Thrombin enhances the barrier function of rat microvascular endothelium in a PAR-1-dependent manner

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 294, Issue 2, 2008, Pages

  Troyanovsky, B ^a   Alvarez, D F ^a   King, J A ^a   Schaphorst, K L ^a  

^a UNIVERSITY OF SOUTH ALABAMA COLLEGE OF MEDICINE   (United States)

Author keywords

Permeability; Proteinase activated receptor

Indexed keywords

ACTIN; LECTIN; PEPTIDE DERIVATIVE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; SERYLPHENYLALANYLLEUCYLLEUCYLARGINYLASPARAGINAMIDE; THREONYLPHENYLALANYLLEUCYLLEUCYLARGINYLASPARAGINAMIDE; THROMBIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; BLOOD VESSEL REACTIVITY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; GRIFFONIA; GRIFFONIA SIMPLICIFOLIA; IN VITRO STUDY; ISOLATED LUNG; LUNG CIRCULATION; LUNG ENDOTHELIUM; LUNG PERFUSION; MALE; MICROCIRCULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS FIBER; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ACTINS; ANIMALS; BLOOD-AIR BARRIER; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FILTRATION; FLUORESCEIN-5-ISOTHIOCYANATE; GENE EXPRESSION REGULATION; INULIN; LUNG; MALE; PEPTIDES; PERFUSION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PAR-1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THROMBIN;

EID: 39149129997     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00107.2007     Document Type: Article

References (48)

