Microcirculatory endothelial dysfunction during endotoxemia - Insights into pathophysiology, pathologic mechanisms and clinical relevance

Current Vascular Pharmacology

Volumn 5, Issue 4, 2007, Pages 266-275

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

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Coagulation; Endothelial hyperpermeability; Endotoxemia; Platelets; Sepsis

Indexed keywords

ABCIXIMAB; ANTITHROMBIN III; BETA2 INTEGRIN; CIMETIDINE; CINANSERIN; DIPHENHYDRAMINE; DROTRECOGIN; FIBRINOGEN RECEPTOR; FUCOIDIN; GINKGOLIDE B; HEAT SHOCK PROTEIN 27; HISTAMINE; INTERLEUKIN 1; INTERLEUKIN 6; KETANSERIN; METHYSERGIDE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY CD 11B; MONOCLONAL ANTIBODY CD18; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; SELECTIN; SEROTONIN; SEROTONIN ANTAGONIST; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR ANTAGONIST; TIRILAZAD; TISSUE FACTOR PATHWAY INHIBITOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

BLOOD VESSEL PERMEABILITY; CELL ACTIVITY; CELL INTERACTION; CLINICAL TRIAL; DRUG MECHANISM; ENDOTHELIAL DYSFUNCTION; ENDOTOXEMIA; ENZYME INHIBITION; HISTAMINE RELEASE; HUMAN; INFLAMMATION; LEUKOCYTE ACTIVATION; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; MAST CELL; MICROCIRCULATION; NONHUMAN; PATHOPHYSIOLOGY; REVIEW; SEPSIS; THROMBOCYTE DYSFUNCTION; ANIMAL; CELL ADHESION; LEUKOCYTE; PATHOLOGY; PHYSIOLOGY; THROMBOCYTE; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD PLATELETS; CELL ADHESION; ENDOTHELIUM, VASCULAR; ENDOTOXEMIA; HUMANS; LEUKOCYTES; MAST CELLS; MICROCIRCULATION; NITRIC OXIDE;

EID: 38449107022     PISSN: 15701611     EISSN: None     Source Type: Journal    
DOI: 10.2174/157016107782023389     Document Type: Review

References (107)

1. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998; 91: 3527-61.
2. Wolinsky H. A proposal linking clearance of circulating lipoproteins to tissue metabolic activity as a basis for understanding atherogenesis. Circ Res 1980; 47: 301-11.
3. Bombeli T, Mueller M, Haeberli A. Anticoagulant properties of the vascular endothelium. Thromb Haemost 1997; 77: 408-23.
4. Vallet B, Wiel E. Endothelial cell dysfunction and coagulation. Crit Care Med 2001; 29: S36-41.
5. Bevilacqua MP,Gimbrone MA, Jr. Inducible endothelial functions in inflammation and coagulation. Semin Thromb Hemost 1987; 13: 425-33.
6. Faust SN, Heyderman RS, Levin M. Coagulation in severe sepsis: a central role for thrombomodulin and activated protein C. Crit Care Med 2001; 29: S62-7; discussion S67-8.
7. Jacobi J. Pathophysiology of sepsis. Am J Health Syst Pharm 2002; 59 Suppl 1: S3-8.
8. Bannerman DD, Sathyamoorthy M,Goldblum SE. Bacterial lipopolysaccharide disrupts endothelial monolayer integrity and survival signaling events through caspase cleavage of adherens junction proteins. J Biol Chem 1998; 273: 35371-80.
9. Bauer PR. Microvascular responses to sepsis: clinical significance. Pathophysiology 2002; 8: 141-148.
10. McCuskey RS, Urbaschek R, Urbaschek B. The microcirculation during endotoxemia. Cardiovasc Res 1996; 32: 752-63.
11. Grega GJ, Adamski SW. The role of venular endothelial cells in the regulation of macromolecular permeability. Microcirc Endothelium Lymphatics 1988; 4: 143-67.
