Skip to main content
Top
Published in: Critical Care 1/2006

Open Access 01-02-2006 | Research

Effects of coagulation factor XIII on intestinal functional capillary density, leukocyte adherence and mesenteric plasma extravasation in experimental endotoxemia

Authors: Jürgen Birnbaum, Ortrud Vargas Hein, Carsten Lührs, Oskar Rückbeil, Claudia Spies, Sabine Ziemer, Matthias Gründling, Taras Usichenko, Konrad Meissner, Dragan Pavlovic, Wolfgang J Kox, Christian Lehmann

Published in: Critical Care | Issue 1/2006

Login to get access

Abstract

Introduction

The objective of this study was to determine the effects of the administration of the coagulation factor XIII (F XIII) on intestinal functional capillary density, leukocyte adherence and mesenteric plasma extravasation during experimental endotoxemia.

Methods

In a prospective, randomized, controlled animal study 42 male Wistar rats were divided into three groups. Group 1 served as the control group. Groups 2 (lipopolysaccharide (LPS) group) and 3 (F XIII group) received endotoxin infusions (2.5 mg/kg/h for 2 hours). In group 3, 50 U/kg body weight F XIII was continuously administered during the first 30 minutes of endotoxemia. F XIII levels were measured in all animals. One half of the animals of each group were studied for intestinal functional capillary density (FCD) and leukocyte adherence on venular endothelium by intravital fluorescence microscopy (IVM). In the other half of each group, mesenteric plasma extravasation (FITC-albumin) was determined by IVM.

Results

The F XIII level was significantly increased in the F XIII treatment group. In the LPS group, endotoxemia led to a significant reduction of mucosal FCD (-18.5%; p < 0.01 versus control group). F XIII administration in the F XIII group attenuated the decrease in mucosal FCD (-3.7% compared to control; p < 0.05 versus LPS group). During endotoxemia, a significant increase of leukocyte adherence at the endothelium could be noted in the LPS group compared to the control group. Leukocyte adherence at the endothelium and plasma extravasation in the F XIII group did not differ significantly from the LPS group.

