Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T08:12:48.400Z Has data issue: false hasContentIssue false
  • English
  • Français

Endothelial cells as active participants in veterinary infections and inflammatory disorders

Published online by Cambridge University Press:  13 August 2007

E. Behling-Kelly  and
C. J. Czuprynski
E. Behling-Kelly
Affiliation:
Department of Pathobiological Sciences, University of Wisconsin, School of Veterinary Medicine, 2015 Linden Drive, Madsion WI 53706, USA
C. J. Czuprynski*
Affiliation:
Department of Pathobiological Sciences, University of Wisconsin, School of Veterinary Medicine, 2015 Linden Drive, Madsion WI 53706, USA
*
*Corresponding author. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Endothelial cells were once viewed as relatively inert cells lining the vasculature. They are now recognized as active and responsive regulators of coagulation, platelet adhesion, fluid homeostasis, wound healing, leukocyte extravasation and vascular tone. Endothelial cells play a key role in the host response to infectious agents by regulating leukocyte trafficking, producing inflammatory cytokines and presenting antigen in association with major histocompatibility class II (MHC II) molecules. A number of infectious agents have a tropism for endothelial cells. Infection of endothelial cells can promote thrombosis, vascular leakage, and increased adherence and emigration of leukocytes. Furthermore, activation of a systemic inflammatory response, in the absence of direct endothelial cell infection, can also lead to endothelial cell dysfunction. The purpose of this review is to highlight the interactions between endothelial cells and infectious or inflammatory agents that contribute to coagulation disturbances, vasculitis and edema. A select group of viral and bacterial pathogens will be used as examples to demonstrate how endothelial cell dysfunction contributes to the pathogenesis of infectious and inflammatory disorders.

Keywords

endotheliuminflammationinfectionthrombosis
Type
Review Article
Information
Animal Health Research Reviews , Volume 8 , Issue 1 , June 2007 , pp. 47 - 58
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, E (2000). Tissue factor inhibition and clinical trial results of tissue factor pathway inhibitor in sepsis. Critical Care Medicine 28: S31–S33.Google Scholar
Aderka, D (1991). Role of tumor necrosis factor in the pathogenesis of intravascular coagulopathy of sepsis: potential new therapeutic implications. Israel Journal of Medical Sciences 27: 52–60.Google Scholar
Aird, WC (2006). Mechanisms of endothelial cell heterogeneity in health and disease. Circulation Research 98: 159–162.Google Scholar
Aird, WC, Edelberg, JM, Weiler-Guettler, H, Simmons, WW, Smith, TW and Rosenberg, RD (1997). Vascular bed-specific expression of an endothelial cell gene is programmed by the tissue microenvironment. Journal of Cell Biology 138: 1117–1124.CrossRefGoogle ScholarPubMed
Andrews, JJ, Anderson, TD, Slife, LN and Stevenson, GW (1985). Microscopic lesions associated with the isolation of Haemophilus somnus from pneumonic bovine lungs. Veterinary Pathology 22: 131–136.CrossRefGoogle ScholarPubMed
Bazzoni, G (2006). Endothelial tight junctions: permeable barriers of the vessel wall. Thrombosis and Haemostasis 95: 36–42.Google ScholarPubMed
Behling-Kelly, E, Kim, KS, McClenahan, D and Czuprynski, CJ (2007). Viable Haemophilus Somnus induce myosin light chain kinase-dependent increase in brain endothelial cell permeability. Infection and Immunity (IAI 00028-07 in press).Google Scholar
Bennet, PM and King, AS (1948). Studies on equine purpura hemorrhagica II. Symptomatology. The British Veterinary Journal 104: 414.Google Scholar