12. Hirano S, Rees RS, Yancy SL, Welsh MJ, Remick DG, Yamada T, et al. Endothelial barrier dysfunction caused by LPS correlates with phosphorylation of HSP27 in vivo. Cell Biol Toxicol 2004; 20: 1-14.
13. Gartner SL, Sieckmann DG, Kang YH, Watson LP, Homer LD. Effects of lipopolysaccharide, lipid A, lipid X, and phorbol ester on cultured bovine endothelial cells. Lab Invest 1988; 59: 181-91.
14. Uchiba M, Okajima K, Murakami K. Effects of various doses of antithrombin III on endotoxin-induced endothelial cell injury and coagulation abnormalities in rats. Thromb Res 1998; 89: 233-41.
15. Barroso-Aranda J, Zweifach BW, Mathison JC,Schmid-Schonbein GW. Neutrophil activation, tumor necrosis factor, and survival after endotoxic and hemorrhagic shock. J Cardiovasc Pharmacol 1995; 25 Suppl 2: S23-9.
16. Kubes P, Kanwar S. Histamine induces leukocyte rolling in post-capillary venules. A P- selectin-mediated event. J Immunol 1994; 152: 3570-7.
17. Kubes P, Ward PA. Leukocyte recruitment and the acute inflammatory response. Brain Pathol 2000; 10: 127-35.
18. Astiz ME, Rackow EC. Septic shock. Lancet 1998; 351: 1501-5.
19. Bannerman DD, Goldblum SE. Direct effects of endotoxin on the endothelium: barrier function and injury. Lab Invest 1999; 79: 1181-99.
20. Schmidt H, Schmidt W, Muller T, Böhrer H, Bach A, Gebhard MM, et al. Effect of the 21-aminosteroid tirilazad mesylate on leukocyte adhesion and macromolecular leakage during endotoxemia. Surgery 1997; 121: 328-34.
21. Percival E, Percival R. Part I. The isolation and purification of fucoidin from brown seaweeds. J Chem Soc 1950; 145: 717-720.
22. Patankar MS, Oehninger S, Barnett T, Williams RL,Clark GF. A revised structure for fucoidan may explain some of its biological activities. J Biol Chem 1993; 268: 21770-6.
23. Kubes P, Jutila M, Payne D. Therapeutic potential of inhibiting leukocyte rolling in ischemia/reperfusion. J Clin Invest 1995; 95: 2510-9.
24. Arfors KE, Lundberg C, Lindbom L, Lundberg K, Beatty PG, Harlan JM. A monoclonal antibody to the membrane glycoprotein complex CD18 inhibits polymorphonuclear leukocyte accumulation and plasma leakage in vivo. Blood 1987; 69: 338-40.
25. Lindbom L, Xie X, Raud J, Hedqvist P. Chemoattractant-induced firm adhesion of leukocytes to vascular endothelium in vivo is critically dependent on initial leukocyte rolling. Acta Physiol Scand 1992; 146: 415-21.
26. Walther A, Weihrauch M, Schmidt W, Gebhard MM, Martin E, Schmidt H. Leukocyte-independent plasma extravasation during endotoxemia. Crit Care Med 2000; 28: 2943-8.
27. Walther A, Czabanka M, Gebhard MM, Martin E. Glykoprotein IIb/ IIIa-inhibition and microcirculatory alterations during experimental endotoxemia. - An intravital microscopic study in the rat. Microcirculation 2004; 11: 79-88.
28. Kurose I, Pothoulakis C, LaMont JT, Anderson DC, Paulson JC, Miyasaka M, et al. Clostridium difficile toxin A-induced microvascular dysfunction. Role of histamine. J Clin Invest 1994; 94: 1919-26.
29. Kurose I, Wolf R, Grisham MB, Granger DN. Modulation of ischemia/ reperfusion-induced microvascular dysfunction by nitric oxide. Circ Res 1994; 74: 376-82.
30. Bonnardel-Phu E, Vicaut E. Role of oxidative stress in permeability changes observed in the microcirculation of diabetic rats in vivo. J Mal Vasc 2000; 25: 115-21.
