cAMP induced Rac 1-mediated cytoskeletal reorganization in microvascular endothelium

Histochemistry and Cell Biology

Volumn 129, Issue 6, 2008, Pages 765-778

  Baumer, Y ^a   Drenckhahn, D ^a   Waschke, J ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

cAMP; Endothelial barrier functions; Epac; Rho GTPase

Indexed keywords

CADHERIN; CLAUDIN 5; CYCLIC AMP; CYTOTOXIC NECROTIZING FACTOR 1; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN;

ARTICLE; CELL JUNCTION; CONTROLLED STUDY; CYTOSKELETON; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM;

ANTIGENS, CD; CADHERINS; CELL POLARITY; CELLS, CULTURED; CYCLIC AMP; CYTOSKELETON; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FORSKOLIN; HUMANS; MEMBRANE PROTEINS; MICROCIRCULATION; PROTEIN TRANSPORT; RAC1 GTP-BINDING PROTEIN; RHOA GTP-BINDING PROTEIN; ROLIPRAM; SKIN; THROMBIN;

EID: 44149106107     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-008-0422-y     Document Type: Article

References (47)

1. Adamson RH, Liu B, Fry GN, Rubin LL, Curry FE (1998) Microvascular permeability and number of tight junctions are modulated by cAMP. Am J Physiol 274:H1885-H1894
2. Adamson RH, Curry FE, Adamson G, Liu B, Jiang Y, Aktories K, Barth H, Daigeler A, Golenhofen N, Ness W, Drenckhahn D (2002) Rho and rho kinase modulation of barrier properties: cultured endothelial cells and intact microvessels of rats and mice. J Physiol 539:295-308
3. Adamson RH, Zeng M, Adamson GN, Lenz JF, Curry FE (2003) PAF- and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction. Am J Physiol Heart Circ Physiol 285:H406-H417
4. Adamson RH, Ly JC, Sarai RK, Lenz JF, Altangerel A, Drenckhahn D, Curry FR (2008) Epac/Rap1 pathway regulates microvascular hyperpermeability induced by PAF in rat mesentery. Am J Physiol Heart Circ Physiol (in press)
5. Baumer Y, Burger S, Curry FE, Golenhofen N, Drenckhahn D, Waschke J (2008) Differential role of Rho GTPases in endothelial barrier regulation dependent on endothelial cell origin. Histochem Cell Biol 129:179-191
6. Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84:869-901
7. Birukova AA, Zagranichnaya T, Alekseeva E, Bokoch GM, Birukov KG (2007) Epac/Rap and PKA are novel mechanisms of ANP-induced Rac-mediated pulmonary endothelial barrier protection. J Cell Physiol 215(3):715-724
8. Blume C, Benz PM, Walter U, Ha J, Kemp BE, Renne T (2007) AMP-activated protein kinase impairs endothelial actin cytoskeleton assembly by phosphorylating vasodilator-stimulated phosphoprotein. J Biol Chem 282:4601-4612
9. Bustelo XR, Sauzeau V, Berenjeno IM (2007) GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays 29:356-370
10. 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
11. Cioffi DL, Moore TM, Schaack J, Creighton JR, Cooper DM, Stevens T (2002) Dominant regulation of interendothelial cell gap formation by calcium-inhibited type 6 adenylyl cyclase. J Cell Biol 157:1267-1278
12. 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
13. Curry FE (2002) Microvascular injury: mechanisms and modulation. Int J Angiol 11:1-6
14. Dormond O, Ruegg C (2003) Regulation of endothelial cell integrin function, angiogenesis by COX-2, cAMP and Protein Kinase A. Thromb Haemost 90:577-585
15. Ellerbroek SM, Wennerberg K, Burridge K (2003) Serine phosphorylation negatively regulates RhoA in vivo. J Biol Chem 278:19023-19031
16. 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
17. 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. Molec Cell Biol 25:136-146
18. 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
19. Halbrugge M, Friedrich C, Eigenthaler M, Schanzenbacher P, Walter U (1990) Stoichiometric and reversible phosphorylation of a 46-kDa protein in human platelets in response to cGMP- and cAMP-elevating vasodilators. J Biol Chem 265:3088-3093
20. Hartmann C, Zozulya A, Wegener J, Galla HJ (2007) The impact of glia-derived extracellular matrices on the barrier function of cerebral endothelial cells: an in vitro study. Exp Cell Res 313:1318-1325
