Epac/Rap and PKA are novel mechanisms of ANP-induced Rac-mediated pulmonary endothelial barrier protection

Journal of Cellular Physiology

Volumn 215, Issue 3, 2008, Pages 715-724

  Birukova, Anna A ^a   Zagranichnaya, Tatiana ^a   Alekseeva, Elena ^a   Bokoch, Gary M ^b   Birukov, Konstantin G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATRIAL NATRIURETIC FACTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE; PROTEIN; PROTEIN TIAM1; PROTEIN VAV2; RAC PROTEIN; RAP1 PROTEIN; RAS PROTEIN; RHO FACTOR; ACTIN; ENZYME INHIBITOR; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; RAPGEF3 PROTEIN, HUMAN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; TIAM1 PROTEIN, HUMAN; VAV PROTEIN; VAV2 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ANALYSIS; HUMAN; HUMAN CELL; LUNG ENDOTHELIUM; PRIORITY JOURNAL; PROTEIN FUNCTION; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; ENDOTHELIUM CELL; ENZYMOLOGY; LUNG; LUNG GAS EXCHANGE; METABOLISM; PATHOLOGY; STRESS FIBER;

ACTINS; ATRIAL NATRIURETIC FACTOR; BLOOD-AIR BARRIER; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ENZYME INHIBITORS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; LUNG; MONOMERIC GTP-BINDING PROTEINS; PROTO-ONCOGENE PROTEINS C-VAV; RAC GTP-BINDING PROTEINS; RHO GTP-BINDING PROTEINS; STRESS FIBERS; THROMBIN;

EID: 42949131177     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21354     Document Type: Article

References (75)