Conclusion

Factor XIII protected mucosal capillary perfusion against endotoxin-induced impairment in an experimental sepsis model in rats, whereas leukocyte adherence and plasma extravasation remained unchanged.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mythen MG, Webb AR: The role of gut mucosal hypoperfusion in the pathogenesis of post-operative organ dysfunction. Intensive Care Med 1994, 20: 203-209. 10.1007/BF01704701CrossRefPubMed Mythen MG, Webb AR: The role of gut mucosal hypoperfusion in the pathogenesis of post-operative organ dysfunction. Intensive Care Med 1994, 20: 203-209. 10.1007/BF01704701CrossRefPubMed
2.
go back to reference Taylor DE: Revving the motor of multiple organ dysfunction syndrome. Gut dysfunction in ARDS and multiorgan failure. Respir Care Clin N Am 1998, 4: 611-631.PubMed Taylor DE: Revving the motor of multiple organ dysfunction syndrome. Gut dysfunction in ARDS and multiorgan failure. Respir Care Clin N Am 1998, 4: 611-631.PubMed
3.
go back to reference Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 2003, 29: 530-538.CrossRefPubMed Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G: 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 2003, 29: 530-538.CrossRefPubMed
4.
go back to reference Muszbek L, Yee VC, Hevessy Z: Blood coagulation factor XIII: structure and function. Thromb Res 1999, 94: 271-305. 10.1016/S0049-3848(99)00023-7CrossRefPubMed Muszbek L, Yee VC, Hevessy Z: Blood coagulation factor XIII: structure and function. Thromb Res 1999, 94: 271-305. 10.1016/S0049-3848(99)00023-7CrossRefPubMed
5.
go back to reference Ueki S, Takagi J, Saito Y: Dual functions of transglutaminase in novel cell adhesion. J Cell Sci 1996, 109: 2727-2735.PubMed Ueki S, Takagi J, Saito Y: Dual functions of transglutaminase in novel cell adhesion. J Cell Sci 1996, 109: 2727-2735.PubMed
6.
go back to reference Noll T, Wozniak G, McCarson K, Hajimohammad A, Metzner HJ, Inserte J, Kummer W, Hehrlein FW, Piper HM: Effect of factor XIII on endothelial barrier function. J Exp Med 1999, 189: 1373-1382. 10.1084/jem.189.9.1373PubMedCentralCrossRefPubMed Noll T, Wozniak G, McCarson K, Hajimohammad A, Metzner HJ, Inserte J, Kummer W, Hehrlein FW, Piper HM: Effect of factor XIII on endothelial barrier function. J Exp Med 1999, 189: 1373-1382. 10.1084/jem.189.9.1373PubMedCentralCrossRefPubMed
7.
go back to reference Noll T, Wozniak G: Factor XIII and endothelial barrier function. Hamostaseologie 2002, 22: 28-31.PubMed Noll T, Wozniak G: Factor XIII and endothelial barrier function. Hamostaseologie 2002, 22: 28-31.PubMed
8.
go back to reference Wozniak G, Noll T, Akinturk H, Thul J, Muller M: Factor XIII prevents development of myocardial edema in children undergoing surgery for congenital heart disease. Ann NY Acad Sci 2001, 936: 617-620.CrossRefPubMed Wozniak G, Noll T, Akinturk H, Thul J, Muller M: Factor XIII prevents development of myocardial edema in children undergoing surgery for congenital heart disease. Ann NY Acad Sci 2001, 936: 617-620.CrossRefPubMed
9.
go back to reference Barry EL, Mosher DF: Factor XIII cross-linking of fibronectin at cellular matrix assembly sites. J Biol Chem 1988, 263: 10464-10469.PubMed Barry EL, Mosher DF: Factor XIII cross-linking of fibronectin at cellular matrix assembly sites. J Biol Chem 1988, 263: 10464-10469.PubMed
10.
go back to reference Mosher DF, Fogerty FJ, Chernousov MA, Barry EL: Assembly of fibronectin into extracellular matrix. Ann NY Acad Sci 1991, 614: 167-180.CrossRefPubMed Mosher DF, Fogerty FJ, Chernousov MA, Barry EL: Assembly of fibronectin into extracellular matrix. Ann NY Acad Sci 1991, 614: 167-180.CrossRefPubMed