21. 2-induced filamin redistribution in endothelial cells is modulated by the cyclic AMP-dependent protein kinase pathway. J Cell Physiol 172:373-381
22. Holz GG, Kang G, Harbeck M, Roe MW, Chepurny OG (2006) Cell physiology of cAMP sensor Epac. J Physiol 577:5-15
23. Hoshino T, Sakisaka T, Baba T, Yamada T, Kimura T, Takai Y (2005) Regulation of E-cadherin endocytosis by nectin through afadin, Rap1, and p120ctn. J Biol Chem 280:24095-24103
24. Jacobson JR, Dudek SM, Singleton PA, Kolosova IA, Verin AD, Garcia JG (2006) Endothelial cell barrier enhancement by ATP is mediated by the small GTPase Rac and cortactin. Am J Physiol 291:L289-L295
25. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Ann Rev of Cell Dev Biol 21:247-269
26. Kooistra MR, Corada M, Dejana E, Bos JL (2005) Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett 579:4966-4972
27. Kooistra MR, Dube N, Bos JL (2007) Rap1: a key regulator in cell-cell junction formation. J Cell Sci 120:17-22
28. Kyhse-Andersen J (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods 10:203-209
29. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
30. Lorenowicz MJ, Fernandez-Borja M, Hordijk PL (2007) cAMP signaling in leukocyte transendothelial migration. Arteriosclerosis Thrombosis Vasc Biol 27:1014-1022
31. Majumdar M, Seasholtz TM, Buckmaster C, Toksoz D, Brown JH (1999) A rho exchange factor mediates thrombin and Galpha(12)-induced cytoskeletal responses. J Biol Chem 274:26815-26821
32. Mehta D, Malik AB (2006) Signaling mechanisms regulating endothelial permeability. Physiol Rev 86:279-367
33. Mehta D, Rahman A, Malik AB (2001) Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J Biol Chem 276:22614-22620
34. Michel CC, Curry FE (1999) Microvascular permeability. Physiol Rev 79:703-761
35. Nishikawa M, de Lanerolle P, Lincoln TM, Adelstein RS (1984) Phosphorylation of mammalian myosin light chain kinases by the catalytic subunit of cyclic AMP-dependent protein kinase and by cyclic GMP-dependent protein kinase. J Biol Chem 259:8429-8436
36. 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
37. Qiao J, Huang F, Lum H (2003) PKA inhibits RhoA activation: a protection mechanism against endothelial barrier dysfunction. Am J Physiol 284:L972-L980
38. Rosenberger P, Khoury J, Kong T, Weissmuller T, Robinson AM, Colgan SP (2007) Identification of vasodilator-stimulated phosphoprotein (VASP) as an HIF-regulated tissue permeability factor during hypoxia. Faseb J 21:2613-2621
39. Schlegel N, Burger S, Golenhofen N, Walter U, Drenckhahn D, Waschke J (2008) The role of VASP in regulation of cAMP- and Rac 1-mediated endothelial barrier stabilization. Am J Physiol Cell Physiol 294:C178-C188
40. Stelzner TJ, Weil JV, O'Brien RF (1989) Role of cyclic adenosine monophosphate in the induction of endothelial barrier properties. J Cell Physiol 139:157-166
41. Tiruppathi C, Malik AB, Del Vecchio PJ, Keese CR, Giaever I (1992) Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc Natl Acad Sci USA 89:7919-7923
42. van Nieuw Amerongen GP, van Hinsbergh VW (2002) Targets for pharmacological intervention of endothelial hyperpermeability and barrier function. Vascul Pharmacol 39:257-272
43. Vouret-Craviari V, Bourcier C, Boulter E, van Obberghen-Schilling E (2002) Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J Cell Sci 115:2475-2484
44. Waschke J, Baumgartner W, Adamson RH, Zeng M, Aktories K, Barth H, Wilde C, Curry FE, Drenckhahn D (2004a) Requirement of Rac activity for maintenance of capillary endothelial barrier properties. Am J Physiol Heart Circ Physiol 286:H394-H401
45. Waschke J, Curry FE, Adamson RH, Drenckhahn D (2005) Regulation of actin dynamics is critical for endothelial barrier functions. Am J Physiol Heart Circ Physiol 288:H1296-H1305
46. Waschke J, Drenckhahn D, Adamson RH, Barth H, Curry FE (2004b) cAMP protects endothelial barrier functions by preventing Rac-1 inhibition. Am J Physiol Heart Circ Physiol 287:H2427-H2433
47. Wojciak-Stothard B, Ridley AJ (2002) Rho GTPases and the regulation of endothelial permeability. Vascul Pharmacol 39:187-199