Morphologic assessment of leukocyte-endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion
Purchase on Springer.com
$39.95 / €34.95 / £29.95*
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.
Intravital microscopic studies of the mesenteric microcirculation have demonstrated that leukocyte adherence and emigration in postcapillary venules are a characteristic feature of tissues exposed to ischemia-reperfusion. The objectives of this study were to determine whether: (1) neutrophils are the predominant leukocytes that adhere and emigrate in postischemic mesenteric venules, and (2) leukocyte adherence and/or emigration are a prerequisite for reperfusion-induced increases in venular permeability. Leukocyte kinetics in cat mesenteric venules (25–35μm diameter) were evaluated using both intravital microscopy and quantitative morphometry. The intestine and mesentery were exposed to 60 min of ischemia, followed by 60 min reperfusion. Some animals were pretreated with a monoclonal antibody (MoAb IB4) against the leukocyte adhesion glycoprotein, CD11/CD18. Vessels observed by intravital microscopy and adjacent venules of similar diameter were excised and processed for light (LM) and electron microscopy (EM). Horseradish peroxidase (HRP), administered intravenously, was used to assess vascular permeability by EM. By LM, the control (nonischemic) mesentery is sparsely populated by plasma cells, mast cells, and leukocytes; 30–50% of the resident population is neutrophils. Ischemia-reperfusion led to a significant increase in the number of extravascular cells, with neutrophils accounting for >80% of the total cell population. Control and ischemic venules demonstrated no leakage of HRP into the interstitium. However, venules exposed to ischemia and reperfusion demonstrated HRP leakage between endothelial cells and into the surrounding interstitium; neutrophils were adherent to the luminal surface of the endothelium, transmigrating the vessel wall, and in the surrounding interstitium. Animals pretreated with MoAb IB4 presented the same cell profile as nonischemic controls, with no adherent or transmigrating neutrophils. However, some HRP leakage was noted following reperfusion in venules treated with MoAb IB4. The results of this study indicate that: (1) neutrophils are the predominate leukocytes that adhere and emigrate in postischemic venules, and (2) inhibition of leukocyte adhesion does not completely prevent the venular dysfunction associated with ischemia-reperfusion.
- Granger, D. N. 1988. Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury.Am. J. Physiol. 255:H1269-H1275.
- Granger, D. N., M. E. Hollwarth, andD. A. Parks. 1986. Ischemia-reperfusion injury: Role of oxygen-derived free radicals.Acta Physiol. Scand. (suppl.) 548:47–53.
- Fujimoto, K., V. H.Price, D. N.Granger, R.Specian, S.Bergstedt, and P.Tso. 1991. Effect of ischemia-reperfusion on lipid digestion and absorption in rat intestine.Am. J. Physiol. (in press).
- Harlan, J. M. 1985. Leukocyte-endothelial cell interactions.Blood 65:513–525.
- Arfors, K. E., G. Rutili, andE. Svensjo. 1979. Microvascular transport of macromolecules in normal and inflammatory conditions.Acta. Physiol. Scand. (Suppl.) 463:93–103.
- Granger, D. N., Benoit, J. N., Suzuki, M., andGrisham, M. B. 1989. Leukocyte adherence to venular endothelium during ischemia-reperfusion.Am. J. Physiol. 257:G683-G688.
- Messmer, K., Sack, F. U., Menger, M. D., Barlett, R., Barker, J. H., andHammersen, F. 1988. White cell-endothelium interaction during postischemic perfusion of skin and skeletal muscle.Adv. Exp. Med. Biol. 242:95–103.
- Grisham, M. B., L. A. Hernandez, andD. N. Granger. 1986. Xanthine oxidase and neutrophil infiltration in intestinal ischemia.Am. J. Physiol. 251:G567-G571.
- Hernandez, L. A., M. B. Grisham, B. Twohig, K. E. Arfors, J. M. Harlan, andD. N. Granger. 1987. Role of neutrophils in ischemia-reperfusion-induced microvascular injury.Am. J. Physiol. 253:H699-H703.
- Kubes, P., G. Ibbotson, J. Russell, J. L. Wallace, andD. N. Granger. 1990. Role of platelet-activating factor in ischemia/reperfusion-induced leukocyte adherence.Am. J. Physiol. 259:G300-G305.
