Role of Antithrombin and Factor XIII In Leukocyte-Independent Plasma Extravasation During Endotoxemia: An Intravital-Microscopic Study in the Rat

Journal of Surgical Research

Volumn 136, Issue 2, 2006, Pages 219-226

  Czabanka, Marcus ^a   Martin, Eike ^a   Walther, Andreas ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

antithrombin; endotoxin; factor XIII; fucoidin; macromolecular efflux; microcirculation

Indexed keywords

ANTITHROMBIN; ANTITHROMBIN III CONCENTRATE; BLOOD CLOTTING FACTOR 13; BLOOD CLOTTING FACTOR 13 CONCENTRATE; FUCOIDIN; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOTOXEMIA; EXTRAVASATION; MACROMOLECULE; MALE; MESENTERIC VEIN; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; SHEAR RATE; STATISTICAL SIGNIFICANCE; VENULE;

ANIMALS; ANTICOAGULANTS; ANTITHROMBIN III; BLOOD PLATELETS; CAPILLARY PERMEABILITY; CELL COMMUNICATION; ENDOTHELIAL CELLS; ENDOTOXEMIA; FACTOR XIII; LEUKOCYTES; LIPOPOLYSACCHARIDES; MACROMOLECULAR SUBSTANCES; MALE; MICROSCOPY, FLUORESCENCE; POLYSACCHARIDES; RATS; RATS, WISTAR; SPLANCHNIC CIRCULATION; VENULES;

EID: 33751066116     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2005.11.574     Document Type: Article

References (63)