31. Windsor AC, Mullen PG, Fowler AA, Sugerman HJ. Role of the neutrophil in adult respiratory distress syndrome. Br J Surg 1993; 80: 10-7.
32. Basadre JO, Singh H, Herndon DN, Stothert J, Traber LD, Horn K, et al. Effect of antibody-mediated neutropenia on the cardiopulmonary response to endotoxemia. J Surg Res 1988; 45: 266-75.
33. Kubes P, Kanwar S, Niu XF, Gaboury JP. Nitric oxide synthesis inhibition induces leukocyte adhesion via superoxide and mast cells. FASEB J 1993; 7: 1293-9.
34. Estevez AG, Jordan J. Nitric oxide and superoxide, a deadly cocktail. Ann N Y Acad Sci 2002; 962: 207-11.
35. Walther A, Barth C, Gebhard MM, Martin E. Role of nitric oxide in leukocyte-independent endothelial damage during experimental endotoxemia. Shock 2003; 20: 286-91.
36. Sacks T, Moldow CF, Craddock PR, Bowers TK, Jacob HS. Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes. An in vitro model of immune vascular damage. J Clin Invest 1978; 61; 1161-7.
37. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci USA 1991; 88: 4651-5.
38. Kurose I, Kubes P, Wolf R, Anderson DC, Paulson J, Miyasaka M, et al. Inhibition of nitric oxide production. Mechanisms of vascular albumin leakage. Circ Res 1993; 73: 164-71.
39. Kurose I, Wolf R, Grisham MB, Aw TY, Specian RD, Granger DN. Microvascular responses to inhibition of nitric oxide production. Role of active oxidants. Circ Res 1995; 76: 30-9.
40. Kubes P, Granger DN. Nitric oxide modulates microvascular permeability. Am J Physiol 1992; 262: H611-5.
41. Kubes P. Nitric oxide modulates epithelial permeability in the feline small intestine. Am J Physiol 1992; 262: G1138-42.
42. Alican I, Kubes P. A critical role for nitric oxide in intestinal barrier function and dysfunction. Am J Physiol 1996; 270: G225-37.
43. Cerwinka WH, Cooper D, Krieglstein CF, Ross CR, McCord JM, Granger DN. Superoxide mediates endotoxin-induced platelet-endothelial cell adhesion in intestinal venules. Am J Physiol Heart Circ Physiol 2003; 284: H535-41.
44. Kurose I, Wolf R, Grisham MB, Granger DN. Effects of an endogenous inhibitor of nitric oxide synthesis on postcapillary venules. Am J Physiol 1995; 268: H2224-31.
45. Kanwar S, Wallace JL, Befus D, Kubes P. Nitric oxide synthesis inhibition increases epithelial permeability via mast cells. Am J Physiol 1994; 266: G222-9.
46. Nguyen BL, Saitoh M, Ware JA. Interaction of nitric oxide and cGMP with signal transduction in activated platelets. Am J Physiol 1991; 261: H1043-52.
47. Packham MA, Nishizawa EE, Mustard JF. Response of platelets to tissue injury. Biochem Pharmacol 1968: Suppl:171-84.
48. Muller-Werdan U, Werdan K. Der anaphylaktische Schock. Anaesthesist 1997; 46: 549-63.
49. Wershil BK, Wang ZS, Gordon JR, Galli SJ. Recruitment of neutrophils during IgE-dependent cutaneous late phase reactions in the mouse is mast cell-dependent. Partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. J Clin Invest 1991; 87: 446-53.
50. Kubes P, Granger DN. Leukocyte-endothelial cell interactions evoked by mast cells. Cardiovasc Res 1996; 32: 699-708.
51. Bridges AJ, Malone DG, Jicinsky J, Chen M, Ory P, Engber W, et al. Human synovial mast cell involvement in rheumatoid arthritis and osteoarthritis. Relationship to disease type, clinical activity, and antirheumatic therapy. Arthritis Rheum 1991; 34: 1116-24.
