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Carbon Monoxide Contributes to the Cytokine-Induced Inhibition of Surfactant Synthesis by Human Type II Pneumocytes

Carbon Monoxide Contributes to the Cytokine-Induced Inhibition of Surfactant Synthesis by Human... Abstract Background: An increase in cyclic guanosine 3',5'-monophosphate (cGMP) due to nitric oxide generation is known to participate in the mediation of the tumor necrosis factor α (TNF-α) effect in type II cells. Because guanylyl cyclase can be activated also by carbon monoxide (CO), in this study we examined the ability of human type II pneumocytes to produce CO in the presence of cytokines and the relative contribution of this molecule to the TNF-α and interleukin 1 effects. Design: Type II pneumocytes were isolated from cadaveric multiple-organ donors by enzymatic digestion, adherence separation of macrophages, and gradient purification. After preculture for 24 hours, cells were cultured for 24 hours in the presence or absence of TNF-α, interleukin 1, sodium nitroprusside, Nωnitro-l-arginine, CO, hemin, zinc-protoporphyrin type IX, deferoxamine mesylate, S-adenosyl-l-methionine, α-tocopherol, methylene blue (a guanylyl cyclase inhibitor), 8-bromine-cGMP, and combinations of these reagents. Both CO (picomole per microgram of protein) and nitric oxide release to the medium and the cGMP (picomole per microgram of protein) content of the cells were measured. In a different set of experiments, d-glucose labeled with radioactive carbon (14C) was added to the medium, and the labeling of several lipid fractions was determined (picomole per microgram of protein). Results: d-[14C]glucose incorporation into phosphatidylcholine, the main surfactant component, was selectively inhibited in the presence of cytokines, CO, sodium nitroprusside, or 8-bromine-cGMP. The inhibitory effect of TNF-α was partially reversed by Nω-nitro-l-arginine, deferoxamine, or α-tocopherol and totally reversed by methylene blue. Tumor necrosis factor α induced an increase in cGMP cell content and in the CO and nitric oxide release to the medium. Hemin increased CO and cGMP production and decreased phosphatidylcholine synthesis. Zinc-protoporphyrin type IX, an inhibitor of heme oxygenase, and all 3 antioxidants, which inhibited CO production, also antagonized the TNF-α effect on cGMP and phosphatidylcholine synthesis. Conclusions: Intracellular cGMP increase due to an endogenous generation of both CO and nitric oxide mediates the cytokine-induced inhibition of surfactant synthesis by type II pneumocytes. Both lipid peroxidation and heme oxygenase activity are sources for the observed CO production.Arch Surg. 1997;132:1352-1361 References 1. Roberts DJ, Dacies JM, Evans CC, Bell M, Mostafa SM. Tumour necrosis factor in inflammation and adult respiratory distress syndrome . Lancet . 1989;28:1043-1044.Crossref 2. Nash JRP, McLaughlin J, Hoyle C, Roberts D. Immunolocalization of tumour necrosis factor alpha in lung tissue from patients dying with adult respiratory distress syndrome . Histopathology . 1991;19:395-402.Crossref 3. Balibrea JL, Arias-Diaz J, Garcia C, et al. Effect of pentoxifylline on the inhibition of surfactant synthesis induced by TNF-α in human type II pneumocytes . Am J Respir Crit Care Med . 1994;149:699-706.Crossref 4. Arias-Diaz J, Vara E, Garcia C, Balibrea JL. Tumor necrosis factor-α–induced inhibition of phosphatidylcholine synthesis by human type II pneumocytes is partially mediated by prostaglandins . J Clin Invest . 1994;94:244-250.Crossref 5. Vara E, Arias-Diaz J, Garcia C, Hernández J, Balibrea JL. Both prostaglandin E2 and nitric oxide sequentially mediate the tumor necrosis factor α–induced inhibition of surfactant synthesis by human type II pneumocytes . Arch Surg . 1995; 130:1279-1286.Crossref 6. Furchgott RF, Jothianandan D. Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light . Blood Vess . 1991;28:52-61. 7. