Lipopolysaccharide-induced endothelial barrier breakdown is cyclic adenosine monophosphate dependent in vivo and in vitro

Critical Care Medicine

Volumn 37, Issue 5, 2009, Pages 1735-1743

  Schlegel, Nicolas ^a   Baumer, Yvonne ^a   Drenckhahn, Detlev ^a   Waschke, Jens ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

cAMP; Claudin 5; Endothelial barrier; Lipopolysaccharide; Rho GTPases

Indexed keywords

CADHERIN; CLAUDIN 5; CYCLIC AMP; F ACTIN; FORSKOLIN; LIPOPOLYSACCHARIDE; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROLIPRAM;

ANIMAL EXPERIMENT; ARTERY PERMEABILITY; ARTICLE; BACTERIOLYSIS; BLOOD PRESSURE; CONTROLLED STUDY; ENDOTHELIUM; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMODYNAMICS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENTERIC VEIN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD; BLOTTING, WESTERN; CADHERINS; CAPILLARY PERMEABILITY; CELLS, CULTURED; CYCLIC AMP; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FEMALE; HISTOCYTOCHEMISTRY; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICROCIRCULATION; PROBABILITY; RAC1 GTP-BINDING PROTEIN; RANDOM ALLOCATION; RATS; RATS, WISTAR; RHO GTP-BINDING PROTEINS; SENSITIVITY AND SPECIFICITY; STATISTICS, NONPARAMETRIC;

EID: 67650492748     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0b013e31819deb6a     Document Type: Article

References (54)