11.
go back to reference Becker SW, Weidt F, Rohl K: The role of plasma transglutaminase (F XIII) in wound healing of complicated pressure sores after spinal cord injury. Spinal Cord 2001, 39: 114-117. 10.1038/sj.sc.3101092CrossRefPubMed Becker SW, Weidt F, Rohl K: The role of plasma transglutaminase (F XIII) in wound healing of complicated pressure sores after spinal cord injury. Spinal Cord 2001, 39: 114-117. 10.1038/sj.sc.3101092CrossRefPubMed
12.
go back to reference el-Hakim IE: The effect of fibrin stabilizing factor (F.XIII) on healing of bone defects in normal and uncontrolled diabetic rats. Int J Oral Maxillofac Surg 1999, 28: 304-308. 10.1034/j.1399-0020.1999.284280413.xCrossRefPubMed el-Hakim IE: The effect of fibrin stabilizing factor (F.XIII) on healing of bone defects in normal and uncontrolled diabetic rats. Int J Oral Maxillofac Surg 1999, 28: 304-308. 10.1034/j.1399-0020.1999.284280413.xCrossRefPubMed
13.
go back to reference Wozniak G, Noll T: Faktor XIII und Wundheilung. Factor XIII and wound healing. Hamostaseologie 2002, 22: 59-62.PubMed Wozniak G, Noll T: Faktor XIII und Wundheilung. Factor XIII and wound healing. Hamostaseologie 2002, 22: 59-62.PubMed
14.
go back to reference Adany R, Bardos H: Factor XIII subunit A as an intracellular transglutaminase. Cell Mol Life Sci 2003, 60: 1049-1060.PubMed Adany R, Bardos H: Factor XIII subunit A as an intracellular transglutaminase. Cell Mol Life Sci 2003, 60: 1049-1060.PubMed
15.
go back to reference Lorenz R, Born P, Olbert P, Classen M: Factor XIII substitution in ulcerative colitis. Lancet 1995, 345: 449-450. 10.1016/S0140-6736(95)90428-XCrossRefPubMed Lorenz R, Born P, Olbert P, Classen M: Factor XIII substitution in ulcerative colitis. Lancet 1995, 345: 449-450. 10.1016/S0140-6736(95)90428-XCrossRefPubMed
16.
go back to reference D'Argenio G, Grossman A, Cosenza V, Valle ND, Mazzacca G, Bishop PD: Recombinant factor XIII improves established experimental colitis in rats. Dig Dis Sci 2000, 45: 987-997. 10.1023/A:1005541512152CrossRefPubMed D'Argenio G, Grossman A, Cosenza V, Valle ND, Mazzacca G, Bishop PD: Recombinant factor XIII improves established experimental colitis in rats. Dig Dis Sci 2000, 45: 987-997. 10.1023/A:1005541512152CrossRefPubMed
17.
go back to reference D'Argenio G, Iovino P, Cosenza V, Della-Valle N, De-Ritis F, Mazzacca G: Factor XIII improves gastric stress lesions in rats. Digestion 1903, 63: 220-228.CrossRef D'Argenio G, Iovino P, Cosenza V, Della-Valle N, De-Ritis F, Mazzacca G: Factor XIII improves gastric stress lesions in rats. Digestion 1903, 63: 220-228.CrossRef
18.
go back to reference Witte J, Jochum M, Scherer R, Schramm W, Hochstrasser K, Fritz H: Disturbances of selected plasma proteins in hyperdynamic septic shock. Intensive Care Med 1982, 8: 215-222. 10.1007/BF01694524CrossRefPubMed Witte J, Jochum M, Scherer R, Schramm W, Hochstrasser K, Fritz H: Disturbances of selected plasma proteins in hyperdynamic septic shock. Intensive Care Med 1982, 8: 215-222. 10.1007/BF01694524CrossRefPubMed
19.
go back to reference Tanaka H, Sugimoto H, Yoshioka T, Sugimoto T: Role of granulocyte elastase in tissue injury in patients with septic shock complicated by multiple-organ failure. Ann Surg 1991, 213: 81-85.PubMedCentralCrossRefPubMed Tanaka H, Sugimoto H, Yoshioka T, Sugimoto T: Role of granulocyte elastase in tissue injury in patients with septic shock complicated by multiple-organ failure. Ann Surg 1991, 213: 81-85.PubMedCentralCrossRefPubMed
20.