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase . Mol Pharmacol . 1987;32:497-504. 8. Coburn RF, Blakemore WS, Foster RE. Endogenous carbon monoxide production in man . J Clin Invest . 1963;42:1172-1178.Crossref 9. Omura T, Sato R. The carbon monoxide-binding pigment of liver microsomes, I: evidence for its hemoprotein nature . J Biol Chem . 1964;239:2370-2385. 10. Stephen H, Stephen T. Solubilities of Organic and Inorganic Compounds . New York, NY: Macmillan Publishing Co Inc; 1963. 11. Bates JN, Baker MT, Guerra R Jr, Harrison DG. Nitric oxide generation from nitroprusside by vascular tissue: evidence that reduction of the nitroprusside anion and cyanide loss are required . Biochem Pharmacol . 1991;42( (suppl) ):S157-S165.Crossref 12. Wolff DG, Bidlack WR. The formation of carbon monoxide during peroxidation of microsomal lipids . Biochem Biophys Res Commun . 1976;73:850-857.Crossref 13. Rodkey FL, Hill TA, Pitts LL, Robertson RF. Spectrophotometric measurement of carboxyhemoglobin and methemoglobin in blood . Clin Chem . 1979:25:1388-1393. 14. Owens CWI, Belcher RV. A colorimetric micro-method for the determination of glutathione . Biochem J . 1965;94:705-711. 15. Vara E, Tamarit-Rodríguez J. Norepinephrine inhibits islet lipid metabolism, 45Ca2+ uptake, and insulin secretion . Am J Physiol . 1989:257( (6 pt 1) ):E923-E929. 16. Tracey KJ, Lowry SF, Fahey TJ, Fong Y, Hesse D. Cachectin/tumour necrosis factor induces lethal septic shock and stress hormone responses in the dog . Surg Gynecol Obstet . 1987;164:415-422. 17. Tracey KJ, Lowry SF, Cerami A. Cachectin/TNFα in septic shock and septic adult respiratory distress syndrome . Am Rev Respir Dis . 1988;138:1377-1379.Crossref 18. Gregory TJ, Longmore WJ, Moxley MA, et al. Surfactant chemical composition and biophysical activity in acute respiratory distress syndrome . J Clin Invest . 1991; 88:1976-1981.Crossref 19. Rooney SA. Young SL, Mendelson CR. Molecular and cellular processing of lung surfactant . FASEB J . 1994;9:957-967. 20. Brüne B, Schmidt KM, Ullrich V. Activation of soluble guanylate cyclase by carbon monoxide and inhibition by superoxide anion . Eur J Biochem . 1990:192: 683-688.Crossref 21. Utz J, Ullrich V. Carbon monoxide relaxes ileal smooth muscle through activation of guanylate cyclase . Biochem Pharmacol . 1991;41:1195-1201.Crossref 22. Arias-Díaz J, Vara E, Garcia C, Villa N, Balibrea JL. Evidence for a cyclic guanosine monophosphate-dependent, carbon monoxide-mediated, signaling system in the regulation of TNF-α production by human pulmonary macrophages . Arch Surg . 1995;130:1287-1293.Crossref 23. Coburn RF, Williams WJ, White P. Kahn SB. The production of carbon monoxide from hemoglobin in vivo . J Clin Invest . 1967;46:346-356.Crossref 24. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions: evidence for the involvement of mitochondrial radical generation . J Biol Chem . 1992;267:5317-5323. 25. Lautier D, Luscher P, Tyrrell RM. Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene . Carcinogenesis . 1992;13:227-232.Crossref 26. Cantoni L, Rossi C, Rizzardini M, Gadina M, Ghezzi P. Interleukin-1 and tumour necrosis factor induce hepatic haem oxygenase . Biochem J . 1991;279( (pt 3) ): 891-894. 27. Maines MD. Zinc protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat . Biochim Biophys Acta . 1981;673:303-309.Crossref 28. Koesling D, Böme E, Schultz G. Guanylyl cyclases, a growing family of signal-transducing enzymes . FASEB J . 1991;5:2785-2791. 29. Steinhorn RH, Morin FC III, Russell JA. The adventitia may be a barrier specific to nitric oxide in rabbit pulmonary artery . J Clin Invest . 1994;94:1883-1888.Crossref 30. Huie RE, Padmaja S. The reaction of nitric oxide with superoxide . Free Radic Res Commun . 1993;18:195-199.Crossref 31. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger . Science . 1993;259:381-384.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Surgery American Medical Association

