Role of the Endothelial Surface Coat
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1 S7 Role of the Endothelial Surface Coat in Microvascular Permeability Christopher Charles Michel Division of Biomedical Sciences, Imperial College School of Medicine, London, UK The luminal glycocalyx of the endothelium plays two rather different roles in determining the permeability of capillaries and venules to fluid and hydrophilic solutes. First, it acts as a barrier impeding the diffusion of macromolecules into the luminal caveolae and intercellular clefts of the continuous endothelium and increasing the hydraulic resistance of fenestrae where the endothelium is fenestrated1. The requirement for a barrier such as the glycocalyx is evident from comparisons between the permeability of microvessels with continuous endothelia and the ultrastructure of the intercellular clefts which form the major pathway for fluid and hydrophilic solutes through the walls of these vessels. Detailed ultrastructure of the intercellular clefts reveals that the tight junctions are interrupted by openings which are too large to act as filters for molecules such as serum albumin. The frequency and dimensions of these openings regulate the fraction of the intercellular cleft which is permeable to fluid and solutes which have passed through the ultrafilter formed by the luminal glycocalyx at the entrance to the clefts. Mathematical models of flow and diffusion through the intercellular clefts with the primary molecular filter being based in a superficial glycocalyx provide a realistic picture which relates ultrastructure to permeability2. The luminal glycocalyx may also have a role in regulating permeability in response to changes in shear stress. There is increasing evidence that the solute permeability of many microvessels increases with the velocity with which they are perfused. In venules of rat mesentery and pig heart, this flow dependent component of permeability can be blocked with NO synthase inhibitors3,4. Very recently in my laboratory, Kajimura has found that flow dependent changes in permeability of rat mesenteric venules to potassium ions are blocked after perfusion of these vessels with neuraminidase. This suggests that glycosylation of molecules of the luminal glycocalyx is important for endothelial cells to sense the shear stress at microvascular walls. It remains to be seen whether the transduction of shear, which signals the increase in permeability, occurs at the luminal surface or whether glycosylation of components of the endothelial glycocalyx is necessary merely to amplify the shear stress signal to the entire endothelial cell. A27
2 References 1. Michel C. C. and Curry F. E. 1999; Physiological Reviews 79, Fu B-M, Curry F. E. and Weinbaum, S. 1995; Amer. J. Physiol. 269, H2124- H Yuan Y., Granger H. J., Zawieja D. C. and Chilian W. M. 1992; Amer. J. Physiol. 263, H641 - H Kajimura M. and Michel C. C. 1999; J. Physiol. 516, A28
3 S8 The Mechanism of the Inhibitory Effect of Hypoxia/Reoxygenation on Gap Junctional Intercellular Communication of Vascular Endothelial Cells in Culture Sei-itsu Murota Department of Cellular Physiological Chemistry, Graduate School, Tokyo Medical and Dental University, Tokyo, Japan Introduction: Parenchymal cells in tissues are known to communicate each other through gap junctions which are intercellular membrane channels that permit the diffusion of ions, small molecules and second messengers between adjacent cells. The structural unit of gap junctions is connexon, a proteinacious cylinder with a hydrophilic channel. The connexon is composed of six subunits called connexin. Gap junctional intercellular communication (GJIC) is an important mechanism for controlling cellular homeostasis, proliferation and differentiation. Since little is known about the influence of hypoxia/reoxygenation on GJIC, we examined it by using cultured human umbilical vein endothelial cells (HUVEC). Experimental: Confluent HUVEC (passages 1-3) were exposed to hypoxia in a chamber purged with an anoxic gas mixture (CO2 5%, N2 95%) for 12h at 37 Ž (PO2<20 mmhg). Reoxygenation was