Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-17T03:24:16.287Z Has data issue: false hasContentIssue false
  • English
  • Français

Acute Lung Injury Induced by Staphylococcal enterotoxin B: Disruption of Terminal Vessels as a Mechanism of Induction of Vascular Leak

Published online by Cambridge University Press:  10 May 2012

Ali Imran Saeed ,
Sadiye Amcaoglu Rieder ,
Robert L. Price ,
James Barker ,
Prakash Nagarkatti  and
Mitzi Nagarkatti
Ali Imran Saeed
Affiliation:
Division of Pulmonology, Department of Internal Medicine, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Sadiye Amcaoglu Rieder
Affiliation:
Department of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Robert L. Price
Affiliation:
Department of Cell Biology and Anatomy, University of South Carolina School of Medicine, Columbia, SC 29209, USA
James Barker
Affiliation:
Division of Pulmonology, Department of Internal Medicine, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Prakash Nagarkatti
Affiliation:
Department of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC 29209, USA
Mitzi Nagarkatti*
Affiliation:
Department of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC 29209, USA
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

The current hypothesis of alveolar capillary membrane dysfunction fails to completely explain the severe and persistent leak of protein-rich fluid into the pulmonary interstitium, seen in the exudative phase of acute lung injury (ALI). The presence of intact red blood cells in the pulmonary interstitium may suggest mechanical failure of pulmonary arterioles and venules. These studies involved the pathological and ultrastructural evaluation of the pulmonary vasculature in Staphylococcal enterotoxin B (SEB)-induced ALI. Administration of SEB resulted in a significant increase in the protein concentration of bronchoalveolar lavage fluid and vascular leak in SEB-exposed mice compared to vehicle-treated mice. In vivo imaging of mice demonstrated the pulmonary edema and leakage in the lungs of SEB-administered mice. The histopathological studies showed intense clustering of inflammatory cells around the alveolar capillaries with subtle changes in architecture. Electron microscopy studies further confirmed the diffuse damage and disruption in the muscularis layer of the terminal vessels. Cell death in the endothelial cells of the terminal vessels was confirmed with TUNEL staining. In this study, we demonstrated that in addition to failure of the alveolar capillary membrane, disruption of the pulmonary arterioles and venules may explain the persistent and severe interstitial and alveolar edema.

Keywords

electron microscopypulmonary vascular leakacute respiratory distress syndromeacute lung injury
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 18 , Issue 3 , June 2012 , pp. 445 - 452
Copyright
Copyright © Microscopy Society of America 2012