52. Atkinson JB, Harlan CW, Harlan GC,Virmani R. The association of mast cells and atherosclerosis: a morphologic study of early atherosclerotic lesions in young people. Hum Pathol 1994; 25: 154-9.
53. Leal-Berumen I, Conlon P, Marshall JS. IL-6 production by rat peritoneal mast cells is not necessarily preceded by histamine release and can be induced by bacterial lipopolysaccharide. J Immunol 1994; 152: 5468-76.
54. Walther A, Schmidt H, Schmidt W, Martin E. Microvascular permeability alterations and mast cell activation during endotoxemia. Crit Care Med. 1998; 26: A 133.
55. Walther A, Yilmaz N, Schmidt W, Bach A, Gebhard MM, Martin E, et al. Role of platelet-activating factor in leukocyte-independent plasma extravasation and mast cell activation during endotoxemia. J Surg Res 2000; 93: 265-71.
56. Paul W, Douglas GJ, Lawrence L, Khawaja AM, Perez AC, Schachter M, et al. Cutaneous permeability responses to bradykinin and histamine in the guinea-pig: possible differences in their mechanism of action. Br J Pharmacol 1994; 111: 159-64.
57. Majno G, Shea SM, Leventhal M. Endothelial contraction induced by histamine-type mediators: an electron microscopic study. J Cell Biol 1969; 42: 647-72.
58. Gimeno G, Carpentier PH, Desquand-Billiald S, Hanf R, Finet M. Histamine-induced biphasic macromolecular leakage in the microcirculation of the conscious hamster: evidence for a delayed nitric oxide-dependent leakage. Br J Pharmacol 1998; 123: 943-51.
59. Clough G, Michel CC, Phillips ME. Inflammatory changes in permeability and ultrastructure of single vessels in the frog mesenteric microcirculation. J Physiol 1988; 395: 99-114.
60. Fox J, Galey F, Wayland H. Action of histamine on the mesenteric microvasculature. Microvasc Res 1980; 19: 108-26.
61. Walther A, Jäger M, Secchi A, Schmidt W, Bach A, Martin E, et al. Effects of histamine-1 receptor antagonism on leukocyte-independent plasma extravasation during endotoxemia. J Crit Care 2001; 16: 24-31.
62. Walther A, Jäger M, Secchi A, Schmidt W, Martin E, Schmidt H. Role of combined histamine-1- and histamine-2-receptor antagonism in leukocyte-independent plasma extravasation during endotoxemia. Intern J Surg Invest 2001; 3: 393-399.
63. Salari H, Demos M, Wong A. Comparative hemodynamics and cardiovascular effects of endotoxin and platelet-activating factor in rat. Circ Shock 1990; 32: 189-207.
64. Ayala A, Chaudry IH. Platelet activating actor and its role in trauma, shock and sepsis. New Horiz 1996; 4: 265-75.
65. Schmidt H, Ebeling D, Bauer H, Böhrer H, Gebhard MM, Martin E. Influence of the platelet-activating factor receptor antagonist BN52021 on endotoxin-induced leukocyte adherence in rat mesenteric venules. J Surg Res 1996; 60: 29-35.
66. Walther A, Yilmaz N, Schmidt W, Bach A, Gebhard MM, Martin E, et al. Methysergide attenuates leukocyte-independent plasma extravasation during endotoxemia. J Crit Care 2001; 16: 121-6.
67. Walther A, Peter C, Secchi A, Gebhard MM, Martin E, Schmidt H. Selective Serotonin Receptor Antagonism and Leukocyte-Independent Plasma Extravasation during Endotoxemia. Microvasc Res 2002; 63: 135-8.
68. Theoharides TC, Kops SK, Bandy PK, Askenase PW. Differential release of serotonin without comparable histamine under diverse conditions in the rat mast cell. Biochem Pharmacol 1985; 34: 1389-98.
