiao, Jing ^a   Huang, Fei ^a   Lum, Hazel ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Endothelial resistance; Guanine nucleotide dissociation inhibitor; Protein kinase A inhibitor; Rho guanosine 5 triphosphate

Indexed keywords

ADENOVIRUS VECTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANOSINE TRIPHOSPHATASE; PROTEIN CDC42; RAC1 PROTEIN; RHO KINASE; RHOA KINASE; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; BLOOD VESSEL PERMEABILITY; CELL MEMBRANE; CELL PROTECTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFLAMMATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 0038172667     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00429.2002     Document Type: Article

References (47)

1. Adamson P, Marshall CJ, Hall A, and Tilbrook PA. Posttranslational modifications of p21rho proteins. J Biol Chem 267: 20033-20038, 1992.
2. Adamson RH, Curry FE, Adamson G, Liu B, Jiang Y, Aktories K, Barth H, Daigeler A, Golenhofen N, Ness W, and Drenckhahn D. Rho and rho kinase modulation of barrier properties: cultured endothelial cells and intact microvessels of rats and mice. J Physiol 539: 295-308, 2002.
3. Ades EW, Candal FJ, Swerlick RA, George VG, Summers S, Bosse DC, and Lawley TJ. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99: 683-690, 1992.
4. Adkins WK, Barnard JW, May S, Seibert AF, Haynes J, and Taylor AE. Compounds that increase cAMP prevent ischemiareperfusion pulmonary capillary injury. J Appl Physiol 72: 492-497, 1992.
5. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, and Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271: 20246-20249, 1996.
6. Aspenstrom P. Effectors for the Rho GTPases. Curr Opin Cell Biol 11: 95-102, 1999.
7. Bourmeyster N and Vignais PV. Phosphorylation of Rho GDI stabilizes the Rho A-Rho GDI complex in neutrophil cytosol. Biochem Biophys Res Commun 218: 54-60, 1996.
8. Busca R, Abbe P, Mantoux F, Aberdam E, Peyssonnaux C, Eychene A, Ortonne JP, and Ballotti R. Ras mediates the cAMP-dependent activation of extracellular signal-regulated kinases (ERKs) in melanocytes. EMBO J 19: 2900-2910, 2000.
9. Carbajal JM and Schaeffer RC Jr. RhoA inactivation enhances endothelial barrier function. Am J Physiol Cell Physiol 277: C955-C964, 1999.
10. Casnocha SA, Eskin SG, Hall ER, and McIntire LV. Permeability of human endothelial monolayers: effect of vasoactive agonists and cAMP. J Appl Physiol 67: 1997-2005, 1989.
11. De Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, and Bos JL. Epac is a Rapl guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396: 474-477, 1998.
12. Dong JM, Leung T, Manser E, and Lim L. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKα. J Biol Chem 273: 22554-22562, 1998.
13. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, and Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 273: 21867-21874, 1998.
14. Essler M, Staddon JM, Weber PC, and Aepfelbacher M. Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J Immunol 164: 6543-6549, 2000.
15. Etienne-Manneville S and Hall A. Rho GTPases in cell biology. Nature 420: 629-635, 2002.
16. 2 adenosine receptors in human mast cells. Mol Pharmacol 58: 903-910, 2000.
17. Ferro T, Neumann P, Gertzberg N, Clements R, and Johnson A. Protein kinase C-α mediates endothelial barrier dysfunction induced by TNF-α. Am J Physiol Lung Cell Mol Physiol 278: L1107-L1117, 2000.
18. Garcia JG, Lazar V, Gilbert-McClain LI, Gallagher PJ, and Verin AD. Myosin light chain kinase in endothelium: molecular cloning and regulation. Am J Respir Cell Mol Biol 16: 489-494, 1997.
19. 2+ mobilization, barrier dysfunction, prostaglandin synthesis, and platelet-derived growth factor mRNA expression in cultured endothelium. J Cell Physiol 156: 541-549, 1993.
20. Garcia JG, Verin AD, Schaphorst K, Siddiqui R, Patterson CE, Csortos C, and Natarajan V. Regulation of endothelial cell myosin light chain kinase by Rho, cortactin, and p60(src). Am J Physiol Lung Cell Mol Physiol 276: L989-L998, 1999.
21. Giaever I and Keese CR. Micromotion of mammalian cells measured electrically. Proc Natl Acad Sci USA 88: 7896-7900, 1991. [Corrigendum. Proc Natl Acad Sci USA 90: February 1993, p. 1634.]
22. Gorvel JP, Chang TC, Boretto J, Azuma T, and Chavrier P. Differential properties of D4/LyGDI versus RhoGDI: phosphorylation and rho GTPase selectivity. FEBS Lett 422: 269-273, 1998.