1. Aghazadeh B, Lowry WE, Huang XY, Rosen MK. 2000. Structural basis for relief of autoinhibition of the Dbl homology domain of proto-oncogene Vav by tyrosine phosphorylation. Cell 102:625-633.
2. Ahluwalia A, MacAllister RJ, Hobbs AJ. 2004. Vascular actions of natriuretic peptides. Cyclic GMP-dependent and -independent mechanisms. Basic Res Cardiol 99:83-89.
3. Arthur WT, Quilliam LA, Cooper JA. 2004. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J Cell Biol 167:111-122.
4. Baxter GF. 2004. The natriuretic peptides. Basic Res Cardiol 99:71-75.
5. Birukov KG, Bochkov VN, Birukova AA, Kawkitinarong K, Rios A, Leitner A, Verin AD, Bokoch GM, Leitinger N. Garcia JG. 2004. Epoxycyclopentenone- containing oxidized phospholipids restore endothelial barrier function via Cdc42 and Rac. Circ Res 95:892-901.
6. Birukova AA, Birukov KG, Smurova K, Adyshev DM, Kaibuchi K, Alieva I, Garcia JG, Verin AD. 2004a. Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB J 18:1879-1890.
7. Birukova AA, Liu F, Garcia JG, Verin AD. 2004b. Protein kinase A attenuates endothelial cell barrier dysfunction induced by microtubule disassembly. Am J Physiol Lung Cell Mol Physiol 287:L86-L93.
8. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JGN, Verin AD. 2004c. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 67:64-77.
9. Birukova AA, Adyshev D, Gorshkov B, Birukov KG, Verin AD. 2005a. ALK5 and Smad4 are involved in TGF-beta1-induced pulmonary endothelial permeability. FEBS Lett 579:4031-4037.
10. Birukova AA, Birukov KG, Gorshkov B, Liu F, Garcia JG, Verin AD. 2005b. MAP kinases in lung endothelial permeability induced by microtubule disassembly. Am J Physiol Lung Cell Mol Physiol 289:L75-L84.
11. Birukova AA, Adyshev D, Gorshkov B, Bokoch GM, Birukov KG, Verin AA. 2006a. GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 290:L540-L548.
12. Birukova AA, Chatchavalvanich S, Rios A, Kawkitinarong K, Garcia JG, Birukov KG. 2006b. Differential regulation of pulmonary endothelial monolayer integrity by varying degrees of cyclic stretch. Am J Pathol 168:1749-1761.
13. Birukova AA, Zagranichnaya T, Alekseeva E, Fu P, Chen W, Jacobson JR, Birukov KG. 2007. Prostaglandins PGE2 and PGI2 promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp Cell Res 313:2504-2520.
14. Bishop AL, Hall A. 2000. Rho GTPases and their effector proteins. Biochem J 348:241-255.
15. Boguski MS, McCormick F. 1993. Proteins regulating Ras and its relatives. Nature 366:643-654.
16. Bokoch GM. 2003. Biology of the p21-activated kinases. Annu Rev Biochem 72:743-781.
17. Bos JL. 2003. Epac: A new cAMP target and new avenues in cAMP research. Nat Rev Mol Cell Biol 4:733-738.
18. Browner NC, Dey NB, Bloch KD, Lincoln TM. 2004a. Regulation of cGMP-dependent protein kinase expression by soluble guanylyl cyclase in vascular smooth muscle cells. J Biol Chem 279:46631-46636.
19. Browner NC, Sellak H, Lincoln TM. 2004b. Downregulation of cGMP-dependent protein kinase expression by inflammatory cytokines in vascular smooth muscle cells. Am J Physiol Cell Physiol 287:C88-C96.
20. Bustelo XR. 2000. Regulatory and signaling properties of the Vav family. Mol Cell Biol 20:1461-1477.
21. Christensen AE, Selheim F, de Rooij J, Dremier S, Schwede F, Dao KK, Martinez A, Maenhaut C, Bos JL, Genieser HG, Doskeland SO. 2003. cAMP analog mapping of Epac1 and cAMP kinase. Discriminating analogs demonstrate that Epac and cAMP kinase act synergistically to promote PC-12 cell neurite extension. J Biol Chem 278:35394-35402.
22. Cornwell TL, Arnold E, Boerth NJ, Lincoln TM. 1994. Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP. Am J Physiol 267:C1405-C1413.
23. Cullere X, Shaw SK, Andersson L, Hirahashi J, Luscinskas FW, Mayadas TN. 2005. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 105:1950-1955.
24. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, Bos JL. 1998. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396:474-477.
25. Dong JM, Leung T, Manser E, Lim L. 1998. cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKalpha. J Biol Chem 273:22554-22562.
26. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
27. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, Aepfelbacher M. 1998. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 273:21867-21874.
28. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N. 2005. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 25:136-146.