1. Opal SM: The host response to endotoxin, antilipopolysaccharide strategies, and the management of severe sepsis. Int J Med Microbiol 2007; 297:365-377
2. Medzhitov R: Toll-like receptors and innate immunity. Nat Rev 2001; 1:135-145
3. Majno G, Palade GE: Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: An electron microscopic study. J Biophys Biochem Cytol 1961; 11:571-605
4. Bazzoni G, Dejana E: Endothelial cell-to-cell junctions: Molecular organization and role in vascular homeostasis. Physiol Rev 2004; 84:869-901
5. Waschke J, Curry FE, Adamson RH, et al: Regulation of actin dynamics is critical for endothelial barrier functions. Am J Physiol Heart Circ Physiol 2005; 288:H1296-H1305
6. Wojciak-Stothard B, Ridley AJ: Rho GTPases and the regulation of endothelial permeability. Vascul Pharmacol 2002; 39:187-199
7. Mehta D, Malik AB: Signaling mechanisms regulating endothelial permeability. Physiol Rev 2006; 86:279-367
8. Essler M, Amano M, Kruse HJ, et al: Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem 1998; 273:21867-21874
9. van Nieuw Amerongen GP, van Delft S, Vermeer MA, et al: Activation of RhoA by thrombin in endothelial hyperpermeability: Role of Rho kinase and protein tyrosine kinases. Circ Res 2000; 87:335-340
10. Tasaka S, Koh H, Yamada W, et al: Attenuation of endotoxin-induced acute lung injury by the Rho-associated kinase inhibitor, Y-27632. Am J Respir Cell Mol Biol 2005; 32:504-510
11. Essler M, Staddon JM, Weber PC, et al: Cyclic AMP blocks bacterial lipopolysaccharideinduced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J Immunol 2000; 164:6543-6549
12. Lundblad C, Bentzer P, Grande PO: The permeability-reducing effects of prostacyclin and inhibition of Rho kinase do not counteract endotoxin-induced increase in permeability in cat skeletal muscle. Microvasc Res 2004; 68:286-294
13. McKenzie JA, Ridley AJ: Roles of Rho/ROCK and MLCK in TNF-alpha-induced changes in endothelial morphology and permeability. J Cell Physiol 2007; 213:221-228
14. Majno G, Palade GE, Schoefl GI: Studies on inflammation. II. The site of action of histamine and serotonin along the vascular tree: A topographic study. J Biophys Biochem Cytol 1961; 11:607-626
15. Secchi A, Ortanderl JM, Schmidt W, et al: Effects of dobutamine and dopexamine on hepatic micro- and macrocirculation during experimental endotoxemia: An intravital microscopic study in the rat. Crit Care Med 2001; 29:597-600
16. De Backer D, Creteur J, Dubois MJ, et al: The effects of dobutamine on microcirculatory alterations in patients with septic shock are independent of its systemic effects. Crit Care Med 2006; 34:403-408
17. Waschke J, Drenckhahn D, Adamson RH, et al: Role of adhesion and contraction in Rac 1-regulated endothelial barrier function in vivo and in vitro. Am J Physiol Heart Circ Physiol 2004; 287:H704-H711
18. van Nieuw Amerongen GP, van Hinsbergh VWM: Targets for pharmacological intervention of endothelial hyperpermeability and barrier function. Vascul Pharmacol 2002; 39: 257-272
19. Baumer Y, Drenckhahn D, Waschke J: cAMP induced Rac 1-mediated cytoskeletal reorga- nization in microvascular endothelium. Histochem Cell Biol 2008; 129:765-778
20. Adamson RH, Ly JC, Sarai RK, et al: Epac/ Rap1 pathway regulates microvascular hy-perpermeability induced by PAF in rat mesentery. Am J Physiol Heart Circ Physiol 2008; 294:H1188-H1196
21. Birukova AA, Zagranichnaya T, Alekseeva E, et al: Epac/Rap and PKA are novel mechanisms of ANP-induced Rac-mediated pulmonary endothelial barrier protection. J Cell Physiol 2008; 215:715-724
22. Scheifele DW, Olsen EM, Pendray MR: Endo-toxinemia and thrombocytopenia during neonatal necrotizing enterocolitis. Am J Clin Pathol 1985; 83:227-229
23. Dofferhoff AS, Nijland JH, de Vries-Hospers HG, et al: Effects of different types and combinations of antimicrobial agents on endotoxin release from Gram-negative bacteria: An in-vitro and in-vivo study. Scand J Infect Dis 1991; 23:745-754
24. Baumer Y, Burger S, Curry FE, et al: Differential role of Rho GTPases in endothelial barrier regulation dependent on endothelial cell origin. Histochem Cell Biol 2008; 129: 179-191
25. Schlegel N, Burger S, Golenhofen N, et al: The role of VASP in regulation of cAMP- and Rac 1-mediated endothelial barrier stabilization. Am J Physiol Cell Physiol 2008; 294: C178-C188
26. Waschke J, Baumgartner W, Adamson RH, et al: Requirement of Rac activity for maintenance of capillary endothelial barrier properties. Am J Physiol Heart Circ Physiol 2004; 286:H394-H401
27. Michel CC, Curry FE: Microvascular permeability. Physiol Rev 1999; 79:703-761
28. Huxley VH, Rumbaut RE: The microvasculature as a dynamic regulator of volume and solute exchange. Clin Exp Pharmacol Physiol 2000; 27:847-854