23. Hippenstiel S, Kratz T, Krull M, Seybold J, von Eichel-Streiber C, and Suttorp N. Rho protein inhibition blocks protein kinase C translocation and activation. Biochem Biophys Res Commun 245: 830-834, 1998.
24. Hirase T, Kawashima S, Wong EY, Ueyama T, Rikitake Y, Tsukita S, Yokoyama M, and Staddon JM. Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J Biol Chem 276: 10423-10431, 2001.
25. Hurst VI, Goldberg PL, Minnear FL, Heimark RL, and Vincent PA. Rearrangement of adherens junctions by transforming growth factor-β1: role of contraction.Am J Physiol Lung Cell Mol Physiol 276: L582-L595, 1999.
26. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, Housman DE, and Graybiel AM. A family of cAMP-binding proteins that directly activate Rapl. Science 282: 2275-2279, 1998.
27. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, and Bertoglio J. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15: 510-519, 1996.
28. Laudanna C, Campbell JJ, and Butcher EC. Elevation of intracellular cAMP inhibits RhoA activation and integrin-dependent leukocyte adhesion induced by chemoattractants. J Biol Chem 272: 24141-24144, 1997.
29. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH, Kluk M, Volpi M, Sha'afi RI, and Hla T. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 99: 301-312, 1999.
30. Lum H, Andersen TT, Siflinger-Birnboim A, Tiruppathi C, Goligorsky MS, Fenton JW, and Malik AB. Thrombin receptor peptide inhibits thrombin-induced increase in endothelial permeability by receptor desensitization. J Cell Biol 120: 1491-1499, 1993.
31. Lum H, Hao Z, Gayle D, Kumar P, Patterson CE, and Uhler MD. Vascular endothelial cells express isoforms of protein kinase A inhibitor. Am J Physiol Cell Physiol 282: C59-C66, 2002.
32. 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.
33. Lum H and Malik AB. Regulation of vascular endothelial barrier function. Am J Physiol Lung Cell Mol Physiol 267: L223-L241, 1994.
34. Lum H and Malik AB. Mechanisms of increased endothelial permeability. Can J Physiol Pharmacol 74: 787-800, 1996.
35. Lum H and Roebuck KA. Oxidant stress and endothelial cell dysfunction. Am J Physiol Cell Physiol 280: C719-C741, 2001.
36. Mehta D, Rahman A, and Malik AB. Protein kinase C-α signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J Biol Chem 276: 22614-22620, 2001.
37. Molnar G, Dagher MC, Geiszt M, Settleman J, and Ligeti E. Role of prenylation in the interaction of Rho-family small GTPases with GTPase activating proteins. Biochemistry 40: 10542-10549, 2001.
38. Moy AB, Bodmer JE, Blackwell K, Shasby S, and Shasby DM. cAMP protects endothelial barrier function independent of inhibiting MLC20-dependent tension development. Am J Physiol Lung Cell Mol Physiol 274: L1024-L1029, 1998.
39. Moy AB, VanEngelenhoven J, Bodmer J, Kamath J, Keese C, Giaever I, Shasby S, and Shasby DM. Histamine and thrombin modulate endothelial focal adhesion through centripetal and centrifugal forces. J Clin Invest 97: 1020-1027, 1996.
40. Nieuw Amerongen GP, Draijer R, Vermeer MA, and van Hinsbergh VW. Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ Res 83: 1115-1123, 1998.
41. Niggli V. Rho-kinase in human neutrophils: a role in signalling for myosin light chain phosphorylation and cell migration. FEBS Lett 445: 69-72, 1999.
42. Ochoa L, Waypa G, Mahoney JR Jr, Rodriguez L, and Minnear FL. Contrasting effects of hypochlorous acid and hydrogen peroxide on endothelial permeability: prevention with cAMP drugs. Am J Respir Crit Care Med 156: 1247-1255, 1997.
43. Patterson CE, Lum H, Schaphorst KL, Verin AD, and Garcia JG. Regulation of endothelial barrier function by the cAMP-dependent protein kinase. Endothelium 7: 287-308, 2000.
44. Snedecor GW and Cochran WG. Statistical Methods. Ames, IA: Iowa State University Press, 1967.
45. Van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, and van Hinsbergh VW. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res 87: 335-340, 2000.
46. Wojciak-Stothard B, Entwistle A, Garg R, and Ridley AJ. Regulation of TNF-α-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells. J Cell Physiol 176: 150-165, 1998.
47. Wojciak-Stothard B, Potempa S, Eichholtz T, and Ridley AJ. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 114: 1343-1355, 2001.