Carbon Monoxide Contributes to the Cytokine-Induced Inhibition of Surfactant Synthesis by Human Type II Pneumocytes

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References (33)

Publisher
American Medical Association
Copyright
Copyright © 1997 American Medical Association. All Rights Reserved.
ISSN
0004-0010
eISSN
1538-3644
DOI
10.1001/archsurg.1997.01430360098018
Publisher site
See Article on Publisher Site

Abstract

Abstract Background: An increase in cyclic guanosine 3',5'-monophosphate (cGMP) due to nitric oxide generation is known to participate in the mediation of the tumor necrosis factor α (TNF-α) effect in type II cells. Because guanylyl cyclase can be activated also by carbon monoxide (CO), in this study we examined the ability of human type II pneumocytes to produce CO in the presence of cytokines and the relative contribution of this molecule to the TNF-α and interleukin 1 effects. Design: Type II pneumocytes were isolated from cadaveric multiple-organ donors by enzymatic digestion, adherence separation of macrophages, and gradient purification. After preculture for 24 hours, cells were cultured for 24 hours in the presence or absence of TNF-α, interleukin 1, sodium nitroprusside, Nωnitro-l-arginine, CO, hemin, zinc-protoporphyrin type IX, deferoxamine mesylate, S-adenosyl-l-methionine, α-tocopherol, methylene blue (a guanylyl cyclase inhibitor), 8-bromine-cGMP, and combinations of these reagents. Both CO (picomole per microgram of protein) and nitric oxide release to the medium and the cGMP (picomole per microgram of protein) content of the cells were measured. In a different set of experiments, d-glucose labeled with radioactive carbon (14C) was added to the medium, and the labeling of several lipid fractions was determined (picomole per microgram of protein). Results: d-[14C]glucose incorporation into phosphatidylcholine, the main surfactant component, was selectively inhibited in the presence of cytokines, CO, sodium nitroprusside, or 8-bromine-cGMP. The inhibitory effect of TNF-α was partially reversed by Nω-nitro-l-arginine, deferoxamine, or α-tocopherol and totally reversed by methylene blue. Tumor necrosis factor α induced an increase in cGMP cell content and in the CO and nitric oxide release to the medium. Hemin increased CO and cGMP production and decreased phosphatidylcholine synthesis. Zinc-protoporphyrin type IX, an inhibitor of heme oxygenase, and all 3 antioxidants, which inhibited CO production, also antagonized the TNF-α effect on cGMP and phosphatidylcholine synthesis. Conclusions: Intracellular cGMP increase due to an endogenous generation of both CO and nitric oxide mediates the cytokine-induced inhibition of surfactant synthesis by type II pneumocytes. Both lipid peroxidation and heme oxygenase activity are sources for the observed CO production.Arch Surg. 1997;132:1352-1361 References 1. Roberts DJ, Dacies JM, Evans CC, Bell M, Mostafa SM. Tumour necrosis factor in inflammation and adult respiratory distress syndrome . Lancet . 1989;28:1043-1044.Crossref 2. Nash JRP, McLaughlin J, Hoyle C, Roberts D. Immunolocalization of tumour necrosis factor alpha in lung tissue from patients dying with adult respiratory distress syndrome . Histopathology . 1991;19:395-402.Crossref 3. Balibrea JL, Arias-Diaz J, Garcia C, et al. Effect of pentoxifylline on the inhibition of surfactant synthesis induced by TNF-α in human type II pneumocytes . Am J Respir Crit Care Med . 1994;149:699-706.Crossref 4. Arias-Diaz J, Vara E, Garcia C, Balibrea JL. Tumor necrosis factor-α–induced inhibition of phosphatidylcholine synthesis by human type II pneumocytes is partially mediated by prostaglandins . J Clin Invest . 1994;94:244-250.Crossref 5. Vara E, Arias-Diaz J, Garcia C, Hernández J, Balibrea JL. Both prostaglandin E2 and nitric oxide sequentially mediate the tumor necrosis factor α–induced inhibition of surfactant synthesis by human type II pneumocytes . Arch Surg . 1995; 130:1279-1286.Crossref 6. Furchgott RF, Jothianandan D. Endothelium-dependent and -independent vasodilation involving cyclic GMP: relaxation induced by nitric oxide, carbon monoxide and light . Blood Vess . 1991;28:52-61. 7. Brune B, Ullrich V. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase . Mol Pharmacol . 1987;32:497-504. 8. Coburn RF, Blakemore WS, Foster RE. Endogenous carbon monoxide production in man . J Clin Invest . 1963;42:1172-1178.Crossref 9. Omura T, Sato R. The carbon monoxide-binding pigment of liver microsomes, I: evidence for its hemoprotein nature . J Biol Chem . 1964;239:2370-2385. 10. Stephen H, Stephen T. Solubilities of Organic and Inorganic Compounds . New York, NY: Macmillan Publishing Co Inc; 1963. 11. Bates JN, Baker MT, Guerra R Jr, Harrison DG. Nitric oxide generation from nitroprusside by vascular tissue: evidence that reduction of the nitroprusside anion and cyanide loss are required . Biochem Pharmacol . 1991;42( (suppl) ):S157-S165.Crossref 12. Wolff DG, Bidlack WR. The formation of carbon monoxide during peroxidation of microsomal lipids . Biochem Biophys Res Commun . 1976;73:850-857.Crossref 13. Rodkey FL, Hill TA, Pitts LL, Robertson RF. Spectrophotometric measurement of carboxyhemoglobin and methemoglobin in blood . Clin Chem . 1979:25:1388-1393. 14. Owens CWI, Belcher RV. A colorimetric micro-method for the determination of glutathione . Biochem J . 1965;94:705-711. 15. Vara E, Tamarit-Rodríguez J. Norepinephrine inhibits islet lipid metabolism, 45Ca2+ uptake, and insulin secretion . Am J Physiol . 1989:257( (6 pt 1) ):E923-E929. 16. Tracey KJ, Lowry SF, Fahey TJ, Fong Y, Hesse D. Cachectin/tumour necrosis factor induces lethal septic shock and stress hormone responses in the dog . Surg Gynecol Obstet . 1987;164:415-422. 17. Tracey KJ, Lowry SF, Cerami A. Cachectin/TNFα in septic shock and septic adult respiratory distress syndrome . Am Rev Respir Dis . 1988;138:1377-1379.Crossref 18. Gregory TJ, Longmore WJ, Moxley MA, et al. Surfactant chemical composition and biophysical activity in acute respiratory distress syndrome . J Clin Invest . 1991; 88:1976-1981.Crossref 19. Rooney SA. Young SL, Mendelson CR. Molecular and cellular processing of lung surfactant . FASEB J . 1994;9:957-967. 20. Brüne B, Schmidt KM, Ullrich V. Activation of soluble guanylate cyclase by carbon monoxide and inhibition by superoxide anion . Eur J Biochem . 1990:192: 683-688.Crossref 21. Utz J, Ullrich V. Carbon monoxide relaxes ileal smooth muscle through activation of guanylate cyclase . Biochem Pharmacol . 1991;41:1195-1201.Crossref 22. Arias-Díaz J, Vara E, Garcia C, Villa N, Balibrea JL. Evidence for a cyclic guanosine monophosphate-dependent, carbon monoxide-mediated, signaling system in the regulation of TNF-α production by human pulmonary macrophages . Arch Surg . 1995;130:1287-1293.Crossref 23. Coburn RF, Williams WJ, White P. Kahn SB. The production of carbon monoxide from hemoglobin in vivo . J Clin Invest . 1967;46:346-356.Crossref 24. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W. Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions: evidence for the involvement of mitochondrial radical generation . J Biol Chem . 1992;267:5317-5323. 25. Lautier D, Luscher P, Tyrrell RM. Endogenous glutathione levels modulate both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene . Carcinogenesis . 1992;13:227-232.Crossref 26. Cantoni L, Rossi C, Rizzardini M, Gadina M, Ghezzi P. Interleukin-1 and tumour necrosis factor induce hepatic haem oxygenase . Biochem J . 1991;279( (pt 3) ): 891-894. 27. Maines MD. Zinc protoporphyrin is a selective inhibitor of heme oxygenase activity in the neonatal rat . Biochim Biophys Acta . 1981;673:303-309.Crossref 28. Koesling D, Böme E, Schultz G. Guanylyl cyclases, a growing family of signal-transducing enzymes . FASEB J . 1991;5:2785-2791. 29. Steinhorn RH, Morin FC III, Russell JA. The adventitia may be a barrier specific to nitric oxide in rabbit pulmonary artery . J Clin Invest . 1994;94:1883-1888.Crossref 30. Huie RE, Padmaja S. The reaction of nitric oxide with superoxide . Free Radic Res Commun . 1993;18:195-199.Crossref 31. Verma A, Hirsch DJ, Glatt CE, Ronnett GV, Snyder SH. Carbon monoxide: a putative neural messenger . Science . 1993;259:381-384.Crossref

Journal

Archives of SurgeryAmerican Medical Association

Published: Dec 1, 1997

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