Bjerketorp, J, Jacobsson, K and Frykberg, L (2004). The von Willebrand factor-binding protein (vWbp) of Staphylococcus aureus is a coagulase. FEMS Microbiology Letters 234: 309–314.Google Scholar
Black, SJ, Lunn, DP, Yin, C, Hwang, M, Lenz, SD and Belknap, JK (2006). Leukocyte emigration in the early stages of laminitis. Veterinary Immunology and Immunopathology 109: 161–166.Google Scholar
Boffa, MC and Karmochkine, M (1998). Thrombomodulin: an overview and potential implications in vascular disorders. Lupus 7 (suppl. 2): S120–S125.CrossRefGoogle ScholarPubMed
Bombeli, T, Karsan, A, Tait, JF and Harlan, JM (1997). Apoptotic vascular endothelial cells become procoagulant. Blood 89: 2429–2442.CrossRefGoogle ScholarPubMed
Boschwitz, JS and Timoney, JF (1994). Inhibition of C3 deposition on Streptococcus equi subsp. equi by M protein: a mechanism for survival in equine blood. Infection and Immunity 62: 3515–3520.CrossRefGoogle Scholar
Boudreaux, MK, Weiss, RC, Toivio-Kinnucan, M, Cox, N and Spano, JS (1990). Enhanced platelet reactivity in cats experimentally infected with feline infectious peritonitis virus. Veterinary Pathology 27: 269–273.CrossRefGoogle ScholarPubMed
Boyd, B, Tyrrell, G, Maloney, M, Gyles, C, Brunton, J and Lingwood, C (1993). Alteration of the glycolipid binding specificity of the pig edema toxin from globotetraosyl to globotriaosyl ceramide alters in vivo tissue targetting and results in a verotoxin 1-like disease in pigs. The Journal of Experimental Medicine 177: 1745–1753.Google Scholar
Brandtzaeg, P, Bjerre, A, Ovstebo, R, Brusletto, B, Joo, GB and Kierulf, P (2001). Neisseria meningitidis lipopolysaccharides in human pathology. Journal of Endotoxin Research 7: 401–420.Google Scholar
Brown, CC, Meyer, RF and Grubman, MJ (1994). Presence of African horse sickness virus in equine tissues, as determined by in situ hybridization. Veterinary Pathology 31: 689–694.CrossRefGoogle ScholarPubMed
Bryant, AE, Hayes-Schroer, SM and Stevens, DL (2003). M type 1 and 3 group A streptococci stimulate tissue factor-mediated procoagulant activity in human monocytes and endothelial cells. Infection and Immunity 71: 1903–1910.CrossRefGoogle Scholar
Carr, C, Bild, GS, Chang, AC, Peer, GT, Palmier, MO, Frazier, RB, Gustafson, ME, Wun, TC, Creasey, AA, Hinshaw, LB, Taylor, FB and Galluppi, GR (1994). Recombinant E. coli-derived tissue factor pathway inhibitor reduces coagulopathic and lethal effects in the baboon gram-negative model of septic shock. Circulatory Shock 44: 126–137.Google Scholar
Carraway, MS, Welty-Wolf, KE, Miller, DL, Ortel, TL, Idell, S, Ghio, AJ, Petersen, LC and Piantadosi, CA (2003). Blockade of tissue factor: treatment for organ injury in established sepsis. American Journal of Respiratory and Critical Care Medicine 167: 1200–1209.Google Scholar
Carson, SD, Johnson, DR and Tracy, SM (1993). Tissue factor and the extrinsic pathway of coagulation during infection and vascular inflammation. European Heart Journal 14 (suppl. K): 98–104.Google ScholarPubMed
Chen, D, Giannopoulos, K, Shiels, PG, Webster, Z, McVey, JH, Kemball-Cook, G, Tuddenham, E, Moore, M, Lechler, R and Dorling, A (2004). Inhibition of intravascular thrombosis in murine endotoxemia by targeted expression of hirudin and tissue factor pathway inhibitor analogs to activated endothelium. Blood 104: 1344–1349.Google Scholar
Chi, JT, Chang, HY, Haraldsen, G, Jahnsen, FL, Troyanskaya, OG, Chang, DS, Wang, Z, Rockson, SG, van de Rijn, M, Botstein, D and Brown, PO (2003). Endothelial cell diversity revealed by global expression profiling. Proceedings of the National Academy of the Sciences of the Unites States of America 100: 10623–10628.Google Scholar