go back to reference Collighan N, Giannoudis PV, Kourgeraki O, Perry SL, Guillou PJ, Bellamy MC: Interleukin 13 and inflammatory markers in human sepsis. Br J Surg 2004, 91: 762-768. 10.1002/bjs.4521CrossRefPubMed Collighan N, Giannoudis PV, Kourgeraki O, Perry SL, Guillou PJ, Bellamy MC: Interleukin 13 and inflammatory markers in human sepsis. Br J Surg 2004, 91: 762-768. 10.1002/bjs.4521CrossRefPubMed
21.
go back to reference van der Poll T, van Deventer SJ, Hack CE, Wolbink GJ, Aarden LA, Buller HR, ten Cate JW: Effects on leukocytes after injection of tumor necrosis factor into healthy humans. Blood 1992, 79: 693-698.PubMed van der Poll T, van Deventer SJ, Hack CE, Wolbink GJ, Aarden LA, Buller HR, ten Cate JW: Effects on leukocytes after injection of tumor necrosis factor into healthy humans. Blood 1992, 79: 693-698.PubMed
22.
go back to reference Suttorp N, Nolte A, Wilke A, Drenckhahn D: Human neutrophil elastase increases permeability of cultured pulmonary endothelial cell monolayers. Int J Microcirc Clin Exp 1993, 13: 187-203.PubMed Suttorp N, Nolte A, Wilke A, Drenckhahn D: Human neutrophil elastase increases permeability of cultured pulmonary endothelial cell monolayers. Int J Microcirc Clin Exp 1993, 13: 187-203.PubMed
23.
go back to reference Klingemann HG, Egbring R, Holst F, Gramse M, Havemann K: Degradation of human plasma fibrin stabilizing factor XIII subunits by human granulocytic proteinases. Thromb Res 1982, 28: 793-801. 10.1016/0049-3848(82)90105-0CrossRefPubMed Klingemann HG, Egbring R, Holst F, Gramse M, Havemann K: Degradation of human plasma fibrin stabilizing factor XIII subunits by human granulocytic proteinases. Thromb Res 1982, 28: 793-801. 10.1016/0049-3848(82)90105-0CrossRefPubMed
24.
go back to reference Bohlen HG, Gore RW: Preparation of rat intestinal muscle and mucosa for quantitative microcirculatory studies. Microvasc Res 1976, 11: 103-110. 10.1016/0026-2862(76)90081-9CrossRefPubMed Bohlen HG, Gore RW: Preparation of rat intestinal muscle and mucosa for quantitative microcirculatory studies. Microvasc Res 1976, 11: 103-110. 10.1016/0026-2862(76)90081-9CrossRefPubMed
25.
go back to reference Schmid-Schoenbein GW, Zweifach BW, Kovalcheck S: The application of stereological principles to morphometry of the microcirculation in different tissues. Microvasc Res 1977, 14: 303-317. 10.1016/0026-2862(77)90028-0CrossRefPubMed Schmid-Schoenbein GW, Zweifach BW, Kovalcheck S: The application of stereological principles to morphometry of the microcirculation in different tissues. Microvasc Res 1977, 14: 303-317. 10.1016/0026-2862(77)90028-0CrossRefPubMed
26.
go back to reference Gore RW, Bohlen HG: Microvascular pressures in rat intestinal muscle and mucosal villi. Am J Physiol 1977, 233: H685-693.PubMed Gore RW, Bohlen HG: Microvascular pressures in rat intestinal muscle and mucosal villi. Am J Physiol 1977, 233: H685-693.PubMed
27.
go back to reference Menger MD, Steiner D, Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: significance of "no reflow". Am J Physiol 1992, 263: H1892-H1900.PubMed Menger MD, Steiner D, Messmer K: Microvascular ischemia-reperfusion injury in striated muscle: significance of "no reflow". Am J Physiol 1992, 263: H1892-H1900.PubMed
28.
go back to reference Dardik R, Solomon A, Loscalzo J, Eskaraev R, Bialik A, Goldberg I, Schiby G, Inbal A: Novel proangiogenic effect of factor XIII associated with suppression of thrombospondin 1 expression. Arterioscler Thromb Vasc Biol 2003, 23: 1472-1477. 10.1161/01.ATV.0000081636.25235.C6CrossRefPubMed Dardik R, Solomon A, Loscalzo J, Eskaraev R, Bialik A, Goldberg I, Schiby G, Inbal A: Novel proangiogenic effect of factor XIII associated with suppression of thrombospondin 1 expression. Arterioscler Thromb Vasc Biol 2003, 23: 1472-1477. 10.1161/01.ATV.0000081636.25235.C6CrossRefPubMed