29. Furst R, Brueckl C, Kuebler WM, Zahler S, Krotz F, Gorlach A, Vollmar AM, Kiemer AK. 2005. Atrial natriuretic peptide induces mitogen-activated protein kinase phosphatase-1 in human endothelial cells via Rac1 and NAD(P)H oxidase/Nox2-activation. Circ Res 96:43-53.
30. Gampel A, Mellor H. 2002. Small interfering RNAs as a tool to assign Rho GTPase exchange-factor function in vivo. Biochem J 366:393-398.
31. Gao Y, Portugal AD, Negash S, Zhou W, Longo LD, Usha Raj J. 2007. Role of Rho kinases in PKG-mediated relaxation of pulmonary arteries of fetal lambs exposed to chronic high altitude hypoxia. Am J Physiol Lung Cell Mol Physiol 292:L678-L684.
32. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. 2001. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108:689-701.
33. Gebb S, Stevens T. 2004. On lung endothelial cell heterogeneity. Microvasc Res 68:1-12.
34. Herbrand U, Ahmadian MR. 2006. p190-RhoGAP as an integral component of the Tiam1/ Rac1-induced down regulation of Rho. Biol Chem 387:311-317.
35. Irwin DC, Rhodes J, Baker DC, Nelson SE, Tucker A. 2001. Atrial natriuretic peptide blockade exacerbates high altitude pulmonary edema in endotoxin-primed rats. High Alt Med Biol 2:349-360.
36. Irwin DC, Tissot van Patot MC, Tucker A, Bowen R. 2005. Direct ANP inhibition of hypoxia-induced inflammatory pathways in pulmonary microvascular and macrovascular endothelial monolayers. Am J Physiol Lung Cell Mol Physiol 288:L849-L859.
37. Kishi Y, Ashikaga T, Watanabe R, Numano F. 1994. Atrial natriuretic peptide reduces cyclic AMP by activating cyclic GMP-stimulated phosphodiesterase in vascular endothelial cells. J Cardiovasc Pharmacol 24:351-357.
38. Klinger JR, Warburton R, Carino GP, Murray J, Murphy C, Napier M, Harrington EO. 2006. Natriuretic peptides differentially attenuate thrombin-induced barrier dysfunction in pulmonary microvascular endothelial cells. Exp Cell Res 312:401-410.
39. Koller KJ, Goeddel DV. 1992. Molecular biology of the natriuretic peptides and their receptors. Circulation 86:1081-1088.
40. Kooistra MR, Corada M, Dejana E, Bos JL. 2005. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett 579:4966-4972.
41. Kouklis P, Konstantoulaki M, Vogel S, Broman M, Malik AB. 2004. Cdc42 regulates the restoration of endothelial barrier function. Circ Res 94:159-166.
42. Kulhanek-Heinze S, Gerbes AL, Gerwig T, Vollmar AM, Kiemer AK. 2004. Protein kinase A dependent signalling mediates anti-apoptotic effects of the atrial natriuretic peptide in ischemic livers. J Hepatol 41:414-420.
43. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, Bertoglio J. 1996. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15:510-519.
44. Liu F, Verin AD, Borbiev T, Garcia JG. 2001. Role of cAMP-dependent protein kinase A activity in endothelial cell cytoskeleton rearrangement. Am J Physiol Lung Cell Mol Physiol 280:L1309-L1317.
45. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, Day RM, Bogatcheva N, Bottaro DP, Garcia JG. 2002. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: Potential role of glycogen synthase kinase-3beta. FASEB J 16:950-962.
46. Liu S, Ma X, Gong M, Shi L, Lincoln T, Wang S. 2007. Glucose down-regulation of cGMP-dependent protein kinase I expression in vascular smooth muscle cells involves NAD(P)H oxidase-derived reactive oxygen species. Free Radic Biol Med 42:852-863.
47. Mackie K, Lai Y, Nairn AC, Greengard P, Pitt BR, Lazo JS. 1986. Protein phosphorylation in cultured endothelial cells. J Cell Physiol 128:367-374.
48. Majumdar M, Seasholtz TM, Goldstein D, de Lanerolle P, Brown JH. 1998. Requirement for Rho-mediated myosin light chain phosphorylation in thrombin-stimulated cell rounding and its dissociation from mitogenesis. J Biol Chem 273:10099-10106.
49. Malliri A, van Es S, Huveneers S, Collard JG. 2004. The Rac exchange factor Tiam1 is required for the establishment and maintenance of cadherin-based adhesions. J Biol Chem 279:30092-30098.
50. Mehta D, Malik AB. 2006. Signaling mechanisms regulating endothelial permeability. Physiol Rev 86:279-367.
51. Mitaka C, Hirata Y, Nagura T, Tsunoda Y, Amaha K. 1998. Beneficial effect of atrial natriuretic peptide on pulmonary gas exchange in patients with acute lung injury. Chest 114:223-228.