Chiam, R, Smid, L, Kydd, JH, Smith, KC, Platt, A and Davis-Poynter, NJ (2006). Use of polarised equine endothelial cell cultures and an in vitro thrombosis model for potential characterisation of EHV-1 strain variation. Veterinary Microbiology 113: 243–249.Google Scholar
Colucci, M, Balconi, G, Lorenzet, R, Pietra, A, Locati, D, Donati, MB and Semeraro, N (1983). Cultured human endothelial cells generate tissue factor in response to endotoxin. The Journal of Clinical Investigation 71: 1893–1896.CrossRefGoogle ScholarPubMed
Cornick, NA, Matise, I, Samuel, JE, Bosworth, BT and Moon, HW (1999). Edema disease as a model for systemic disease induced by Shiga toxin-producing E. coli. Advances in Experimental Medicine and Biology 473: 155–161.Google Scholar
Creasey, AA, Chang, AC, Feigen, L, Wun, TC, Taylor, FB Jr and Hinshaw, LB (1993). Tissue factor pathway inhibitor reduces mortality from Escherichia coli septic shock. Journal of Clinical Investigation 91: 2850–2860.CrossRefGoogle ScholarPubMed
Cunningham, M, McCormack, J, Fenderson, P, Ho, M, Beachey, E and Dale, J (1989). Human and murine antibodies cross-reactive with streptococcal M protein and myosin recognize the sequence GLN-LYS-SER-LYS-GLN in M protein. Journal of Immunology 143: 2677–2683.Google Scholar
Dackiw, AP, McGilvray, ID, Woodside, M, Nathens, AB, Marshall, JC and Rotstein, OD (1996). Prevention of endotoxin-induced mortality by antitissue factor immunization. Archives of Surgery 131: 1273–1278; discussion 1278–1279.Google Scholar
Dang, O, Navarro, L and David, M (2004). Inhibition of lipopolysaccharide-induced interferon regulatory factor 3 activation and protection from septic shock by hydroxystilbenes. Shock 21: 470–475.Google Scholar
D'Angelo, A, Della Valle, P, Giudici, D and Vigano D'Angelo, S (2004). Protein C and coagulation in sepsis. Minerva Anestesiologica 70: 339–350.Google ScholarPubMed
Dauphinee, SM and Karsan, A (2005). Lipopolysaccharide signaling in endothelial cells. Laboratory Investigation 86: 9–22.CrossRefGoogle Scholar
Davidson, MG, Breitschwerdt, EB, Walker, DH, Levy, MG, Carlson, CS, Hardie, EM, Grindem, CA and Nasisse, MP (1990). Vascular permeability and coagulation during Rickettsia rickettsii infection in dogs. American Journal of Veterinary Research 51: 165–170.Google Scholar
de Jonge, E, Dekkers, PE, Creasey, AA, Hack, CE, Paulson, SK, Karim, A, Kesecioglu, J, Levi, M, van Deventer, SJ and van der Poll, T (2001). Tissue factor pathway inhibitor does not influence inflammatory pathways during human endotoxemia. The Journal of Infectious Diseases 183: 1815–1818.Google Scholar
DeMaula, CD, Jutila, MA, Wilson, DW and MacLachlan, NJ (2001). Infection kinetics, prostacyclin release and cytokine-mediated modulation of the mechanism of cell death during bluetongue virus infection of cultured ovine and bovine pulmonary artery and lung microvascular endothelial cells. The Journal of General Virology 82: 787–794.Google Scholar
DeMaula, CD, Leutenegger, CM, Bonneau, KR and MacLachlan, NJ (2002). The role of endothelial cell-derived inflammatory and vasoactive mediators in the pathogenesis of bluetongue. Virology 296: 330–337.CrossRefGoogle ScholarPubMed
Dhainaut, JF, Yan, SB, Margolis, BD, Lorente, JA, Russell, JA, Freebairn, RC, Spapen, HD, Riess, H, Basson, B, Johnson, G III and Kinasewitz, GT (2003). Drotrecogin alfa (activated) (recombinant human activated protein C) reduces host coagulopathy response in patients with severe sepsis. Thrombosis and Haemostasis 90: 642–653.Google Scholar
Dosquet, C, Weill, D and Wautier, JL (1995). Cytokines and thrombosis. Journal of Cardiovascular Pharmacology 25 (suppl. 2): S13–S19.Google Scholar