69. Galli SJ. New concepts about the mast cell. N Engl J Med 1993; 328: 257-65.
70. Walther A, Jäger M, Schmidt W, Secchi A, Gebhard MM, Martin E, et al. Influence of mast cells on cells on leukocyte-independent plasma extravasation during endotoxemia. Microvasc Res 2001; 62: 79-82.
71. Tannenbaum S, Oertel H, Henderson W, Kaliner M. The biologic activity of mast cell granules. I. Elicitation of inflammatory responses in rat skin. J Immunol 1980; 125: 325-35.
72. Klein LM, Lavker RM, Matis WL, Murphy GF. Degranulation of human mast cells induces an endothelial antigen central to leukocyte adhesion. Proc Natl Acad Sci USA 1989; 86: 8972-6.
73. Iuvone T, Den Bossche RV, D'Acquisto F, Carnuccio R, Herman AG. Evidence that mast cell degranulation, histamine and tumour necrosis factor alpha release occur in LPS-induced plasma leakage in rat skin. Br J Pharmacol 1999; 128: 700-4.
74. Katz HR, Stevens RL, Austen KF. Heterogeneity of mammalian mast cells differentiated in vivo and in vitro. J Allergy Clin Immunol 1985; 76: 250-9.
75. Kitamura Y. Heterogeneity of mast cells and phenotypic change between subpopulations. Annu Rev Immunol 1989; 7: 59-76.
76. Costa JJ, Harris AG, Delano FA, Zweifach BW, Schmid-Schonbein GW. Mast cell degranulation and parenchymal cell injury in the rat mesentery. Microcirculation 1999; 6: 237-44.
77. Gaboury JP, Niu XF, Kubes P. Nitric oxide inhibits numerous features of mast cell-induced inflammation. Circulation 1996; 93: 318-26.
78. Cerwinka WH, Cooper D, Krieglstein CF, Feelisch M, Granger DN. Nitric oxide modulates endotoxin-induced platelet-endothelial cell adhesion in intestinal venules. Am J Physiol Heart Circ Physiol 2002; 282: H1111-7.
79. Massberg S, Sausbier M, Klatt P, Bauer M, Pfeifer A, Siess W, et al. Increased adhesion and aggregation of platelets lacking cyclic guanosine 3′,5′-monophosphate kinase I. J Exp Med 1999; 189: 1255-64.
80. Topol EJ, Byzova TV,Plow EF. Platelet GPIIb-IIIa blockers. Lancet 1999; 353: 227-31.
81. Tam SH, Sassoli PM, Jordan RE, Nakada MT. Abciximab (ReoPro, chimeric 7E3 Fab) demonstrates equivalent affinity and functional blockade of glycoprotein IIb/IIIa and alpha(v)beta3 integrins. Circulation 1998; 98: 1085-91.
82. Pu Q, Wiel E, Corseaux D, Bordet R, Azrin MA, Ezekowitz MD, et al. Beneficial effect of glycoprotein IIb/IIIa inhibitor (AZ-1) on endothelium in Escherichia coli endotoxin-induced shock. Crit Care Med 2001; 29: 1181-8.
83. Xiao Z, Theroux P, Frojmovic M. Modulation of platelet-neutrophil interaction with pharmacological inhibition of fibrinogen binding to platelet GPIIb/IIIa receptor. Thromb Haemost 1999; 81: 281-5.
84. Bombeli T, Schwartz BR, Harlan JM. Adhesion of activated platelets to endothelial cells: evidence for a GPIIbIIIa-dependent bridging mechanism and novel roles for endothelial intercellular adhesion molecule 1 (ICAM-1), alphavbeta3 integrin, and GPIbalpha. J Exp Med 1998; 187: 329-39.
85. Li N, Soap A, Sollevi A, Hjemdahl P. Multi-cellular activation in vivo by endotoxin in humans - limited protection by adenosine infusion. Thromb Haemost 2000; 84: 381-7.
86. Frenette PS, Moyna C, Hartwell DW, Lowe JB, Hynes RO, Wagner DD. Platelet-endothelial interactions in inflamed mesenteric venules. Blood 1998; 91: 1318-24.