performed by placing the HUVEC in an ambient air atmosphere containing CO2 (5%) at 37 Ž. We analyzed GJIC by the fluorescence recovery after photobleaching technique using an interactive laser cytometer. Adhesion assay - HUVEC grown to confluency were stimulated for 4 hours with LPS and exposed to a LPS-stimulated neutrophils suspension. After incubation for 1 hour, non-adherent neutrophils were removed by washing. Then the GJIC was measured. Results: (1) No morphological changes were observed in HUVEC after hypoxia/reoxygenation. (2) GJIC in HUVEC decreased linearly with time and reached minimum level at 6h after reoxygenation, which was recovered to the basal level after 18-24h. Hypoxia condition alone did not alter GJIC. (3) Hydroxylradical scavengers abolished the reduction in GJIC under hypoxia/reoxygenation conditiion. (4) No significant change was observed in the total expression of connexin 43 after hypoxia/reoxygenation, suggesting some functional disorder occurred in the connexin protein. (5) Because there was 3-4 hours time difference between the generation of free radicals and the occurrence of the connexon dysfunction, we explored the factor responsible for this phenomenon, and found that the generated free radicals triggered TNFa production, which caused inhibition of GJIC. (6) Activated leukocytes also caused inhibition of GJIC, in which ICAM-1/integrin binding and A29
4 tyrosine kinase were deeply involved. Because the suppression was abolished by inhibiting neutrophils adhesion to HUVEC with anti-human ICAM-1 antibody. Assay using intercell chambers, which prevented the direct contact of neutrophils with HUVEC, showed that no suppression of GJIC was observed. The suppression of HUVEC GJIC by adherent neutrophils was not abolished by protease inhibitors, but it was abolished by the pretreatment of HUVEC with tyrosine kinase inhibitors. (7) To characterize the nature of this suppression, we examined the GJIC by anti-icam-1 antibody cross-linking. Even in the absence of activated leukocytes, cross-linking of ICAM-1 to HUVEC caused inhibition of GJIC. Conclusion: GJIC of HUVEC reduced under hypoxia/reoxygenation condition, and this phenomenon was reversible. It was evident that free radicals may play a role in the reduced GJIC under hypoxia/reoxygenation condition. Qualitative but not quantitative change in connexin 43 was observed. Our data also suggest that the suppression of GJIC by adherent leukocytes is mediated by free radicals, but not by proteases and this suppression is attributed to tyrosine phosphorylation of connexin protein. A30
5 S9 Perivascular Cells of Small Cerebral Vessels (FGP; Mato Cells) and Their Permeability under Pathological Condition Masao Mato Department of Anatomy, Jichi Medical School, Tochigi, Japan The FGP (fluorescent granular perithelial) cells contain many autofluorescent inclusion bodies and are localized in the Virchow-Robin space of cerebral microvessels of mammalia including humans. The FGP cells are provided with several epitopes common to monocytic macrophages and potent in the uptake capacity for lipid and protein administered intravenously under physiological conditions. The inclusion bodies in the FGP cells are rich in hydrolytic enzymes and categolized as lysosomes. Under the electron microscope, the inclusions are round in shape and stained moderately intense. After the cerebral insult (cold injury) (experiment 1) and the cerebral ischemia (experiment 2) produced by occlusion of bilateral vertebral arteries and ligation unilateral right carotid artery of Wistar rats, following the increase of pinocytosis in the endothelium, the pinocytosis of FGP cells carried out markedly, and the incorporated substances were transferred into the inclusion bodies in either experiments. Subsequently. lysosomal inclusion bodies decreased in their electron opacity and were vacuolized following intake of plasmal components. Concomitantly, astrocytes are swollen and the border between astrocytes and FGP cells became obscure. In the experiment 1, the increase of pinocytotic vesicles and the decrease of electron opacity of inclusion bodies