1. Bone R.C. Inhibitors of complement and neutrophils: a critical evaluation of their role in the treatment of sepsis. Crit Care Med 20 (1992) 891
2. Redl H., Nikolai A., Kneidinger R., and Schlag G. Endothelial and leukocyte activation in experimental polytrauma and sepsis. Behring Inst Mitt 92 (1993) 218
3. Katiyar A.K., Vegad J.L., and Awadhiya R.P. Increased vascular permeability and leucocyte emigration in Escherichia coli endotoxin injury in the chicken skin. Res Vet Sci 52 (1992) 154
4. Malmros C., Holst E., Hansson L., Martensson L., and Thorne J. Dynamic accumulation of neutrophils in lungs and visceral organs during early abdominal sepsis in the pig. World J Surg 18 (1994) 811
5. Basadre J.O., Singh H., Herndon D.N., et al. Effect of antibody-mediated neutropenia on the cardiopulmonary response to endotoxemia. J Surg Res 45 (1988) 266
6. Walther A., Weihrauch M., Schmidt W., Gebhard M.M., Martin E., and Schmidt H. Leukocyte-independent plasma extravasation during endotoxemia. Crit Care Med 28 (2000) 2943
7. Winn R., Maunder R., Chi E., and Harlan J. Neutrophil depletion does not prevent lung edema after endotoxin infusion in goats. J Appl Physiol 62 (1987) 116
8. De Clerck F., Van Gorp L., Beetens J., and Reneman R.S. Platelet-mediated vascular permeability in the rat: a predominant role for 5-hydroxytryptamine. Thromb Res 38 (1985) 321
9. Vincent J.L., Yagushi A., and Pradier O. Platelet function in sepsis. Crit Care Med 30 (2002) S313
10. Walther A., Czabanka M., Gebhard M.M., and Martin E. Glycoprotein IIB/IIIA-inhibition and microcirculatory alterations during experimental endotoxemia-an intravital microscopic study in the rat. Microcirculation 11 (2004) 79
11. Leithauser B., Schumacher J., Lendemans S., Tillmanns H., and Matthias F.R. Antithrombin attenuates microvascular leakage and leukocyte-endothelial interaction in response to endotoxin. Semin Thromb Hemost 28 Suppl)1 (2002) 87
12. Neviere R., Tournoys A., Mordon S., et al. Antithrombin reduces mesenteric venular leukocyte interactions and small intestine injury in endotoxemic rats. Shock 15 (2001) 220
13. Uchiba M., and Okajima K. Antithrombin III (AT III) prevents LPS-induced pulmonary vascular injury: novel biological activity of AT III. Semin Thromb Hemost 23 (1997) 583
14. Kozek-Langenecker S.A., Spiss C.K., Michalek-Sauberer A., Felfernig M., and Zimpfer M. Effect of prostacyclin on platelets, polymorphonuclear cells, and heterotypic cell aggregation during hemofiltration. Crit Care Med 31 (2003) 864
15. Mizutani A., Okajima K., Uchiba M., et al. Antithrombin reduces ischemia/reperfusion-induced renal injury in rats by inhibiting leukocyte activation through promotion of prostacyclin production. Blood 101 (2003) 3029
16. Noll T., Wozniak G., McCarson K., et al. Effect of factor XIII on endothelial barrier function. J Exp Med 189 (1999) 1373
17. Dardik R., Shenkman B., Tamarin I., et al. Factor XIII mediates adhesion of platelets to endothelial cells through alpha(v)beta(3) and glycoprotein IIb/IIIa integrins. Thromb Res 105 (2002) 317
18. Bauer P.R. Microvascular responses to sepsis: clinical significance. Pathophysiology 8 (2002) 141
19. Nimah M., and Brilli R.J. Coagulation dysfunction in sepsis and multiple organ system failure. Crit Care Clin 19 (2003) 441
20. Aird W.C. Vascular bed-specific hemostasis: role of endothelium in sepsis pathogenesis. Crit Care Med 29 (2001) S28
21. Zahler S., Heindl B., and Becker B.F. Selectin-mediated rolling of neutrophils is essential for their activation and retention in the reperfused coronary system. Basic Res Cardiol 97 (2002) 359
22. Klintman D., Li X., and Thorlacius H. Important role of P-selectin for leukocyte recruitment, hepatocellular injury, and apoptosis in endotoxemic mice. Clin Diagn Lab Immunol 11 (2004) 56
23. Klintman D., Schramm R., Menger M.D., and Thorlacius H. Leukocyte recruitment in hepatic injury: selectin-mediated leukocyte rolling is a prerequisite for CD18-dependent firm adhesion. J Hepatol 36 (2002) 53
24. Walzog B., and Gaehtgens P. Adhesion molecules: the path to a new understanding of acute inflammation. News Physiol Sci 15 (2000) 107
25. Yuan Y., Granger H.J., Zawieja D.C., and Chilian W.M. Flow modulates coronary venular permeability by a nitric oxide-related mechanism. Am J Physiol 263 (1992) H641
26. Zilberberg J., and Harris N.R. Role of shear and leukocyte adherence on venular permeability in the rat mesentery. Microvasc Res 62 (2001) 215
27. Ostrovsky L., Woodman R.C., Payne D., Teoh D., and Kubes P. Antithrombin III prevents and rapidly reverses leukocyte recruitment in ischemia/reperfusion. Circulation 96 (1997) 2302
28. Nishijima K., Kiryu J., Tsujikawa A., et al. Inhibitory effects of antithrombin III on interactions between blood cells and endothelial cells during retinal ischemia-reperfusion injury. Invest Ophthalmol Vis Sci 44 (2003) 332
29. Yamashiro K., Kiryu J., Tsujikawa A., et al. Inhibitory effects of antithrombin III against leukocyte rolling and infiltration during endotoxin-induced uveitis in rats. Invest Ophthalmol Vis Sci 42 (2001) 1553
30. Dunzendorfer S., Kaneider N., Rabensteiner A., et al. Cell-surface heparan sulfate proteoglycan-mediated regulation of human neutrophil migration by the serpin antithrombin III. Blood 97 (2001) 1079
31. Hoffmann J.N., Vollmar B., Inthorn D., Schildberg F.W., and Menger M.D. Antithrombin reduces leukocyte adhesion during chronic endotoxemia by modulation of the cyclooxygenase pathway. Am J Physiol Cell Physiol 279 (2000) C98
32. D'Acquisto F., Sautebin L., Iuvone T., Di Rosa M., and Carnuccio R. Prostaglandins prevent inducible nitric oxide synthase protein expression by inhibiting nuclear factor-kappaB activation in J774 macrophages. FEBS Lett 440 (1998) 76