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

Artigas, A., Bernard, G.R., Carlet, J., Dreyfuss, D., Gattinoni, L., Hudson, L., Lamy, M., Marini, J.J., Matthay, M.A., Pinsky, M.R., Spragg, R. & Suter, P.M. (1998). The American-European Consensus Conference on ARDS, part 2: Ventilatory, pharmacologic, supportive therapy, study design strategies, and issues related to recovery and remodeling. Acute respiratory distress syndrome. Am J Respir Crit Care Med 157, 1332–1347.CrossRefGoogle ScholarPubMed
Baffert, F., Le, T., Thurston, G. & McDonald, D.M. (2006). Angiopoietin-1 decreases plasma leakage by reducing number and size of endothelial gaps in venules. Am J Physiol Heart Circ Physiol 290, 107–118.CrossRefGoogle ScholarPubMed
Beasley, M.B. (2010). The pathologist's approach to acute lung injury. Arch Pathol Lab Med 134, 719–727.Google Scholar
Bernard, G.R., Artigas, A., Brigham, K.L., Carlet, J., Falke, K., Hudson, L., Lamy, M., Legall, J.R., Morris, A. & Spragg, R. (1994). The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. Am J Respir Crit Care Med 149, 818–824.CrossRefGoogle ScholarPubMed
Campbell, W.N., Fitzpatrick, M., Ding, X., Jett, M., Gemski, P. & Goldblum, S.E. (1997). SEB is cytotoxic and alters EC barrier function through protein tyrosine phosphorylation in vitro. Am J Physiol 273, 31–33.Google Scholar
Collar, J.E., Ladva, S., Cairns, T.D. & Cattell, V. (2001). Red cell traverse through thin glomerular basement membranes. Kidney Int 59, 2069–2072.Google Scholar
Diaz, J.V., Brower, R., Calfee, C.S. & Matthay, M.A. (2010). Therapeutic strategies for severe acute lung injury. Crit Care Med 38, 1644–1650.CrossRefGoogle ScholarPubMed
Fraser, J.D. & Proft, T. (2008). The bacterial superantigen and superantigen-like proteins. Immunol Rev 225, 226–243.Google Scholar
Green, D.R., Oberst, A., Dillon, C.P., Weinlich, R. & Salvesen, G.S. (2011). RIPK-dependent necrosis and its regulation by caspases: A mystery in five acts. Mol Cell 44, 9–16.Google Scholar
Henghold, W.B. 2nd (2004). Other biologic toxin bioweapons: Ricin, staphylococcal enterotoxin B, and trichothecene mycotoxins. Dermatol Clin 22, 257–262.CrossRefGoogle ScholarPubMed
Liapis, H., Foster, K. & Miner, J.H. (2002). Red cell traverse through thin glomerular basement membrane. Kidney Int 61, 762–763.Google Scholar
Lucas, R., Verin, A.D., Black, S.M. & Catravas, J.D. (2009). Regulators of endothelial and epithelial barrier integrity and function in acute lung injury. Biochem Pharmacol 77, 1763–1772.CrossRefGoogle ScholarPubMed
Maniatis, N.A., Kotanidou, A., Catravas, J.D. & Orfanos, S.E. (2008). Endothelial pathomechanisms in acute lung injury. Vascul Pharmacol 49, 119–133.CrossRefGoogle ScholarPubMed
Mattix, M.E., Hunt, R.E., Wilhelmsen, C.L., Johnson, A.J. & Baze, W.B. (1995). Aerosolized staphylococcal enterotoxin B-induced pulmonary lesions in rhesus monkeys (Macaca mulatta). Toxicol Pathol 23, 262–268.Google Scholar
Matute-Bello, G., Frevert, C.W. & Martin, T.R. (2008). Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295, 379–399.Google Scholar
Maybauer, M.O., Maybauer, D.M. & Herndon, D.N. (2006). Incidence and outcomes of acute lung injury. N Engl J Med 354, 416–417.Google ScholarPubMed
McDonald, D.M. (1994). Endothelial gaps and permeability of venules in rat tracheas exposed to inflammatory stimuli. Am J Physiol 266, 61–83.Google Scholar
Neumann, B., Engelhardt, B., Wagner, H. & Holzmann, B. (1997). Induction of acute inflammatory lung injury by Staphylococcal enterotoxin B. J Immunol 158, 1862–1871.CrossRefGoogle ScholarPubMed
Persson, C.C. (1986). The role of microvascular permeability in the pathogenesis of asthma. Eur J Respir Dis Suppl 144, 190–216.Google ScholarPubMed
Peter, J.V., John, P., Graham, P.L., Moran, J.L., George, I.A. & Bersten, A. (2007). Corticosteroids in the prevention and treatment of acute respiratory distress syndrome (ARDS) in adults: Meta-analysis. BMJ 336, 1006–1009.CrossRefGoogle Scholar
Rafi, A.Q., Zeytun, A., Bradley, M.J., Sponenberg, D.P., Grayson, R.L., Nagarkatti, M. & Nagarkatti, P.S. (1998). Evidence for the involvement of Fas ligand and perforin in the induction of vascular leak syndrome. J Immunol 161, 3077–3086.CrossRefGoogle ScholarPubMed
Rafi-Janajreh, A.Q., Chen, D., Schmits, R., Mak, T.W., Grayson, R.L., Sponenberg, D.P., Nagarkatti, M. & Nagarkatti, P.S. (1999). Evidence for the involvement of CD44 in endothelial cell injury and induction of vascular leak syndrome by IL-2. J Immunol 163, 1619–1627.CrossRefGoogle ScholarPubMed
Rieder, S.A., Nagarkatti, P. & Nagarkatti, M. (2011). Cd1d-independent activation of invariant natural killer T cells by Staphylococcal enterotoxin B through major histocompatibility complex class II/T cell receptor interaction results in acute lung injury. Infect Immun 79, 3141–3148.Google Scholar
Teke, Z., Adali, F., Kelten, E.C., Enli, Y., Sackan, K.G., Karaman, K., Akbulut, M. & Goksin, I. (2011). Mannitol attenuates acute lung injury induced by infrarenal aortic occlusion-reperfusion in rats. Surg Today 41, 955–965.Google Scholar
Tomashefski, J.F. Jr. (2000). Pulmonary pathology of acute respiratory distress syndrome. Clin Chest Med 21, 435–466.Google Scholar
Tsushima, K., King, L.S., Aggarwal, N.R., De Gorordo, A., D'Alessio, F.R. & Kubo, K. (2009). Acute lung injury review. Intern Med 48, 621–630.Google Scholar
Wheeler, A.P. & Bernard, G.R. (2007). Acute lung injury and the acute respiratory distress syndrome: A clinical review. Lancet 369, 1553–1564.Google Scholar