Dudek, SM and Garcia, JG (2001). Cytoskeletal regulation of pulmonary vascular permeability. Journal of Applied Physiology 91: 1487–1500.Google Scholar
Edgington, TS, Mackman, N, Fan, ST and Ruf, W (1992). Cellular immune and cytokine pathways resulting in tissue factor expression and relevance to septic shock. Nouvelle Revue Francaise Hematology 34 (suppl.): S15–S27.Google Scholar
Elghetany, MT and Walker, DH (1999). Hemostatic changes in Rocky Mountain spotted fever and Mediterranean spotted fever. American Journal of Clinical Pathology 112: 159–168.CrossRefGoogle ScholarPubMed
Emerson, TE Jr, Lindsey, DC, Jesmok, GJ, Duerr, ML and Fournel, MA (1992). Efficacy of monoclonal antibody against tumor necrosis factor alpha in an endotoxemic baboon model. Circulatory Shock 38: 75–84.Google Scholar
Erasmus, BJ (1975). Bluetongue in sheep and goats. Australian Veterinary Journal 51: 165–170.CrossRefGoogle ScholarPubMed
Erlich, J, Fearns, C, Mathison, J, Ulevitch, RJ and Mackman, N (1999). Lipopolysaccharide induction of tissue factor expression in rabbits. Infection and Immunity 67: 2540–2546.Google Scholar
Esmon, CT (2003). The protein C pathway. Chest 124: 26S–32S.CrossRefGoogle ScholarPubMed
Faust, SN, Heyderman, RS and Levin, M (2001). Coagulation in severe sepsis: a central role for thrombomodulin and activated protein C. Critical Care Medicine 29: S62–S67; discussion S67-S68.CrossRefGoogle ScholarPubMed
Galan, JE and Timoney, JF (1985). Immune complexes in purpura hemorrhagica of the horse contain IgA and M antigen of Streptococcus equi. Journal of Immunology 135: 3134–3137.Google Scholar
Gannon, VP and Gyles, CL (1990). Characteristics of the Shiga-like toxin produced by Escherichia coli associated with porcine edema disease. Veterinary Microbiology 24: 89–100.CrossRefGoogle ScholarPubMed
Garcia, JG, Davis, HW and Patterson, CE (1995). Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. Journal of Cellular Physiology 163: 510–522.Google Scholar
Gomez-Villamandos, JC, Sanchez, C, Carrasco, L, Laviada, MM, Bautista, MJ, Martinez-Torrecuadrada, J, Sanchez-Vizcaino, JM and Sierra, MA (1999). Pathogenesis of African horse sickness: ultrastructural study of the capillaries in experimental infection. Journal of Comparative Pathology 121: 101–116.Google Scholar
Gouverneur, M, Berg, B, Nieuwdorp, M, Stroes, E and Vink, H (2006). Vasculoprotective properties of the endothelial glycocalyx: effects of fluid shear stress. Journal of Internal Medicine 259: 393–400.Google Scholar
Granger, DN and Kubes, P (1994). The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. Journal of Leukocyte Biology 55: 662–675.Google Scholar
Gryglewski, RJ, Botting, RM and Vane, JR (1988). Mediators produced by the endothelial cell. Hypertension 12: 530–548.Google Scholar
Guerin, JL, Gelfi, J, Dubois, L, Vuillaume, A, Boucraut-Baralon, C and Pingret, JL (2000). A novel polyomavirus (goose hemorrhagic polyomavirus) is the agent of hemorrhagic nephritis enteritis of geese. Journal of Virology 74: 4523–4529.CrossRefGoogle ScholarPubMed
Henson, JB and Crawford, TB (1974). The pathogenesis of virus-induced arterial disease–Aleutian disease and equine viral arteritis. Advances in Cardiology 13: 183–191.Google Scholar
Heyderman, RS, Klein, NJ, Daramola, OA, Hammerschmidt, S, Frosch, M, Robertson, BD, Levin, M and Ison, CA (1997). Induction of human endothelial tissue factor expression by Neisseria meningitidis: the influence of bacterial killing and adherence to the endothelium. Microbial Pathogenesis 22: 265–274.Google Scholar
Hoffman, JN and Faist, E (2000). Coagulation inhibitor replacement during sepsis: useless? Critical Care Medicine 28: S74–S76.Google Scholar