33. Oh-ishi S., Utsunomiya I., Yamamoto T., Komuro Y., and Hara Y. Effects of prostaglandins and cyclic AMP on cytokine production in rat leukocytes. Eur J Pharmacol 300 (1996) 255
34. Uchiba M., Okajima K., and Murakami K. Effects of various doses of antithrombin III on endotoxin-induced endothelial cell injury and coagulation abnormalities in rats. Thromb Res 89 (1998) 233
35. Uchiba M., Okajima K., Murakami K., Okabe H., and Takatsuki K. Attenuation of endotoxin-induced pulmonary vascular injury by antithrombin III. Am J Physiol 270 (1996) L921
36. Pu Q., Wiel E., Corseaux D., et al. Beneficial effect of glycoprotein IIb/IIIa inhibitor (AZ-1) on endothelium in Escherichia coli endotoxin-induced shock. Crit Care Med 29 (2001) 1181
37. Walther A., Yilmaz N., Schmidt W., Bach A., Gebhard M.M., Martin E., and Schmidt H. Role of platelet-activating factor in leukocyte-independent plasma extravasation and mast cell activation during endotoxemia. J Surg Res 93 (2000) 265
38. De Clerck F. Effects of serotonin on platelets and blood vessels. J Cardiovasc Pharmacol 17 Suppl)5 (1991) S1
39. Walther A., Peter C., Secchi A., Gebhard M.M., Martin E., and Schmidt H. Selective serotonin receptor antagonism and leukocyte-independent plasma extravasation during endotoxemia. Microvasc Res 63 (2002) 135
40. Hein L., Ishii K., Coughlin S.R., and Kobilka B.K. Intracellular targeting and trafficking of thrombin receptors. A novel mechanism for resensitization of a G protein-coupled receptor. J Biol Chem 269 (1994) 27719
41. Ishii K., Chen J., Ishii M., et al. Inhibition of thrombin receptor signaling by a G-protein coupled receptor kinase. Functional specificity among G-protein coupled receptor kinases. J Biol Chem 269 (1994) 1125
42. Roemisch J., Gray E., Hoffmann J.N., and Wiedermann C.J. Antithrombin: a new look at the actions of a serine protease inhibitor. Blood Coagul Fibrinolysis 13 (2002) 657
43. Harada N., Okajima K., Kushimoto S., Isobe H., and Tanaka K. Antithrombin reduces ischemia/reperfusion injury of rat liver by increasing the hepatic level of prostacyclin. Blood 93 (1999) 157
44. Fletcher J.R., and Ramwell P.W. The effects of prostacyclin (PGI2) on endotoxin shock and endotoxin-induced platelet aggregation in dogs. Circ Shock 7 (1980) 299
45. Matthias F.R., and Ditter H. The effects of an infusion of prostacyclin on their endotoxin shock in rabbits. Folia Haematol Int Mag Klin Morphol Blutforsch 117 (1990) 209
46. Adany R., Kiss A., and Muszbek L. Factor XIII: a marker of mono- and megakaryocytopoiesis. Br J Haematol 67 (1987) 167
47. Ariens R.A., Kohler H.P., Mansfield M.W., and Grant P.J. Subunit antigen and activity levels of blood coagulation factor XIII in healthy individuals. Relation to sex, age, smoking, and hypertension. Arterioscler Thromb Vasc Biol 19 (1999) 2012
48. Muszbek L., Adany R., and Mikkola H. Novel aspects of blood coagulation factor XIII. I. Structure, distribution, activation, and function. Crit Rev Clin Lab Sci 33 (1996) 357
49. Karpati L., Penke B., Katona E., Balogh I., Vamosi G., and Muszbek L. A modified, optimized kinetic photometric assay for the determination of blood coagulation factor XIII activity in plasma. Clin Chem 46 (2000) 1946
50. Adany R., and Bardos H. Factor XIII subunit A as an intracellular transglutaminase. Cell Mol Life Sci 60 (2003) 1049
51. Dardik R., Solomon A., Loscalzo J., et al. Novel proangiogenic effect of factor XIII associated with suppression of thrombospondin 1 expression. Arterioscler Thromb Vasc Biol 23 (2003) 1472
52. Hevessy Z., Haramura G., Boda Z., Udvardy M., and Muszbek L. Promotion of the crosslinking of fibrin and alpha 2-antiplasmin by platelets. Thromb Haemost 75 (1996) 161
53. Kamitsuji H., Tani K., Yasui M., et al. Activity of blood coagulation factor XIII as a prognostic indicator in patients with Henoch-Schonlein purpura. Efficacy of factor XIII substitution. Eur J Pediatr 146 (1987) 519
54. Lorenz R., Born P., Olbert P., and Classen M. Factor XIII substitution in ulcerative colitis. Lancet 345 (1995) 449
55. Lorenz R., Olbert P., and Born P. Factor XIII in chronic inflammatory bowel diseases. Semin Thromb Hemost 22 (1996) 451
56. Hirahara K., Shinbo K., Takahashi M., and Matsuishi T. Suppressive effect of human blood coagulation factor XIII on the vascular permeability induced by anti-guinea pig endothelial cell antiserum in guinea pigs. Thromb Res 71 (1993) 139
57. Noll T., and Wozniak G. [Factor XIII and endothelial barrier function]. Haemostaseologie 22 (2002) 28
58. Clough G. Relationship between microvascular permeability and ultrastructure. Prog Biophys Mol Biol 55 (1991) 47
59. Grega G.J., and Adamski S.W. The role of venular endothelial cells in the regulation of macromolecular permeability. Microcirc Endothelium Lymphatics 4 (1988) 143
60. Schnittler H.J., Wilke A., Gress T., Suttorp N., and Drenckhahn D. Role of actin and myosin in the control of paracellular permeability in pig, rat and human vascular endothelium. J Physiol 431 (1990) 379
61. Lopaciuk S., Lovette K.M., McDonagh J., Chuang H.Y., and McDonagh R.P. Subcellular distribution of fibrinogen and factor XIII in human blood platelets. Thromb Res 8 (1976) 453
62. Sixma J.J., van den Berg A., Schiphorst M., Geuze H.J., and McDonagh J. Immunocytochemical localization of albumin and factor XIII in thin cryo sections of human blood platelets. Thromb Haemost 51 (1984) 388
63. Serrano K., and Devine D.V. Intracellular factor XIII crosslinks platelet cytoskeletal elements upon platelet activation. Thromb Haemost 88 (2002) 315