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Comparison of inhibitory effects of oxygen radicals and calf serum protein on surfactant activity

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Abstract

The effects of the reactive oxygen species (ROS) superoxide anion (O .2 −) and hydroxyl radical (•OH) on the surface tension lowering properties of bovine lipid extract surfactant (BLES) were compared to the effects of calf serum protein (CSP) in a captive bubble surfactometer (CBS). O .2 − was generated from xanthine/xanthine oxidase (X/XO), and •OH was generated by the Fenton reaction. ROS were demonstrated by electron spin resonance (ESR) using 5,5-dimethyl-1-pyrroline-N-oxide (DMPO) as the spin trap. Lipid peroxidation was measured using the thiobarbituric acid method. •OH had broad inhibitory effects on surface tension parameters, including adsorption, minimum surface tension, percentage film area change and film compressibility. O .2 − showed inhibitory effects on adsorption, film area change and film compressibility but had no significant effect on minimum surface tension. Both O .2 − and •OH treatment were associated with a large ‘squeezeout’ plateau around 20–25 mN/m in the surface tension—area relation, indicating poor film organization during the compression phase. At the concentrations used, ROS were associated with lipid peroxidation of BLES, which also demonstrated radical scavenging properties. Calf serum protein produced inhibitory effects on adsorption, minimum surface tension and percentage film area change that were quantitatively similar to those produced by •OH. The effects on film compression were significantly greater and qualitatively different from those seen with either O .2 − or •OH. We conclude that the inhibition of BLES surface activity by ROS and inhibitory proteins can be distinguished in the captive bubble surfactometer and, particularly, by changes in the film compressibility modulus.

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References

  1. Wright JR, Clements JA: Metabolism and turnover of lung surfactant. Am Rev Respir Dis 135: 426-444, 1987

    PubMed  Google Scholar 

  2. Veldhuizen RK, Nag K, Orgeig S, Possmayer F: The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408: 180-202, 1998

    PubMed  Google Scholar 

  3. Possmayer F: Physico-chemical aspects of pulmonary surfactant. In: R.A. Polin, W.W. Fox (eds). Fetal and Neonatal Physiology. W & B Saunders, Philadelphia, PA, 1997, pp 1259-1275

    Google Scholar 

  4. Bachofen H, Schürch S, Urbinelli M, Weibel ER: Relations among alveolar surface tension, surface area, volume, and recoil pressure. J Appl Physiol 62: 1878-1887, 1987

    PubMed  Google Scholar 

  5. Spragg RG, Gilliard N, Richman P, Smith RM, Hite D, Papert D, Heldt GP, Merritt TA: The adult respiratory distress syndrome: Clinical aspects relevant to surfactant supplementation. In: B. Robertson, L.M.G. van Golde, J.J. Batenburg (eds). Pulmonary Surfactant: From Molecular Biology to Clinical Practice, vol. 1. Elsevier Science, Amsterdam, 1992, pp 685-703.

    Google Scholar 

  6. Ward PA, Johnson KJ, Till GO: Current concepts regarding adult respiratory distress syndrome. Ann Emerg Med 14: 724-728, 1985

    Article  PubMed  Google Scholar 

  7. Lewis JF, Veldhuizen R: The role of exogenous surfactant in the treatment of acute lung injury. Annu Rev Physiol 65: 613-642, 2003

    Article  PubMed  Google Scholar 

  8. Oosting RS, van Iwaarden JF, van Bree L, Verhoef J, van Golde LMG, Haagsman HP: Exposure of surfactant protein A to ozone in vitro and in vivo impairs its interactions with alveolar cells. Am J Physiol 262: L63-L68, 1992

    PubMed  Google Scholar 

  9. Muller B, Barth P, von Wichert P: Structural and functional impairment of surfactant protein A after exposure to nitrogen dioxide in rats. Am J Physiol 263: L177-L184, 1992

    PubMed  Google Scholar 

  10. Silva MF, Saldiva PH: Paraquat poisoning: An experimental model of dose dependent acute lung injury due to surfactant dysfunction. Braz J Med Biol Res 31: 445-450, 1998

    PubMed  Google Scholar 

  11. Haagsman HP, van Golde LMG: Lung surfactant and pulmonary toxicology. Lung 163: 275-303, 1985

    PubMed  Google Scholar 

  12. Grum CM, Ragsdale RA, Ketai LH, Simon RH: Plasma xanthine oxidase activity in patients with adult respiratory distress syndrome. J Crit Care 2: 22-26, 1987

    Article  Google Scholar 

  13. Haddad IY, Ischiropoulos H, Holm BA, Beckman JS, Baker JR, Matalon S: Mechanisms of peroxynitrite-induced injury to pulmonary surfactants. Am J Physiol 265: L555-L564, 1993

