Abstract
Effects of nitrogen dioxide (NO2) on pulmonary defense systems were investigated by determining phagocytosis and Superoxide anion (O −2 ) production by alveolar macrophages (AM) of rats. Rats were exposed to 8 ppm NO2 for 1 to 7 days and 4 ppm NO2 for 1 to 10 days, respectively. The phagocytic activity of AM was determined by taking yeast particles into the cells. The O −2 production by AM was determined at rest during phagocytosis of zymosan particles and stimulation with phorbol myristate acetate (PMA). The suppression of phagocytosis of AM was observed in cells from rats exposed to 8 ppm NO2 for 5 and 7 days. The suppression was also shown in AM from rats exposed to 4 ppm NO2 for 7 days. There were remarkable decreases in the O −2 production by AM from 8 ppm NO2-exposed rats at rest during zymosan phagocytosis and PMA stimulation on and after day 3. The O −2 production by AM from 4 ppm NO2-exposed rats at rest and during zymosan phagocytosis decreased on days 3, 5, and 10, but remained unchanged on day 7. The O −2 production by PMA-stimulated AM from 4 ppm NO2-exposed rats decreased on day 3. The results suggest that such diminution in phagocytosis and O −2 production by AM from NO2-exposed rats demonstrated the adverse effects on the pulmonary early defense systems and potentially causes bacterial infections.
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Acton JD, Myrvik QN (1966) Production of interferon by alveolar macrophage. J Bacteriol 91:2300–2304
— (1972) Nitrogen dioxide effects on alveolar macrophage. Arch Environ Health 24:48–52
Blair WH, Henry MC, Ehrlich R (1969) Chronic toxicity of nitrogen dioxide. II. Effect on histopathology of lung tissue. Arch Environ Health 18:186–192
Boxer LA, Ismail G, Allen JM, Baehner RL (1979) Oxidative metabolic responses of rabbit pulmonary alveolar macrophages. Blood 53:486–491
Chio KS, Tappel AL (1969) Inactivation of ribonuclease and other enzymes by peroxidizing lipids and by malonaldehyde. Biochemistry 8:2827–2832
Cross AR, Parkinson JF, Jones OTG (1984) The superoxide-generating oxidase of leucocytes. NADPH-dependent reduction of flavin and cytochrome b in solubilized preparations. Biochem J 223:337–344
— (1985) Mechanism of the superoxide-producing oxidase of neutrophils. O2 is necessary for the fast reduction of cytochrome b-245 by NADPH. Biochem J 226:881–884
Dowell AR, Kilburn KH, Pratt PC (1971) Short-term exposure to nitrogen dioxide. Effects on pulmonary ultrastructure, compliance, and the surfactant system. Arch Intern Med 128:74–80
Drath DB, Harper AA, Karnovsky ML (1976) Biochemical characteristics of alveolar macrophages. In: Bouhuys A (ed) Lung cells in disease, North-Holland Biomedical Press, Amsterdam, pp 153–161
Ehrlich R (1966) Effect of nitrogen dioxide on resistance to respiratory infection. Bacteriol Rev 30:604–614
Ehrlich R, Henry MC (1968) Chronic toxicity of nitrogen dioxide. I. Effect on resistance to bacterial pneumonia. Arch Environ Health 17:860–865
Evans MJ, Stephens RJ, Cabral LJ, Freeman G (1972) Cell renewal in the lungs of rats exposed to low levels of NO2. Arch Environ Health 24:180–189
Evans MJ, Freeman G (1980) Morphological and pathological effects of NO2 on the rat lung. In: Lee SD (ed) Nitrogen oxides and their effects on health, Ann Arbor Science, Ann Arbor, Michigan, pp 243–265
Freeman G, Grane SC, Stephens RJ, Furiosi NJ (1968) Pathogenesis of the nitrogen dioxide-induced lesion in the rat lung. A review and presentation of new observations. Amer Rev Respir Dis 98:429–443
— (1969) The subacute nitrogen dioxide-induced lesion of the rat lung. Arch Environ Health 18:609–612
Gabig TG, Lefker BA (1984) Catalytic properties of the resolved flavoprotein and cytochrome B components of the NADPH dependent O −2 generating oxidase from human neutrophils. Biochem Biophys Res Comm 118:430–436
Gardner DE, Holzman RS, Coffin DL (1969) Effects of nitrogen dioxide on pulmonary cell population. J Bacteriol 98:1041–1043
Gardner DE, Loosli CG, Hanes B, Blackmore W, Teebken D (1970) Pulmonary changes in 7,000 mice following prolonged exposure to ambient and filtered Los Angeles air. Arch Environ Health 20:310–317
Gee JBL, Vassallo CL, Kaskin J, Basford RE, Field JB (1970) Catalase-dependent peroxidative metabolism in the alveolar macrophage during phagocytosis. J Clin Invest 49:1280–1287
Gee JBL, Khandwala AS (1976) Oxygen metabolism in the alveolar macrophage: Friend and foe? J Reticuloendothel Soc 19:229–236
Giordano AM, Morrow PE (1972) Chronic low-level nitrogen dioxide exposure and mucociliary clearance. Arch Environ Health 25:443–449
Goldstein E, Hoeprich PD (1973) Effect of nitrogen dioxide on pulmonary bacterial defense mechanisms. Arch Environ Health 26:202–204