Hoffman, M (2003). Remodeling the blood coagulation cascade. Journal of Thrombosis and Thrombolysis 16: 17–20.CrossRefGoogle ScholarPubMed
Hoffman, M and Monroe, DM III (2001). A cell-based model of hemostasis. Thrombosis and Haemostasis 85: 958–965.Google Scholar
Hoffman, M, Monroe, DM and Roberts, HR (1996). Cellular interactions in hemostasis. Haemostasis 26 (suppl. 1): 12–16.Google ScholarPubMed
Horzinek, MC, Ederveen, J, Egberink, H, Jacobse-Geels, HE, Niewold, T and Prins, J (1986). Virion polypeptide specificity of immune complexes and antibodies in cats inoculated with feline infectious peritonitis virus. American Journal of Veterinary Research 47: 754–761.Google Scholar
Howerth, EW and Tyler, DE (1988). Experimentally induced bluetongue virus infection in white-tailed deer: ultrastructural findings. American Journal of Veterinary Research 49: 1914–1922.Google Scholar
Hurley, DJ, Parks, RJ, Reber, AJ, Donovan, DC, Okinaga, T, Vandenplas, ML, Peroni, JF and Moore, JN (2006). Dynamic changes in circulating leukocytes during the induction of equine laminitis with black walnut extract. Veterinary Immunology and Immunopathology 110: 195–206.Google Scholar
Jacobse-Geels, HE and Horzinek, MC (1983). Expression of feline infectious peritonitis coronavirus antigens on the surface of feline macrophage-like cells. Journal of General Virology 64 (Pt 9): 1859–1866.Google Scholar
Jones, TC, Hunt, RD and King, NW (1997). In Veterinary Pathology. Media, Pennsylvania: Williams and Wilkins.Google Scholar
Kipar, A, May, H, Menger, S, Weber, M, Leukert, W and Reinacher, M (2005). Morphologic features and development of granulomatous vasculitis in feline infectious peritonitis. Veterinary Pathology 42: 321–330.CrossRefGoogle ScholarPubMed
Kuckleburg, CJ, Sylte, MJ, Inzana, TJ, Corbeil, LB, Darien, BJ and Czuprynski, CJ (2005). Bovine platelets activated by Haemophilus somnus and its LOS induce apoptosis in bovine endothelial cells. Microbial Pathogenesis 38: 23–32.Google Scholar
Lacroux, C, Andreoletti, O, Payre, B, Pingret, JL, Dissais, A and Guerin, JL (2004). Pathology of spontaneous and experimental infections by Goose haemorrhagic polyomavirus. Avian Pathology 33: 351–358.Google Scholar
Levi, M, van der Poll, T and ten Cate, H (2006). Tissue factor in infection and severe inflammation. Seminars in Thrombosis and Hemostasis 32: 33–39.Google Scholar
Linggood, MA and Thompson, JM (1987). Verotoxin production among porcine strains of Escherichia coli and its association with oedema disease. Journal of Medical Microbiology 24: 359–362.Google Scholar
Logan, LL, Whyard, TC, Quintero, JC and Mebus, CA (1987). The development of Cowdria ruminantium in neutrophils. Onderstepoort Journal of Veterinary Research 54: 197–204.Google ScholarPubMed
Louise, CB and Obrig, TG (1991). Shiga toxin-associated hemolytic-uremic syndrome: combined cytotoxic effects of Shiga toxin, interleukin-1 beta, and tumor necrosis factor alpha on human vascular endothelial cells in vitro. Infection and Immunity 59: 4173–4179.Google Scholar
Louise, CB and Obrig, TG (1992). Shiga toxin-associated hemolytic uremic syndrome: combined cytotoxic effects of shiga toxin and lipopolysaccharide (endotoxin) on human vascular endothelial cells in vitro. Infection and Immunity 60: 1536–1543.CrossRefGoogle ScholarPubMed
Lum, H and Malik, AB (1996). Mechanisms of increased endothelial permeability. Canadian Journal of Physiology and Pharmacology 74: 787–800.Google ScholarPubMed
MacLachlan, NJ (1994). The pathogenesis and immunology of bluetongue virus infection of ruminants. Comparative Immunology, Microbiology and Infectious Disease 17: 197–206.CrossRefGoogle ScholarPubMed