    PubMed  Google Scholar 

  14. Matalon S, DeMarco V, Haddad IY, Myles C, Skimming JW, Schürch S, Cheng S, Cassin S: Inhaled nitric oxide injures the pulmonary surfactant system of lambs in vivo. Am J Physiol 270: L272-L280, 1996

    Google Scholar 

  15. Ryan SF, Ghassibi Y, Liau DF: Effects of activated polymorphonuclear leukocytes upon pulmonary surfactant in vitro. Am J Respir Cell Mol Biol 4: 33-41, 1991

    PubMed  Google Scholar 

  16. Cantin AM, North SL, Hubbard RC, Crystal RG: Normal alveolar epithelial lining fluid contains high levels of glutathione. J Appl Physiol 63: 152-157, 1987

    PubMed  Google Scholar 

  17. Davis WB, Pacht ER: Extracellular antioxidant defenses. In: R.G. Crystal, J.B. West (eds). The Lung: Scientific Foundations, 2nd ed. Lippincott-Raven, Philadelphia, PA, 1997, pp 2271-2278

    Google Scholar 

  18. Jackson RM: Molecular, pharmacologic, and clinical aspects of oxygen-induced lung injury. Clin Chest Med 11: 73-83, 1990

    PubMed  Google Scholar 

  19. Lewis JF, Veldhuizen RAW: Factors influencing the efficacy of exogenous surfactant in acute lung injury. Biol Neonate 67(suppl 1): 48-60, 1995

    PubMed  Google Scholar 

  20. Gilliard N, Heldt GP, Gasser H, Redi H, Merritt TA, Spragg RG: Exposure of the hydrophobic components of porcine lung surfactant to oxidant stress alters surface tension properties. J Clin Invest 93: 2608-2615, 1994

    PubMed  Google Scholar 

  21. Mark L, Ingenito EP: Surfactant function and composition after free radical exposure generated by transition metals. Am J Physiol 276: L491-L500, 1999

    PubMed  Google Scholar 

  22. Haddad IY, Crow JP, Hu P, Yaozu Y, Beckman J, Matalon S: Concurrent generation of nitric oxide and superoxide damages surfactant protein A. Am J Physiol 267: L242-L249, 1994

    PubMed  Google Scholar 

  23. Holm BA, Enhorning G, Notter RH: A biophysical mechanism by which plasma proteins inhibit lung surfactant activity. Chem Phys Lipids 49: 49-55, 1988

    Article  PubMed  Google Scholar 

  24. Holm BA, Hudak BB, Keicher L, Cavanaugh C, Baker RR, Hu P, Matalon S: Mechanisms of H2O2-mediated injury to type II cell surfactant metabolism and protection with PEG-catalase. Am J Physiol 261: C751-C757, 1991

    PubMed  Google Scholar 

  25. Marzan Y, Mora R, Butler A, Butler M, Ingenito EP: Effects of simultaneous exposure of surfactant to serum proteins and free radicals. Exp Lung Res 28: 99-121, 2002

    Article  PubMed  Google Scholar 

  26. Seeger W, Lepper H, Hellmut WRD, Neuhof H: Alteration of alveolar surfactant function after exposure to oxidative stress and to oxygenated and native arachidonic acid in vitro. Biochim Biophys Acta 835: 58-67, 1985

    PubMed  Google Scholar 

  27. Yu SH, Possmayer F: Comparative studies on the biophysical activities of the low-molecular-weight hydrophobic proteins purified from bovine pulmonary surfactant. Lipids 18: 522-529, 1983

    PubMed  Google Scholar 

  28. Risberg B, Smith L, Örtenwall P: Oxygen radicals and lung injury. Acta Anaesthesiol Scand Suppl 95: 106-116; discussion 116–118, 1991

    PubMed  Google Scholar 

  29. Davies KJA, Goldberg A: Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes. J Biol Chem 262: 8220-8226, 1987

    PubMed  Google Scholar 

  30. Lee MM, Green FHY, Roth SH, Karkhanis A, Bjarnason SG, Schürch S: Sulfuric acid aerosol induces changes in alveolar surface tension in the guinea pig but not in the rat. Exp Lung Res 25: 229-244, 1999

    Article  PubMed  Google Scholar 

  31. Schoel WM, Goerke J, Schürch S: The captive bubble method for the evaluation of pulmonary surfactant: Surface tension, area and volume calculations. Biochim Biophys Acta 1200: 281-290, 1994

