Review article
The effect of oxidant gases on membrane fluidity and function in pulmonary endothelial cells

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Abstract

Free radicals and oxidant gases, such as oxygen (O2) and nitrogen dioxide (NO2), are injurious to mammalian lung cells. One of the postulated mechanisms for the cellular injury associated with these gases and free radicals involves peroxidative cleavage of membrane lipids. We have hypothesized that oxidant-related alterations in membrane lipids may result in disordering of the plasma membrane lipid bilayer, leading to derangements in membrane-dependent functions. To test hypothesis, we examined the effect of exposure to high partial pressures of O2 or NO2 on the physical state and function of pulmonary endothelial cell plasma membranes. Both hyperoxia (95% O2 at 1 ATA) and NO2 exposure (5 ppm) caused early and significant decreases in fluidity in the hydrophobic interior of the plasma membrane lipid bilayer and subsequent depressions in plasma membrane-dependent transport of 5-hydroxytryptamine. Lipid domains at the surface of pulmonary endothelial cell plasma membranes are more susceptible to NO2-induced injury than to hyperoxic injury. Alterations in the fluidity of these more superficial domains are associated with derangements in surface dependent functions, such as receptor-ligand interaction. These results support our hypothesis and advance our understanding of how the chemical events of free radical injury associated with high O2 and NO2 tensions are translated into functional manifestations of O2 and NO2-induced cellular injury.

References (62)

  • G.M. Rosen et al.

    Disruption of erythrocyte membranal organization by superoxide

    J. Biol. Chem.

    (1983)
  • A.W. Girotti et al.

    Damaging effects of oxygen radicals on resealed erythrocyte ghosts

    J. Biol. Chem.

    (1984)
  • E.R. Block et al.

    Effect of oxygen and endotoxin on lactate dehydrogenase release, 5-hydroxytryptamine uptake, and antioxidant enzyme activities in endothelial cells

    J. Cell. Physiol.

    (1985)
  • R.F.R. Brown et al.

    The histopathology of rat lungs following short term exposures to mixed oxides of nitrogen (NOx)

    Br. J. Exp. Pathol.

    (1983)
  • J.M. Patel et al.

    Nitrogen dioxide-induced changes in cell membrane fluidity and function

    Am. Rev. Respir. Dis.

    (1986)
  • R.S. Bar et al.

    Interactions of multiplication-stimulating activity with bovine endothelium: comparative studies in primary, passaged, and cloned cultures from the pulmonary and systemic circulations

    Endocrinology

    (1982)
  • A.P. Fishman

    Endothelium: A distributed organ of diverse capabilities

    Ann. N.Y. Acad. Sci.

    (1982)
  • J.W. Ryan et al.

    Pulmonary endothelial cells

  • A.P. Fishman et al.

    Handling of vasoactive material by the lung

    N. Engl. J. Med.

    (1974)
    A.P. Fishman et al.

    Handling of vasoactive material by the lung

    N. Engl. J. Med.

    (1974)
  • K.J. Dobuler et al.

    Early detection of oxygen-induced lung injury in conscious rabbits

    Am. Rev. Respir. Dis.

    (1982)
  • E.R. Block et al.

    Depression of serotonin clearance by rat lungs during oxygen exposure

    J. Appl. Physiol.: Respirat. Environ. Exercise Physiol.

    (1977)
  • A.H. Krulewitz et al.

    The effect of oxygen tension on the in vitro production and release of angiotensin converting enzyme by bovine pulmonary artery endothelial cells

    Am. Rev. Respir. Dis.

    (1984)
  • B.E. Barry et al.

    Patterns of accumulation of platelets and neutrophils in rat lungs during exposure to 100% and 85% oxygen

    Am. Rev. Respir. Dis.

    (1985)
  • M.D. Boogaerts et al.

    Enhancement of granulocyte endothelial cell adherence and granulocyte-induced cytotoxicity by platelet release products

  • J.E. Repine et al.

    Tate P.M.

    Neutrophils and lung edema

    Chest

    (1982)
  • J.H. Newman et al.

    Effect of 100% oxygen on lung vascular function in awake sheep

    J. Appl. Physiol.: Respirat. Environ. Exercise Physiol.

    (1983)
  • A.J. Erdmann et al.

    Pure oxygen breathing increases sheep lung microvascular permeability

    Anesthesiology

    (1983)
  • D.M. Shasby et al.

    Reversible oxidant induced increases in permeability of cultured endothelium: alterations in cell shape and calcium homeostasis

    Blood

    (1985)
  • S.J. Weiss

    Oxygen, ischemia and inflamation

    Acta. Physiol. Scand.

    (1986)
  • S.J. Singer et al.

    The fluid mosaic model of the structure of cell membranes

    Science

    (1972)
  • M.D. Houslay et al.

    Dynamics of Biological Membranes

    (1983)
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      The molecular mechanisms mediating membrane blebbing are largely unknown, but several potential mechanisms have been hypothesized and reviewed elsewhere (D'Agostino et al., 2009). In brief, membrane blebbing may occur via (1) altered membrane phospholipid organization (Sabatini et al., 2006; Megli and Sabatini, 2004; Megli and Russo, 2007), (2) changes in plasma membrane fluidity (Patel and Block, 1988; Block et al., 1986; Urano et al., 1998; Joseph et al., 1998), and/or (3) oxidation of cytoskeletal proteins (Miyoshi et al, 1996) and membrane–cytoskeleton bonds such as adhesion molecules (Sheetz et al., 2006). Oxidation of lipid–protein bonds that tether the two nanostructures together could result in localized protrusions of the plasma membrane as a result of intracellular hydrostatic pressure (Charras et al., 2005), causing patches of membrane that separate from the underlying cytoskeleton (Dai and Sheetz, 1999). (

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    1

    Jawalharlal M. Patel received a Ph.D. in Biochemistry from Marathwada University in India in 1973 and was a Visiting Fellow at the National Institute of Environmental Health Sciences in Research Triangle Park, NC from 1974–1977. Dr. Patel is currently as Assistant Research Scientist in the Pulmonary Medicine Division of the Department of Medicine at the University of Florida. Dr. Patel's primary research interests include drug metabolism, the biochemical toxicity of inhaled compounds, and the cell biology of the lung.

    2

    Edward R. Block was awarded and M.D. by the Johns Hopkins School of Medicine in 1968. After completing internal medicine residency training at Johns Hopkins Hospital, he spent three years at the National Institute of Allergy and Infections Diseases and then completed a fellowship in Pulmonary Medicine and Physiology at the University of Pennsylvania. Dr. Block is presently Associate Chief of Staff for Research at the Veterans Administration Medical Center in Gainesville adn is a Professor of Medicine at the University of Florida, College of Medicine. He is interested in the cell biology of the pulmonary endothelium, and his current research activities focus on the effects of high and low partial pressures of oxygen on the structure and function of the plasma membrane of pulmonary endothelial cells.

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