MacLachlan, NJ, Balasuriya, UB, Rossitto, PV, Hullinger, PA, Patton, JF and Wilson, WD (1996). Fatal experimental equine arteritis virus infection of a pregnant mare: immunohistochemical staining of viral antigens. Journal of Veterinary Diagnostic Investigation 8: 367–374.Google Scholar
Mahrt, CR and Osburn, BI (1986). Experimental bluetongue virus infection of sheep; effect of vaccination: pathologic, immunofluorescent, and ultrastructural studies. American Journal of Veterinary Research 47: 1198–1203.Google Scholar
Mairey, E, Genovesio, A, Donnadieu, E, Bernard, C, Jaubert, F, Pinard, E, Seylaz, J, Olivo-Marin, J-C, Nassif, X and Dumenil, G (2006). Cerebral microcirculation shear stress levels determine Neisseria meningitidis attachment sites along the blood-brain barrier. Journal of Experimental Medicine 203: 1939–1950.Google Scholar
Mallem, MY, Gogny, M, Gautier, F, Bucas, V and Desfontis, JC (2003). Evaluation of beta3-adrenoceptor-mediated relaxation in intact and endotoxin-treated equine digital veins. American Journal of Veterinary Research 64: 708–714.Google Scholar
Matise, I, Sirinarumitr, T, Bosworth, BT and Moon, HW (2000). Vascular ultrastructure and DNA fragmentation in swine infected with Shiga toxin-producing Escherichia coli. Veterinary Pathology 37: 318–327.Google Scholar
Mattsson, E, Herwald, H and Egesten, A (2003). Superantigens from Staphylococcus aureus induce procoagulant activity and monocyte tissue factor expression in whole blood and mononuclear cells via IL-1 beta. Journal of Thrombosis and Haemostasis 1: 2569–2576.Google Scholar
McLaughlin, BE, DeMaula, CD, Wilson, WC, Boyce, WM and MacLachlan, NJ (2003). Replication of bluetongue virus and epizootic hemorrhagic disease virus in pulmonary artery endothelial cells obtained from cattle, sheep, and deer. American Journal of Veterinary Research 64: 860–865.Google Scholar
Mebus, CA and Logan, LL (1988). Heartwater disease of domestic and wild ruminants. Journal of the American Veterinary Medical Association 192: 950–952.Google Scholar
Mehta, D and Malik, AB (2006). Signaling mechanisms regulating endothelial permeability. Physiological Review 86: 279–367.Google Scholar
Mellor, PS and Hamblin, C (2004). African horse sickness. Veterinary Research 35: 445–466.Google Scholar
Mirlashari, MR, Hoiby, EA, Holst, J and Lyberg, T (2001). Outer membrane vesicles from Neisseria meningitidis: effects on cytokine production in human whole blood. Cytokine 13: 91–97.Google Scholar
Momotani, E, Yabuki, Y, Miho, H, Ishikawa, Y and Yoshino, T (1985). Histopathological evaluation of disseminated intravascular coagulation in Haemophilus somnus infection in cattle. Journal of Comparative Pathology 95: 15–23.Google Scholar
Montali, RJ and Strandberg, JD (1972). Extraperitoneal lesions in feline infectious peritonitis. Veterinary Pathology 9: 109–121.Google Scholar
Moore, BD, Balasuriya, UBR, Hedges, JF and MacLachlan, NJ (2002). Growth Characteristics of a highly virulent, a moderately virulent, and an avirulent strain of equine arteritis virus in primary equine endothelial cells are predictive of their virulence to horses. Virology 298: 39–44.Google Scholar
Moriez, R, Salvador-Cartier, C, Theodorou, V, Fioramonti, J, Eutamene, H and Bueno, L (2005). Myosin light chain kinase is involved in lipopolysaccharide-induced disruption of colonic epithelial barrier and bacterial translocation in rats. The American Journal of Pathology 167: 1071–1079.Google Scholar
Nawroth, PP, Handley, DA, Esmon, CT and Stern, DM (1986). Interleukin 1 induces endothelial cell procoagulant while suppressing cell-surface anticoagulant activity. Proceedings of the National Academy of Sciences of the United States of America 83: 3460–3464.CrossRefGoogle ScholarPubMed