52. Moldobaeva A, Welsh-Servinsky LE, Shimoda LA, Stephens RS, Verin AD, Tuder RM, Pearse DB. 2005. Role of Protein Kinase G in barrier protective effects of cGMP in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol.
53. Nakayama T, Harada N, Asano M, Nomura N, Saito T, Mishima A, Okajima K. 2007. Atrial natriuretic peptide reduces ischemia/reperfusion-induced spinal cord injury in rats by enhancing sensory neuron activation. J Pharmacol Exp Ther 322:582-590.
54. O'Connor KL, Mercurio AM. 2001. Protein kinase A regulates Rac and is required for the growth factor-stimulated migration of carcinoma cells. J Biol Chem 276:47895-47900.
55. Parker JC. 2000. Inhibitors of myosin light chain kinase and phosphodiesterase reduce ventilator-induced lung injury. J Appl Physiol 89:2241-2248.
56. Price LS, Hajdo-Milasinovic A, Zhao J, Zwartkruis FJ, Collard JG, Bos JL. 2004. Rap1 regulates E-cadherin-mediated cell-cell adhesion. J Biol Chem 279:35127-35132.
57. Qiao J, Huang F, Lum H. 2003. PKA inhibits RhoA activation: A protection mechanism against endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 284:L972-L980.
58. Rangarajan S, Enserink JM, Kuiperij HB, de Rooij J, Price LS, Schwede F, Bos JL. 2003. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol 160:487-493.
59. Rosenfeldt H, Castellone MD, Randazzo PA, Gutkind JS. 2006. Rac inhibits thrombin-induced Rho activation: Evidence of a Pak-dependent GTPase crosstalk. J Mol Signal 1:8.
60. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P. 1999. Inhibition of myosin light chain kinase by p21-activated kinase [see comments]. Science 283:2083-2085.
61. Sanghi S, Kumar R, Smith M, Baker KM, Dostal DE. 2005. Activation of protein kinase A by atrial natriuretic peptide in neonatal rat cardiac fibroblasts: Role in regulation of the local renin-angiotensin system. Regul Pept 132:1-8.
62. Sayner SL, Alexeyev M, Dessauer CW, Stevens T. 2006. Soluble adenylyl cyclase reveals the significance of cAMP compartmentation on pulmonary microvascular endothelial cell barrier. Circ Res 98:675-681.
63. Schumacher H, Muller D, Mukhopadhyay AK. 1992. Stimulation of testosterone production by atrial natriuretic peptide in "isolated mouse Leydig cells results from a promiscuous activation of cyclic AMP-dependent protein kinase by cyclic GMP. Mol Cell Endocrinol 90:47-52.
64. Shikata Y, Birukov KG, Birukova AA, Verin AD, Garcia JG. 2003. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: Role of Sre and GIT. FASEB J 17:2240-2249.
65. Surapisitchat J, Jeon KI, Yan C, Beavo JA. 2007. Differential regulation of endothelial cell permeability by cGMP via phosphodiesterases 2 and 3. Circ Res 101:811-818.
66. Tanabe M, Ueda M, Endo M, Kitajima M. 1996. The effect of atrial natriuretic peptide on pulmonary acid injury in a pig model. Am J Respir Crit Care Med 154:1351-1356.
67. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW. 2000. Activation of RhoA by thrombin in endothelial hyperpermeability: Role of Rho kinase and protein tyrosine kinases. Circ Res 87:335-340.
68. von Lintig FC, Pilz RB, Boss GR. 2000. Quantitative determination of Rap1 activation in cyclic nucleotide-treated HL-60 leukemic cells: Lack of Rap1 activation in variant cells. Oncogene 19:4029-4034.
69. Vouret-Craviari V, Boquet P, Pouyssegur J, Van Obberghen-Schilling E. 1998. Regulation of the actin cytoskeleton by thrombin in human endothelial cells: Role of Rho proteins in endothelial barrier function. Mol Biol Cell 9:2639-2653.
70. Wong KW, Mohammadi S, Isberg RR. 2006. Disruption of RhoGDI and RhoA regulation by a Rac1 specificity switch mutant. J Biol Chem 281:40379-40388.
71. Yonemaru M, Ishii K, Murad F, Raffin TA. 1992. Atriopeptin-induced increases in endothelial cell permeability are associated with elevated cGMP levels. Am J Physiol 263:L363-L369.
72. Yuan Y, Huang Q, Wu HM. 1997. Myosin light chain phosphorylation: Modulation of basal and agonist-stimulated venular permeability. Am J Physiol 272:H1437-H1443.
73. Zeng Y, Zhuang S, Gloddek J, Tseng CC, Boss GR, Pilz RB. 2006. Regulation of cGMP-dependent protein kinase expression by Rho and Kruppel-like transcription factor-4. J Biol Chem 281:16951-16961.
74. Zheng Y. 2001. Dbl family guanine nucleotide exchange factors. Trends Biochem Sci 26:724-732.
75. Zhou W, Dasgupta C, Negash S, Raj JU. 2007. Modulation of pulmonary vascular smooth muscle cell phenotype in hypoxia: Role of cGMP-dependent protein kinase. Am J Physiol Lung Cell Mol Physiol 292:L1459-L1466.