1. Alvarez DF, Gjerde EA, Townsley MI. Role of EETs in regulation of endothelial permeability in rat lung. Am J Physiol Lung Cell Mol Physiol 286: L445-L451, 2004.
2. Alvarez DF, King JA, Weber D, Addison E, Liedtke W, Townsley MI. Transient receptor potential vanilloid 4-mediated disruption of the alveolar septal barrier: a novel mechanism of acute lung injury. Circ Res 99: 988-995, 2006.
3. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 407: 258-264, 2000.
4. 2+-inhibited adenylyl cyclase and phosphodiesterase activities. Am J Physiol Lung Cell Mol Physiol 284: L100-L107, 2003.
5. Curry FE, Zeng M, Adamson RH. Thrombin increases permeability only in venules exposed to inflammatory conditions. Am J Physiol Heart Circ Physiol 285: H2446-H2453, 2003.
6. Dery O, Corvera CU, Steinhoff M, Bunnett NW. Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol Cell Physiol 274: C1429-C1452, 1998.
7. Drake R, Gaar KA, Taylor AE. Estimation of the filtration coefficient of pulmonary exchange vessels. Am J Physiol Heart Circ Physiol 234: H266-H274, 1978.
8. Dudek SM, Garcia JG. Cytoskeletal regulation of pulmonary vascular permeability. J Appl Physiol 91: 1487-1500, 2001.
9. Feistritzer C, Schuepbach RA, Mosnier LO, Bush LA, Di Cera E, Griffin JH, Riewald M. Protective signaling by activated protein C is mechanistically linked to protein C activation on endothelial cells. J Biol Chem 281: 20077-20084, 2006.
10. Finigan JH, Dudek SM, Singleton PA, Chiang ET, Jacobson JR, Camp SM, Ye SQ, Garcia JG. Activated protein C mediates novel lung endothelial barrier enhancement: role of sphingosine 1-phosphate receptor transactivation. J Biol Chem 280: 17286-17293, 2005.
11. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108: 689-701, 2001.
12. 2+ mobilization, barrier dysfunction, prostaglandin synthesis, and platelet-derived growth factor mRNA expression in cultured endothelium. J Cell Physiol 156: 541-549, 1993.
13. Garcia JG, Schaphorst KL, Verin AD, Vepa S, Patterson CE, Natarajan V. Diperoxovanadate alters endothelial cell focal contacts and barrier function: role of tyrosine phosphorylation. J Appl Physiol 89: 2333-2343, 2000.
14. Garcia JG, Siflinger-Birnboim A, Bizios R, Del Vecchio PJ, Fenton JW 2nd, Malik AB. Thrombin-induced increase in albumin permeability across the endothelium. J Cell Physiol 128: 96-104, 1986.
15. Garcia JG, Verin AD, Schaphorst KL. Regulation of thrombin-mediated endothelial cell contraction and permeability. Semin Thromb Hemost 22: 309-315, 1996.
16. Gilchrist A, Vanhauwe JF, Li A, Thomas TO, Voyno-Yasenetskaya T, Hamm HE. Gα minigenes expressing C-terminal peptides serve as specific inhibitors of thrombin-mediated endothelial activation. J Biol Chem 276: 25672-25679, 2001.
17. Guo H, Liu D, Gelbard H, Cheng T, Insalaco R, Fernandez JA, Griffin JH, Zlokovic BV. Activated protein C prevents neuronal apoptosis via protease activated receptors 1 and 3. Neuron 41: 563-572, 2004.
18. Hanson SR, Griffin JH, Harker LA, Kelly AB, Esmon CT, Gruber A. Antithrombotic effects of thrombin-induced activation of endogenous protein C in primates. J Clin Invest 92: 2003-2012, 1993.
19. Hoffmann JN, Vollmar B, Inthorn D, Schildberg FW, Menger MD. The thrombin antagonist hirudin fails to inhibit endotoxin-induced leukocyte/endothelial cell interaction and microvascular perfusion failure. Shock 14: 528-534, 2000.
20. Ishihara H, Zeng D, Connolly AJ, Tam C, Coughlin SR. Antibodies to protease-activated receptor 3 inhibit activation of mouse platelets by thrombin. Blood 91: 4152-4157, 1998.
21. Joris I, Majno G, Corey EJ, Lewis RA. The mechanism of vascular leakage induced by leukotriene E4. Endothelial contraction. Am J Pathol 126: 19-24, 1987.
22. Kahn ML, Zheng YW, Huang W, Bigornia V, Zeng D, Moff S, Farese RV Jr, Tam C, Coughlin SR. A dual thrombin receptor system for platelet activation. Nature 394: 690-694, 1998.
23. King J, Hamil T, Creighton J, Wu S, Bhat P, McDonald F, Stevens T. Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes. Microvasc Res 67: 139-151, 2004.
24. Klinger JR, Warburton R, Carino GP, Murray J, Murphy C, Napier M, Harrington EO. Natriuretic peptides differentially attenuate thrombin-induced barrier dysfunction in pulmonary microvascular endothelial cells. Exp Cell Res 312: 401-410, 2006.
25. Liu F, Schaphorst KL, Verin AD, Jacobs K, Birukova A, Day RM, Bogatcheva N, Bottaro DP, Garcia JG. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rear-rangement: potential role of glycogen synthase kinase-3β. FASEB J 16: 950-962, 2002.
26. Lowe K, Alvarez D, King J, Stevens T. Phenotypic heterogeneity in lung capillary and extra-alveolar endothelial cells. Increased extra-alveolar endothelial permeability is sufficient to decrease compliance. J Surg Res 143: 70-77, 2007.
27. Macfarlane SR, Seatter MJ, Kanke T, Hunter GD, Plevin R. Proteinase-activated receptors. Pharmacol Rev 53: 245-282, 2001.
28. McLaughlin JN, Patterson MM, Malik AB. Protease-activated receptor-3 (PAR3) regulates PAR1 signaling by receptor dimerization. Proc Natl Acad Sci USA 104: 5662-5667, 2007.
29. McLaughlin JN, Shen L, Holinstat M, Brooks JD, Dibenedetto E, Hamm HE. Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 280: 25048-25059, 2005.
30. Minnear FL, Martin D, Hill L, Taylor AE, Malik AB. Lung morphological and permeability changes induced by intravascular coagulation in dogs. Am J Physiol Heart Circ Physiol 253: H634-H644, 1987.
31. Murphy JT, Duffy SL, Hybki DL, Kamm K. Thrombin-mediated permeability of human microvascular pulmonary endothelial cells is calcium dependent. J Trauma 50: 213-222, 2001.
32. O'Brien PJ, Molino M, Kahn M, Brass LF. Protease activated receptors: theme and variations. Oncogene 20: 1570-1581, 2001.
33. Parker JC. Hydraulic conductance of lung endothelial phenotypes and Starling safety factors against edema. Am J Physiol Lung Cell Mol Physiol 292: L378-L380, 2007.
34. Parker JC, Townsley MI. Evaluation of lung injury in rats and mice. Am J Physiol Lung Cell Mol Physiol 286: L231-L246, 2004.
35. Parker JC, Yoshikawa S. Vascular segmental permeabilities at high peak inflation pressure in isolated rat lungs. Am J Physiol Lung Cell Mol Physiol 283: L1203-L1209, 2002.
36. Parkinson JF, Bang NU, Garcia JG. Recombinant human thrombo-modulin attenuates human endothelial cell activation by human thrombin. Arterioscler Thromb 13: 1119-1123, 1993.
37. Riewald M, Ruf W. Science review: role of coagulation protease cascades in sepsis. Crit Care 7: 123-129, 2003.
38. Rohatgi T, Sedehizade F, Sabel BA, Reiser G. Protease-activated receptor subtype expression in developing eye and adult retina of the rat after optic nerve crush. J Neurosci Res 73: 246-254, 2003.
39. Ruf W, Dorfleutner A, Riewald M. Specificity of coagulation factor signaling. J Thromb Haemost 1: 1495-1503, 2003.
40. Stevens T, Creighton J, Thompson WJ. Control of cAMP in lung endothelial cell phenotypes. Implications for control of barrier function. Am J Physiol Lung Cell Mol Physiol 277: L119-L126, 1999.
41. Stevens T, Garcia JG, Shasby DM, Bhattacharya J, Malik AB. Mechanisms regulating endothelial cell barrier function. Am J Physiol Lung Cell Mol Physiol 279: L419-L422, 2000.
42. Taylor FB Jr, Chang A, Esmon CT, D'Angelo A, Vigano-D'Angelo S, Blick KE. Protein C prevents the coagulopathic and lethal effects of Escherichia coli infusion in the baboon. J Clin Invest 79: 918-925, 1987.
43. Taylor FB Jr, Chang A, Hinshaw LB, Esmon CT, Archer LT, Beller BK. A model for thrombin protection against endotoxin. Thromb Res 36: 177-185, 1984.
44. 2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ Res 91: 70-76, 2002.
45. Urban JD, Clarke WP, von Zastrow M, Nichols DE, Kobilka B, Weinstein H, Javitch JA, Roth BL, Christopoulos A, Sexton PM, Miller KJ, Spedding M, Mailman RB. Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320: 1-13, 2007.
46. Van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, 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.
47. Vogel SM, Gao X, Mehta D, Ye RD, John TA, Andrade-Gordon P, Tiruppathi C, Malik AB. Abrogation of thrombin-induced increase in pulmonary microvascular permeability in PAR-1 knockout mice. Physiol Genomics 4: 137-145, 2000.
48. 2+-selective, store-operated current (ISOC) in endothelial cell permeability: determinants of the vascular leak site. Circ Res 96: 856-863, 2005.