    PubMed  Google Scholar 

  32. Schürch S, Bachofen H, Goerke J, Possmayer F: A captive bubble method reproduces the in situ behavior of lung surfactant monolayers. J Appl Physiol 67: 2389-2396, 1989

    PubMed  Google Scholar 

  33. Schürch S, Possmayer F, Cheng S, Cockshutt AM: Pulmonary SP-A enhances adsorption and appears to induce surface sorting of lipid extract surfactant. Am J Physiol 263: L210-L218, 1992

    PubMed  Google Scholar 

  34. Rouser G, Fleischer S, Yamamoto A: Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis. Lipids 5: 494-496, 1970

    PubMed  Google Scholar 

  35. Vallyathan V, Leonard S, Kuppusamy P, Pack D, Chzhan M, Sanders SP, Zweier JL: Oxidative stress in silicosis: Evidence for the enhanced clearance of free radicals from whole lungs. Mol Cell Biochem 168: 125-132, 1997

    Article  PubMed  Google Scholar 

  36. Borg DC: Applications of electron spin resonance in biology. In: W.A. Pryor (ed). Free Radicals in Biology, vol. 1. Academic Press, New York, 1976, pp 69-147

    Google Scholar 

  37. Qanbar R, Cheng S, Possmayer F, Schürch S: Role of the palmitoylation of surfactant-associated protein C in surfactant film formation and stability. Am J Physiol 271: L572-L580, 1996

    PubMed  Google Scholar 

  38. Rice-Evans CA: Techniques in free radical chemistry. Elsevier, New York, 1991

    Google Scholar 

  39. Cifuentes J, Ruiz-Oronoz J, Myles C, Nieves B, Carlo W, Matalon S: Interaction of surfactant mixtures with reactive oxygen and nitrogen species. J Appl Physiol 78: 1800-1805, 1995

    PubMed  Google Scholar 

  40. Stults JT, Griffin PR, Lesikar DD, Naidu A, Moffat B, Benson BJ: Lung surfactant protein SP-C from human, bovine and canine sources contains palmityl cysteine thioester linkages. Am J Physiol 261: L118-L125, 1991

    PubMed  Google Scholar 

  41. Taneva S, Keough KMW: Pulmonary surfactant proteins SP-B and SP-C in spread monolayers at the air—water interface: III. Proteins SP-B plus SP-C with phospholipids in spread monolayers. Biophys J 66: 1158-1166, 1994

    PubMed  Google Scholar 

  42. Davis IC, Zhu S, Sampson JB, Crow JP, Matalon S: Inhibition of human surfactant protein A function by oxidation intermediates of nitrite. Free Radic Biol Med 33: 1703-1713, 2002

    Article  PubMed  Google Scholar 

  43. Matalon S, Holm BA, Baker RR, Whitfield MK, Freedman BA: Characterization of antioxidant activities of pulmonary surfactant mixtures. Biochim Biophys Acta 1035: 121-127, 1990

    PubMed  Google Scholar 

  44. Ghio AJ, Fracia PJ, Young SL, Piantadosi CA: Synthetic surfactant scavenges oxidants and protects against hyperoxic lung injury. J Appl Physiol 77: 1217-1223, 1994

    PubMed  Google Scholar 

  45. Bridges JP, Davis HW, Damodarasamy M, Kuroki Y, Howles G, Hui DY, McCormack FX: Pulmonary surfactant proteins A and D are potent endogenous inhibitors of lipid peroxidation and oxidative cellular injury. J Biol Chem 275: 38848-38855, 2000

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Laboratory Medicine, The Children's Hospital, Harvard Medical School, Boston, MA, USA

    M.M. Lee

  2. Respiratory Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada

    F.H.Y. Green, S. Schürch & S. Cheng

  3. Environmental Health Directorate, Health and Welfare Canada, Ottawa, Ontario, Canada

    S.G. Bjarnason (Environmental Health Directorate)

  4. Health Effects Laboratory Division, NIOSH, Morgantown, WV, USA

    S. Leonard & W. Wallace

  5. Department of Obstetrics and Gynecology, University of Western Ontario, London

    F. Possmayer

  6. MRC Group, Fetal and Neonatal Health and Development, Ontario, Canada

    F. Possmayer

  7. Health Effects Laboratory Division, NIOSH, Morgantown, WV, 26505, USA

    V. Vallyathan

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  2. F.H.Y. Green
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Lee, M., Green, F., Schürch, S. et al. Comparison of inhibitory effects of oxygen radicals and calf serum protein on surfactant activity. Mol Cell Biochem 259, 15–22 (2004). https://doi.org/10.1023/B:MCBI.0000021340.79014.a3

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  • DOI: https://doi.org/10.1023/B:MCBI.0000021340.79014.a3

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