29. Michel CC, Mason JC, Curry FE, et al: A development of the Landis technique for measuring the filtration coefficient of individual capillaries in the frog mesentery. Q J Exp Physiol Cogn Med Sci 1974; 59:283-309
30. Cinel I, Dellinger RP: Advances in pathogenesis and management of sepsis. Curr Opin Infect Dis 2007; 20:345-352
31. Adamson RH, Liu B, Fry GN, et al: Microvascular permeability and number of tight junctions are modulated by cAMP. Am J Physiol 1998; 274(6 Pt 2):H1885-H1894
32. Adamson RH, Curry FE, Adamson G, et al: Rho and rho kinase modulation of barrier properties: Cultured endothelial cells and intact microvessels of rats and mice. J Physiol 2002; 539(Pt 1):295-308
33. Adamson RH, Zeng M, Adamson GN, et al: PAF- and bradykinin-induced hyperpermeability of rat venules is independent of actinmyosin contraction. Am J Physiol Heart Circ Physiol 2003; 285:H406-H417
34. Adamson RH, Ly JC, Sarai RK, et al: Epac/ Rap1 pathway regulates microvascular hyperpermeability induced by PAF in rat mesentery. Am J Physiol Heart Circ Physiol 2008; 294:H1188-H1196
35. Cioffi DL, Moore TM, Schaack J, et al: Dominant regulation of interendothelial cell gap formation by calcium-inhibited type 6 adeny-lyl cyclase. J Cell Biol 2002; 157:1267-1278
36. Stevens T, Nakahashi Y, Cornfield DN, et al: Ca2+-inhibitable adenylyl cyclase modulates pulmonary artery endothelial cell cAMP content and barrier function. Proc Natl Acad Sci USA 1995; 92:2696-2700
37. Risoe PK, Wang Y, Stuestol JF, et al: Lipopolysaccharide attenuates mRNA levels of several adenylyl cyclase isoforms in vivo. Biochim Biophys Acta 2007; 1772:32-39
38. Waschke J, Burger S, Curry FR, et al: Activation of Rac-1 and Cdc42 stabilizes the microvascular endothelial barrier. Histochem Cell Biol 2006; 125:397-406
39. Coimbra R, Melbostad H, Loomis W, et al: LPS-induced acute lung injury is attenuated by phosphodiesterase inhibition: Effects on proinflammatory mediators, metalloproteinases, NF-kappaB, and ICAM-1 expression. J Trauma 2006; 60:115-125
40. Waschke J, Drenckhahn D, Adamson RH, et al: cAMP protects endothelial barrier functions by preventing Rac-1 inhibition. Am J Physiol Heart Circ Physiol 2004; 287: H2427-H2433
41. Peng X, Hassoun PM, Sammani S, et al: Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am JRespir Crit Care Med 2004; 169:1245-1251
42. Birukova AA, Zagranichnaya T, Fu P, et al: Prostaglandins PGE2 and PGI2 promote endothelial barrier enhancement via PKA- and Epac1/Rap1-dependent Rac activation. Exp Cell Res 2007; 313:2504-2520
43. Wojciak-Stothard B, Potempa S, Eichholtz T, et al: Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 2001; 114(Pt 7):1343-1355
44. Goldblum SE, Ding X, Brann TW, et al: Bacterial lipopolysaccharide induces actin reorganization, intercellular gap formation, and endothelial barrier dysfunction in pulmonary vascular endothelial cells: Concurrent F-actin depolymerization and new actin synthesis. J Cell Physiol 1993; 157:13-23
45. Berman RS, Frew JD, Martin W: Endotoxininduced arterial endothelial barrier dysfunction assessed by an in vitro model. Br J Pharmacol 1993; 110:1282-1284
46. Gong P, Angelini DJ, Yang S, et al: TLR4 signaling is coupled to SRC family kinase activation, tyrosine phosphorylation of zonula adherens proteins, and opening of the paracellular pathway in human lung micro-vascular endothelia. J Biol Chem 2008; 283: 13437-13449
47. Veszelka S, Pszti M, Farkas AE, et al: Pentosan polysulfate protects brain endothelial cells against bacterial lipopolysaccharideinduced damages. Neurochem Int 2007; 50: 219-228
48. Bannerman DD, Goldblum SE: Mechanisms of bacterial lipopolysaccharide- induced endothelial apoptosis. Am J Physiol Lung Cell Mol Physiol 2003; 284:L899-L914
49. Ishizaki T, Chiba H, Kojima T, et al: Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain-barrier endothelial cells via protein kinase A-dependent and -independent pathways. Exp Cell Res 2003; 290: 275-288
50. Soma T, Chiba H, Kato-Mori Y, et al: Thr207 of claudin-5 is involved in size-selective loosening of the endothelial barrier by cyclic AMP. Exp Cell Res 2004; 300:202-212
51. Wachtel M, Frei K, Ehler E, et al: Occludin proteolysis and increased permeability in endothelial cells through tyrosine phosphatase inhibition. J Cell Sci 1999; 112:4347-4356
52. Aasen AO, Wang JE: Mediator responses in surgical infections. Surg Infect 2006; 7(Suppl 2):S3-S4
53. Lee J-F, Zeng Q, Ozaki H, et al: Dual roles of tight junction-associated protein, zonula occludens-1, in sphingosine 1-phosphate-mediated endothelial chemotaxis and barrier integrity. J Biol Chem 2006; 281:29190-29200
54. Mertens AE, Rygiel TP, Olivo C, et al: The Rac activator Tiam1 controls tight junction biogenesis in keratinocytes through binding to and activation of the Par polarity complex. J Cell Biol 2005; 170:1029-1037