Goldstein E, Warshauer D, Lippert W, Tarkington B (1974) Ozone and nitrogen dioxide exposure. Murine pulmonary defense mechanisms. Arch Environ Health 28:85–90
Green GM, Kass EH (1964) The role of the alveolar macrophage in the clearance of bacteria from the lung. J Exp Med 119:167–175
Green GM, Goldstein E (1966) A method for quantitating intra-pulmonary bacterial inactivation in individual animals. J Lab Clin Med 68:669–677
Green RC, Little C, O'Brien J (1971) The inactivation of isocitrate dehydrogenase by lipid peroxide. Arch Biochem Biophys 142:598–605
Henry MC, Findlay J, Spangler J, Ehrilich, R (1970) Chronic toxicity of NO2 in Squirrel monkeys. III. Effect on resistance to bacterial and viral infection. Arch Environ Health 20:566–570
Hirai K, Ueno S, Ogawa K (1980) Plasma membrane-associated NADPH oxidase and superoxide dismutase in pulmonary alveolar macrophages. Saishin Igaku 35:718–723
Isaacs A, Lindenmann J (1957) Virus interference. I. The interferon. Proc R Soc 147:258–267
Johnston RD Jr., Godzik CA, Cohn ZA (1978) Increased superoxide anion production by immunologically activated and chemically elicited macrophages. J Exp Med 148:115–127
Kass EH, Green GM, Goldstein E (1966) Mechanisms of anti-bacterial action in the respiratory system. Bacteriol Rev 30:488–497
Katoh O (1980) An ultrastructural study on pathologic alterations and early response to infection due to Klebsiella pneumoniae in the lungs of mice exposed to nitrogen dioxide. Japanese J Thoracic Diseases 18:435–446
Khandwala A, Gee JBL (1973) Linoleic acid hydroperoxide: Impaired bacterial uptake by alveolar macrophages, a mechanism of oxidant lung injury. Science 182:1363–1365
Knowles DM, II, Hoffman T, Ferrarini M, Kunkel HG (1978) The demonstration of acid α-naphthyl acetate esterase activity in human lymphocytes: Usefulness as a T-cell marker. Cell Immunol 35:112–123
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
McCord JM, Day ED (1978) Superoxide-dependent production of hydroxyl radical catalyzed by iron-EDTA complex. FEBS Lett 86:139–142
Nakamura M, Minakami S (1984) Superoxide generation in macrophages: Enzymatic basis and function. Japanese J Inflammation 4:381–382
Oyanagui Y (1984) Establishment of nitrite-kit for SOD activity determination. Japanese J Inflammation 4:63–73
Pearlman ME, Finklea JF, Creason JP, Shy CM, Young MM, Horton RJM (1971) Nitrogen dioxide and lower respiratory illness. Pediatrics 47:391–398
Raylander R (1968) Pulmonary defence mechanisms to airborne bacteria. Acta Physiol Scand (Suppl.) 306:1–89
Roehm JN, Hadley JG, Menzel DB (1971) Antioxidants vs lung disease. Arch Intern Med 128:88–93
Romeo D, Zabucchi G, Marzi T, Rossi F (1973) Kinetic and enzymatic features of metabolic stimulation of alveolar and peritoneal macrophages challenged with bacteria. Exp Cell Res 78:423–432
Sherwin RP, Richters V, Brooks M, Buckley RD (1968) The phenomenon of macrophage congregationin vitro and its relationship toin vivo NO2 exposure of guinea pigs. Lab Invest 18:269–277
Shy CM, Creason JP, Pearlman ME, McClain KE, Benson FB, Young MM (1970) The Chattanooga school children study: Effects of community exposure to nitrogen dioxide. II. Incidence of acute respiratory illness, J Air Pollut Control Assoc 20:582–588
Suzuki T, Terada N, Ikeda S, Ohsawa M, Endo K, Mizoguchi I (1984) Effect of NO2 exposure on the activity of angiotensin converting enzyme in lung. Ann Rep Tokyo Metr Res Lab PH 35:279–288
Taketa K, Watanabe A (1971) Interconvertible rnicroheterogeneity of glucose-6-phosphate dehydrogenase in rat liver. Biochim Biophys Acta 235:19–26
Thomas HV, Mueler PK, Lyman RL (1968) Lipoperoxidation of lung lipids in rats exposed to nitrogen dioxide. Science 159:532–534
Tsan MF (1977) Stimulation of the hexose monophosphate shunt independent of hydrogen peroxide and Superoxide production in rabbit alveolar macrophages during phagocytosis. Blood 50:935–945
Valand SB, Acton JD, Myrvik QN (1970) Nitrogen dioxide inhalation of viral-induced resistance in alveolar monocytes. Arch Environ Health 20:303–309
Wills ED (1961) Effect of unsaturated fatty acids and their per-oxides on enzymes. Biochem Pharmacol 7:7–16
Yam LT, Li CY, Crosby WH (1971) Cytochemical identification of monocytes and granulocytes. Amer J Clin Pathol 55:283–290
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Suzuki, T., Ikeda, S., Kanoh, T. et al. Decreased phagocytosis and superoxide anion production in alveolar macrophages of rats exposed to nitrogen dioxide. Arch. Environ. Contam. Toxicol. 15, 733–739 (1986). https://doi.org/10.1007/BF01054920
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DOI: https://doi.org/10.1007/BF01054920