87. Massberg S, Enders G, Leiderer R, Eisenmenger S, Vestweber D, Krombach F, et al. Platelet-endothelial cell interactions during ischemia/ reperfusion: the role of P-selectin. Blood 1998; 92: 507-15.
88. Csako G, Suba EA, Elin R J. Endotoxin-induced platelet activation in human whole blood in vitro. Thromb Haemost 1988; 59: 378-82.
89. De Clerck F, Van Gorp L, Beetens J, Reneman RS. Platelet-mediated vascular permeability in the rat: a predominant role for 5-hydroxytryptamine. Thromb Res 1985; 38: 321-39.
90. Walther A, Peter C, Yilmaz N, Schmidt W, Martin E, Schmidt H. Influence of seratonin-receptor antagonism on mast cell activation during endotoxemia. Pathophysiology 2002; 8: 161-165.
91. De Clerck FF,Janssen PA. Amplification mechanisms in platelet activation and arterial thrombosis. J Hypertens Suppl 1990; 8: S87-93.
92. De Clerck F, Janssen PA. 5-Hydroxytryptamine and thromboxane A2 in ischaemic heart disease. Blood Coagul Fibrinolysis 1990; 1: 201-9.
93. De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL. Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002; 166: 98-104.
94. Sakr Y, Dubois MJ, De Backer D, Creteur J, Vincent JL. Persistent microcirculatory alterations are associated with organ failure and death in patients with septic shock. Crit Care Med 2004; 32: 1825-31.
95. Franchini M, Lippi G, Manzato F. Recent acquisitions in the pathophysiology, diagnosis and treatment of disseminated intravascular coagulation. Thromb J 2006; 4: 4.
96. Riewald M, Ruf W. Science review: role of coagulation protease cascades in sepsis. Crit Care 2003; 7: 123-9.
97. Oelschlager C, Romisch J, Staubitz A, Stauss H, Leithauser B, Tillmanns H, et al. Antithrombin III inhibits nuclear factor kappaB activation in human monocytes and vascular endothelial cells. Blood 2002; 99: 4015-20.
98. Warren BL, Eid A, Singer P, Pillay SS, Carl P< Novak I, et al. Caring for the critically ill patient. High-dose antithrombin III in severe sepsis: a randomized controlled trial. JAMA 2001; 286: 1869-78.
99. Fourrier F, Chopin C, Huart JJ, Runge I, Caron C, Goudemand J. Double-blind, placebo-controlled trial of antithrombin III concentrates in septic shock with disseminated intravascular coagulation. Chest 1993; 104: 882-8.
100. Minneci PC, Deans KJ, Cui X, Banks SM, Natanson C, Eichacker PQ. Antithrombotic therapies for sepsis: a need for more studies. Crit Care Med 2006; 34: 538-41.
101. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001; 344: 699-709.
102. Esmon CT. Role of coagulation inhibitors in inflammation. Thromb Haemost 2001; 86: 51-6.
103. Abraham E, Reinhart K, Svoboda P, Seihert A, Olthoff D, Dal Nogare A, et al. Assessment of the safety of recombinant tissue factor pathway inhibitor in patients with severe sepsis: a multicenter, randomized, placebo-controlled, single-blind, dose escalation study. Crit Care Med 2001; 29: 2081-9.
104. Abraham E, Reinhart K, Opal S, Demeyer I, Doig C, Rodriguez AL, et al. Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA 2003; 290: 238-47.
105. Kirschenbaum LA, Adler D, Astiz ME, Barua RS, Saha D, Rackow EC. Mechanisms of platelet-neutrophil interactions and effects on cell filtration in septic shock. Shock 2002; 17: 508-12.
106. Impaired platelet function correlates with multi-organ dysfunction. A study of patients with sepsis. Platelets 1998; 9: 223-5.
107. Walther A, Petri E, Peter C, Czabanka M, Martin E. Selective Serotonin. Receptor Antagonism and Microcirculatory Alterations during Experimental. Endotoxemia. J Surg Res [in press].