- Wright, S. D., D. E. Rao, W. C. Van Voorhis, L. S. Craigmyle, K. Iida, M. A. Talle, E. F. Westberg, G. Goldstein, andS. C. Silverstein. 1983. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies.Proc. Natl. Acad. Sci. U.S.A. 80:5699–5704.
- Suzuki, M., W. Inauen, P. R. Kvietys, M. B. Grisham, C. J. Meininger, M. E. Schelling, H. J. Granger, andD. N. Granger. 1989. Superoxide mediates reperfusion-induced leukocyte-endothelial cell interactions.Am. J. Physiol. 257:H1740-H1745.
- Perry, M. A., andD. N. Granger. 1991. Role of CD11/CD18 in shear rate-dependent leukocyte-endothelial cell interactions in cat mesenteric venules.J. Clin. Invest. 87:1798–1804.
- House, S. D., andH. Lipowsky. 1987. Leukocyte-endothelium adhesion: Microhemodynamics in mesentery of the cat.Microvasc. Res. 34:363–379.
- Watson, M. L. 1958. Staining of tissue sections for electron microscopy with heavy metals.J. Biophys. Biochem. Cytol. 4:727–729.
- Reynolds, E. S. 1963. The use of lead citrate at high pH as an electron opaque stain in electron microscopy.J. Cell Biol. 17:208–212.
- Kvietys, P. R., B. Twohig, J. Danzell, andR. D. Specian. 1990. Ethanol-induced injury to the rat gastric mucosa: Role of neutrophils and xanthine oxidase derived radicals.Gastroenterology 98:909–920.
- Wallace, J. L., C. M. Keenan, andD. N. Granger. 1990. Gastric ulceration induced by non-steroidal anti-inflammatory drugs is a neutrophil-dependent process.Am. J. Physiol. 259:G462-G467.
- Grisham, M. B., J. N. Benoit, andD. N. Granger. 1990. Assessment of leukocyte involvement during ischemia and reperfusion of the intestine.Methods Enzymol. 186:729–742.
- Lewis, R. E., andH. J. Granger. 1988. Diapedesis and the permeability of venous microvessels to protein macromolecules: The impact of leukotriene B4.Microvasc. Res. 35:27–47.
- Lewis, R. E., R. A. Miller, andH. J. Granger. 1989. Acute microvascular effects of the chemotactic peptideN-fonnyl-methionyl-leucyl-phenylalanine: Comparisons with leukotriene B4.Microvasc. Res. 37:53–69.
- Zimmerman, B. J., andD. N. Granger. 1990. Reperfusion-induced leukocyte infiltration: Role of elastase.Am. J. Physiol. 259:H390-H394.
- Inauen, W., D. N. Granger, C. J. Meininger, M. E. Schelling, H. J. Granger, andP. R. Kvietys. 1990. An in vitro model of ischemia/reperfusion-induced microvascular injury.Am. J. Physiol. 259:G134-G139.
- Inauen, W., D. N. Granger, C. J. Meininger, M. E. Schelling, H. J. Granger, andP. R. Kvietys. 1990. Anoxia-reoxygenation-induced, neutrophil-mediated endothelial cell injury: Role of elastase.Am. J. Physiol. 259:H925-H931.
- Kubes, P., andD. N. Granger. 1989. Interaction between circulating granulocytes and xanthine oxidase-derived oxidants in the postischemic intestine.In Clinical Aspects of O2 Transport and Tissue Oxygenation. K. Reinhart and K. Eyrich, editors. Springer-Verlag, Berlin. 133–147.
- Morphologic assessment of leukocyte-endothelial cell interactions in mesenteric venules subjected to ischemia and reperfusion
Volume 15, Issue 5 , pp 331-346
- Cover Date
- Print ISSN
- Online ISSN
- Kluwer Academic Publishers-Plenum Publishers
- Additional Links
- Industry Sectors
- Author Affiliations
- 1. Departments of Cellular Biology and Anatomy, and Physiology, Louisiana State University Medical Center, Shreveport, Louisiana
- 2. School of Physiology and Pharmacology, University of New South Wales, Kensington, Australia