Nieuwdorp, M, van Haeften, TW, Gouverneur, MC, Mooij, HL, van Lieshout, MH, Levi, M, Meijers, JC, Holleman, F, Hoekstra, JB, Vink, H, Kastelein, JJ and Stroes, ES (2006). Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55: 480–486.Google Scholar
Obrig, TG, Louise, CB, Lingwood, CA, Boyd, B, Barley-Maloney, L and Daniel, TO (1993). Endothelial heterogeneity in Shiga toxin receptors and responses. The Journal of Biological Chemistry 268: 15484–15488.Google Scholar
Parola, P, Paddock, CD and Raoult, D (2005). Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clinical Microbiology Review 18: 719–756.CrossRefGoogle ScholarPubMed
Pawlinski, R, Pedersen, B, Schabbauer, G, Tencati, M, Holscher, T, Boisvert, W, Andrade-Gordon, P, Frank, RD and Mackman, N (2003). Role of tissue factor and protease activated receptors in a mouse model of endotoxemia. Blood 103: 1342–1347.Google Scholar
Pedersen, NC, Evermann, JF, McKeirnan, AJ and Ott, RL (1984). Pathogenicity studies of feline coronavirus isolates 79–1146 and 79–1683. American Journal of Veterinary Research 45: 2580–2585.Google Scholar
Peroni, JF, Moore, JN, Noschka, E, Grafton, ME, Aceves-Avila, M, Lewis, SJ and Robertson, TP (2006). Predisposition for venoconstriction in the equine laminar dermis: implications in equine laminitis. Journal of Applied Physiology 100: 759–763.Google Scholar
Ray, PE and Liu, XH (2001). Pathogenesis of Shiga toxin-induced hemolytic uremic syndrome. Pediatric Nephrology 16: 823–839.Google Scholar
Roberts, L, Wood, DA, Hunter, AR, Munro, R and Imray, WS (1979). Thromboembolic meningoencephalitis associated with Haemophilus somnus infection. The Veterinary Record 104: 605.Google Scholar
Rydkina, E, Sahni, A, Baggs, RB, Silverman, DJ and Sahni, SK (2006). Infection of human endothelial cells with spotted Fever group rickettsiae stimulates cyclooxygenase 2 expression and release of vasoactive prostaglandins. Infection and Immunity 74: 5067–5074.Google Scholar
Salgado, A, Boveda, JL, Monasterio, J, Segura, RM, Mourelle, M, Gomez-Jimenez, J and Peracaula, R (1994). Inflammatory mediators and their influence on haemostasis. Haemostasis 24: 132–138.Google Scholar
Smith, KC, Whitwell, KE, Mumford, JA, Gower, SM, Hannant, D and Tearle, JP (1993). An immunohistological study of the uterus of mares following experimental infection by equid herpesvirus 1. Equine Veterinary Journal 25: 36–40.Google Scholar
Sporn, LA, Haidaris, PJ, Shi, RJ, Nemerson, Y, Silverman, DJ and Marder, VJ (1994). Rickettsia rickettsii infection of cultured human endothelial cells induces tissue factor expression. Blood 83: 1527–1534.Google Scholar
Sporn, LA, Shi, RJ, Lawrence, SO, Silverman, DJ and Marder, VJ (1991). Rickettsia rickettsii infection of cultured endothelial cells induces release of large von Willebrand factor multimers from Weibel–Palade bodies. Blood 78: 2595–2602.Google Scholar
Stephens, LR, Little, PB, Wilkie, BN and Barnum, DA (1984). Isolation of Haemophilus somnus antigens and their use as vaccines for prevention of bovine thromboembolic meningoencephalitis. American Journal of Veterinary Research 45: 234–239.Google Scholar
Stern, DM, Bank, I, Nawroth, PP, Cassimeris, J, Kisiel, W, Fenton, II JW, Dinarello, C, Chess, L and Jaffe, EA (1985). Self-regulation of procoagulant events on the endothelial cell surface. The Journal of Experimental Medicine 162: 1223–1235.Google Scholar
Stricklett, PK, Hughes, AK, Ergonul, Z and Kohan, DE (2002). Molecular basis for up-regulation by inflammatory cytokines of Shiga toxin 1 cytotoxicity and globotriaosylceramide expression. The Journal of Infectious Diseases 186: 976–982.Google Scholar