began to appear within 30 minutes after the treatments and continued over for several days. In the experiment 2, similar changes to the experiment 1 were clearly demonstrated in the FGP cells in the both sides of cerebral cortices within 4 hours and continued for 2 days. However, those changes were more intensive in the ligated side, and some regressive changes appeared in FGP cells at 4 days after the treatment. From these findings, it may be concluded that the morphological changes of FGP cells parallel to those of endothelium within a certain period, but their morphology at the later stage of ligation experiment does not always reflect the hyperpermeability of cerebral microvessels, but is influenced by the blood supply to the FGP cells. A31
6 S10 Proteolytic Disruption of the Blood-Brain Barrier in Neuroinflammation Gary A. Rosenberg Departments of Neurology, Neuroscience, and Cell Biology and Physiology University of New Mexico School of Medicine, Albuquerque, New Mexico, USA Neuroinflammation opens the blood-brain barrier (BBB) in multiple sclerosis, meningitis, AIDS, metastatic spread of cancer to the brain, and reperfusion injury after stroke. Matrix metalloproteinases (MMPs) are Zn+2-containing, Ca2+-dependent neutral proteases that attack a variety of extracellular matrix components.1 Release and activation of MMPs attacks the basal lamina surrounding the capillary and opens the BBB.2 During the neuroinflammatory response, proteases are released from brain cells and from invading leukocytes. Atrocytes, microglia, and endothelial cells make the MMPs. Gelatinase B (92-kDa type IV collagenase) is induced by the intracerebral injection of tumor necrosis factor (TNF-ƒ ), or lipopolysaccharide (LPS) injection3,4 and in permanent and transient occlusion of the middle cerebral artery.5 Reperfusion of brain after a 2-hour middle cerebral artery occlusion causes a biphasic opening of the BBB. The early opening corresponds to an increase in gelatinase A (72-kDa type IV collagenase), and the late opening with gelatinase B.6 Synthetic inhibitors to metalloproteinases blocked the initial opening of the BBB and the cerebral edema at 24 hours. Immunochemistry for the MMPs showed that normal rats have gelatinase A in glia cell processes next to blood vessels and beneath the ependymal and pial surfaces. An increase in gelatinase A was seen 3 hours after the stroke. At 24 and 48 hours stromelysin and gelatinase B were increased in the region of the stroke. Both enzymes were seen diffusely in the extracellular space, and around blood vessels. We conclude that gelatinase A is found normally in glia cell processes near cerebral blood vessels where it contributes to fluid regulation. Reperfusion opens the BBB by induction of gelatinase A at the early stage and of gelatinase B and stromelysin at the later stage. Proteolytic attack on the extracellular matrix is an important mechanism of blood vessel damage secondary to neuroinflammation after an ischemic injury. A32
7 References 1. Mun-Bryce S, Rosenberg GA. - Matrix metalloproteinases in cerebrovascular disease. [Review] - Joumal of Cerebral Blood Flow & Metabolism 1998 Nov; 18 (11): Rosenberg GA, Kornfeld M, Estrada E, Kelley RO, Liotta LA, Stetler-Stevenson WG. TIMP-2 reduces proteolytic opening ofblood-brain barrier by type IV collagenase. Brain Res 1992; 576: Rosenberg GA, Estrada EY, Dencoff JE, Stetler-Stevenson WG. Tumor necrosis factor -alpha-induced gelatinase B causes delayed opening of the blood-brain barrier: an expanded therapeutic window. Brain Res 1995; 703: Mun-Bryce S, Rosenberg GA. Gelatinase B modulates selective opening of die blood-brain barrier during inflammation. American Journal of Physiology 1998; 274: R Rosenberg GA, Navratil M, Barone F, Feuerstein G. Proteolytic cascade enzymes increase in focal cerebral ischemia in rat. Joumal of Cerebral Blood Flow & Metabolism 1996; 16: Rosenberg GA, Estrada EY, Dencoff JE. - Matrix metalloproteinases and TIMPs are associated with blood-brain barrier opening after reperfusion in rat brain. - Stroke 1998 Oct; 29 (10): A33
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