29.
go back to reference Lee SY, Chang SK, Lee IH, Kim YM, Chung SI: Depletion of plasma factor XIII prevents disseminated intravascular coagulation-induced organ damage. Thromb Haemost 2001, 85: 464-469.PubMed Lee SY, Chang SK, Lee IH, Kim YM, Chung SI: Depletion of plasma factor XIII prevents disseminated intravascular coagulation-induced organ damage. Thromb Haemost 2001, 85: 464-469.PubMed
30.
go back to reference Marzano AV, Federici AB, Gasparini G, Mannucci PM, Caputo R, Berti E: Coagulation factor XIII, endothelial damage and systemic sclerosis. Eur J Dermatol 2000, 10: 14-17. 10.1159/000047586PubMed Marzano AV, Federici AB, Gasparini G, Mannucci PM, Caputo R, Berti E: Coagulation factor XIII, endothelial damage and systemic sclerosis. Eur J Dermatol 2000, 10: 14-17. 10.1159/000047586PubMed
31.
go back to reference Wozniak G, Noll T, Brunner U, Hehrlein FW: Topical treatment of venous ulcer with fibrin stabilizing factor: experimental investigation of effects on vascular permeability. Vasa 1999, 28: 160-163. 10.1024/0301-1526.28.3.160CrossRefPubMed Wozniak G, Noll T, Brunner U, Hehrlein FW: Topical treatment of venous ulcer with fibrin stabilizing factor: experimental investigation of effects on vascular permeability. Vasa 1999, 28: 160-163. 10.1024/0301-1526.28.3.160CrossRefPubMed
32.
go back to reference Hirahara K, Shinbo K, Takahashi M, 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 1993, 71: 139-148. 10.1016/0049-3848(93)90180-VCrossRefPubMed Hirahara K, Shinbo K, Takahashi M, 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 1993, 71: 139-148. 10.1016/0049-3848(93)90180-VCrossRefPubMed
33.
go back to reference Akimov SS, Belkin AM: Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001, 98: 1567-1576. 10.1182/blood.V98.5.1567CrossRefPubMed Akimov SS, Belkin AM: Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 2001, 98: 1567-1576. 10.1182/blood.V98.5.1567CrossRefPubMed
34.
go back to reference Dallabrida SM, Falls LA, Farrell DH: Factor XIIIa supports microvascular endothelial cell adhesion and inhibits capillary tube formation in fibrin. Blood 2000, 95: 2586-2592.PubMed Dallabrida SM, Falls LA, Farrell DH: Factor XIIIa supports microvascular endothelial cell adhesion and inhibits capillary tube formation in fibrin. Blood 2000, 95: 2586-2592.PubMed
35.
go back to reference Takahashi H, Isobe T, Horibe S, Takagi J, Yokosaki Y, Sheppard D, Saito Y: Tissue transglutaminase, coagulation factor XIII, and the pro-polypeptide of von Willebrand factor are all ligands for the integrins alpha 9beta 1 and alpha 4beta 1. J Biol Chem 2000, 275: 23589-23595. 10.1074/jbc.M003526200CrossRefPubMed Takahashi H, Isobe T, Horibe S, Takagi J, Yokosaki Y, Sheppard D, Saito Y: Tissue transglutaminase, coagulation factor XIII, and the pro-polypeptide of von Willebrand factor are all ligands for the integrins alpha 9beta 1 and alpha 4beta 1. J Biol Chem 2000, 275: 23589-23595. 10.1074/jbc.M003526200CrossRefPubMed
Metadata
Title
Effects of coagulation factor XIII on intestinal functional capillary density, leukocyte adherence and mesenteric plasma extravasation in experimental endotoxemia
Authors
Jürgen Birnbaum
Ortrud Vargas Hein
Carsten Lührs
Oskar Rückbeil
Claudia Spies
Sabine Ziemer
Matthias Gründling
Taras Usichenko
Konrad Meissner
Dragan Pavlovic
Wolfgang J Kox
Christian Lehmann
Publication date
01-02-2006
Publisher
BioMed Central
Published in
Critical Care / Issue 1/2006
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/cc3994

Other articles of this Issue 1/2006

Critical Care 1/2006 Go to the issue