Strukova, S (2006). Blood coagulation-dependent inflammation. Coagulation-dependent inflammation and inflammation-dependent thrombosis. Frontiers in Bioscience 11: 59–80.Google Scholar
Sylte, MJ, Corbeil, LB, Inzana, TJ and Czuprynski, CJ (2001). Haemophilus somnus induces apoptosis in bovine endothelial cells in vitro. Infection and Immunity 69: 1650–1660.Google Scholar
Terry, CM and Callahan, KS (1996). Protein kinase C regulates cytokine-induced tissue factor transcription and procoagulant activity in human endothelial cells. The Journal of Laboratory Clinical and Medicine 127: 81–93.Google Scholar
Thompson, KG, Vickers, M C, Stevenson, BJ and Davidson, GW (1987). Thromboembolic meningocephalitis caused by Haemophilus somnus infection in a bull calf-a new disease in New Zealand. New Zealand Veterinary Journal 35: 5–7.Google Scholar
Treiber, KH, Kronfeld, DS and Geor, RJ (2006). Insulin resistance in equids: possible role in laminitis. The Journal of Nutrition 136: 2094S–2098S.Google Scholar
Vachiery, N, Trap, I, Totte, P, Martinez, D and Bensaid, A (1998). Inhibitory effect of Cowdria ruminantium on the expression of MHC class I and class II molecules on bovine endothelial cells. Annals of the New York Academy of Sciences 849: 181–187.Google Scholar
Valbuena, G and Walker, DH (2005). Changes in the adherens junctions of human endothelial cells infected with spotted fever group rickettsiae. Virchows Archiv 446: 379–382.Google Scholar
Veltrop, MH, Thompson, J and Beekhuizen, H (2001). Monocytes augment bacterial species- and strain-dependent induction of tissue factor activity in bacterium-infected human vascular endothelial cells. Infection and Immunity 69: 2797–2807.CrossRefGoogle ScholarPubMed
Wada, Y, Otu, H, Wu, S, Abid, MR, Okada, H, Libermann, T, Kodama, T, Shih, SC, Minami, T and Aird, WC (2005). Preconditioning of primary human endothelial cells with inflammatory mediators alters the ‘set point’ of the cell. FASEB Journal 19: 1914–1916.CrossRefGoogle ScholarPubMed
Walker, DH, Valbuena, GA and Olano, JP (2003). Pathogenic mechanisms of diseases caused by Rickettsia. Annals of the New York Academy of Sciences 990: 1–11.Google Scholar
Weiss, RC, Dodds, WJ and Scott, FW (1980). Disseminated intravascular coagulation in experimentally induced feline infectious peritonitis. American Journal of Veterinary Research 41: 663–671.Google Scholar
Weiss, RC and Scott, FW (1981). Pathogenesis of feline infectious peritonitis: nature and development of viremia. American Journal of Veterinary Research 42: 382–390.Google Scholar
Weiss, RC and Scott, FW (1981). Pathogenesis of feline infetious peritonitis: pathologic changes and immunofluorescence. American Journal of Veterinary Research 42: 2036–2048.Google Scholar
Welty-Wolf, KE, Carraway, MS, Ortel, TL, Ghio, AJ, Idell, S, Egan, J, Zhu, X, Jiao, J-A, Wong, HC and Piantadosi, CA (2006). Blockade of tissue factor-factor X binding attenuates sepsis-induced respiratory and renal failure. American Journal of Physiology Lung Cellular and Molecular Physiology 290: L21–L31.CrossRefGoogle ScholarPubMed
Wiedermann Ch, J and Romisch, J (2002). The anti-inflammatory actions of antithrombin – a review. Acta Medica Austriaca 29: 89–92.Google Scholar
Wohlsein, P, Pohlenz, JF, Salt, JS and Hamblin, C (1998). Immunohistochemical demonstration of African horse sickness viral antigen in tissues of experimentally infected equines. Archives of Virology Supplementum 14: 57–65.Google Scholar
Wu, KK and Thiagarajan, P (1996). Role of endothelium in thrombosis and hemostasis. Annual Review of Medicine 47: 315–331.Google Scholar