The Respiratory Burst and the NADPH Oxidase of Phagocytic Leukocytes

  • Dirk Roos
  • René Lutter
  • Ben G. J. M. Bolscher


When phagocytic leukocytes are activated to kill microorganisms, these cells respond with considerable changes in their cellular metabolism and structure.1 Most marked is a 20- to 30-fold increase in the oxygen consumption (i.e., the respiratory burst) that is not sensitive to inhibitors of the mitochondrial respiration.2 The extra oxygen consumption reflects the action of a phagocyte-specific oxidase, responsible for the generation of reduced oxygen species.1 This enzyme is localized in the plasma membrane and—after phagocytosis—in the phagosomal membranes of the cell.3,4


NADPH Oxidase Oxidase Activity Human Neutrophil Respiratory Burst Chronic Granulomatous Disease 


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  1. 1.
    Klebanoff SJ, Clark RA: The Neutrophil: Function and Clinical Disorders. Amsterdam, Elsevier/North-Holland Biomedical, 1978.Google Scholar
  2. 2.
    Sbarra AJ, Karnovsky ML: The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J Biol Chem 234: 1355–1362, 1959.PubMedGoogle Scholar
  3. 3.
    Dewald B, Baggiolini M, Curnutte JT, et al: Subcellular localization of the superoxide-forming enzyme in human neutrophils. J Clin Invest 63: 21–29, 1979.PubMedGoogle Scholar
  4. 4.
    Briggs RT, Drath DB, Karnovsky ML, et al: Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J Cell Biol 67: 566–586, 1975.PubMedGoogle Scholar
  5. 5.
    Iyer GYN, Islam MF, Quastel JH: Biochemical aspects of phagocytosis. Nature (Lond) 192:535– 541, 1961.Google Scholar
  6. 6.
    Babior BM, Kipnes RS, Curnutte JT: Biological defense mechanisms: The production by leuko-cytes of superoxide, a potential bactericidal agent. J Clin Invest 52: 741–744, 1973.PubMedGoogle Scholar
  7. 7.
    Hamers MN, Roos D: Oxidative stress in human neutrophilic granulocytes: Host defence and self defence, in Sies H (ed): Oxidative Stress. London, Academic, 1985, p 351.Google Scholar
  8. 8.
    Britigan BE, Rosen GM, Chai Y, et al: Do human neutrophils make hydroxyl radical? J Biol Chem 261: 4426–4431, 1986.PubMedGoogle Scholar
  9. 9.
    Klebanoff SJ: Myeloperoxidase-halide-hydrogen peroxide anti-bacterial system. J Bacteriol 95: 2131–2138, 1968.PubMedGoogle Scholar
  10. 10.
    Cuperus RA, Muijsers AO, Wever R: The superoxide dismutase activity of myeloperoxidase; formation of Compound III. Biochim Biophys Acta 871: 78–84, 1986.PubMedGoogle Scholar
  11. 11.
    Tauber AI, Goetzl EJ: Structural and catalytic properties of the solubilized superoxide-generating activity of human polymorphonuclear leukocytes. Solubilization, stabilization in solution, and partial characterization. Biochemistry 18: 5576–5584, 1979.PubMedGoogle Scholar
  12. 12.
    Light DR, Walsh C, O’Callaghan AM, et al: Characteristics of the cofactor requirements for the superoxide-generating NADPH oxidase of human polymorphonuclear leukocytes. Biochemistry 20: 1468–1476, 1981.PubMedGoogle Scholar
  13. 13.
    Babior BM, Peters WA: The O2-producing enzyme of human neutrophils. Further properties. J Biol Chem 256: 2321–2323, 1981.PubMedGoogle Scholar
  14. 14.
    Tauber AI, Borregaard N, Simons E, et al: Chronic granulomatous disease: A syndrome of phagocyte deficiencies. Medicine (Baltimore) 62: 286–309, 1983.Google Scholar
  15. 15.
    Rossi F: The O2- forming NADPH oxidase of the phagocyte: Nature, mechanisms of activation and function. Biochim Biophys Acta 853: 65–89, 1986.PubMedGoogle Scholar
  16. 16.
    Test ST, Weiss SJ: Quantitative and temporal characterization of the extracellular H202 pool generated by human neutrophils. J Biol Chem 259: 399–405, 1984.PubMedGoogle Scholar
  17. 17.
    Ruch W, Cooper PH, Baggiolini M: Assay of H202 production by macrophages and neutrophils with homovanillic acid and horse radish peroxidase. J Immunol Methods 63: 347–357, 1983.PubMedGoogle Scholar
  18. 18.
    Roos D, Eckmann CM, Yazdanbakhsh M, et al: Excretion of superoxide by phagocytes measured with cytochromec entrapped in resealed erythrocyte ghosts. J Biol Chem 259: 1770–1775, 1984.PubMedGoogle Scholar
  19. 19.
    Makino R, Tanaka T, Iizuka T, et al: Stoichiometric conversion of oxygen to superoxide anion during the respiratory burst in neutrophils. J Biol Chem 261: 11444–11447, 1986.PubMedGoogle Scholar
  20. 20.
    Green TR, Wu DE: The NADPH: 02 oxidoreductase of human neutrophils. Stoichiometry of univalent and divalent reduction of 02. J Biol Chem 261: 6010–6015, 1986.PubMedGoogle Scholar
  21. 21.
    Bainton DF: Sequential degranulation of the two types of polymorphonuclear leukocyte granules during phagocytosis of microorganisms. J Cell Biol 58: 249–264, 1973.PubMedGoogle Scholar
  22. 22.
    Dewald B, Bretz U, Baggiolini M: Release of gelatinase from a novel secretory compartment of human neutrophils. J Clin Invest 70: 518–525, 1982.PubMedGoogle Scholar
  23. 23.
    Gallin JI: Neutrophil specific granules: A fuse that ignites the inflammatory response. Clin Res 32: 320–328, 1984.PubMedGoogle Scholar
  24. 24.
    Wright DG: The neutrophil as a secretory organ of the host defense, in Gallin JI, Fauci AS (eds): Advances in Host Defense Mechanisms. New York, Raven, 1982, vol 1: Phagocytic Cells, p 75.Google Scholar
  25. 25.
    Borregaard N, Heiple JN, Simons ER, et al: Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: Translocation during activation. J Cell Biol 97: 52–61, 1983.PubMedGoogle Scholar
  26. 26.
    Garcia RC, Segal AW: Changes in the subcellular distribution of the cytochrome b-245 on stimulation of human neutrophils. Biochem J 219: 233–242, 1984.PubMedGoogle Scholar
  27. 27.
    Lutter R, van Zwieten R, Weening R, et al: Cytochrome b, flavins, and ubiquinone-50 in enucleated human neutrophils (PMN cytoplasts). J Biol Chem 259: 9603–9606, 1984.PubMedGoogle Scholar
  28. 28.
    Ohno Y, Seligmann BE, Gallin JI: Cytochrome b translocation to human neutrophil plasma membranes and superoxide release. J Biol Chem 268: 2409–2414, 1985.Google Scholar
  29. 29.
    Parkos CA, Cochrane CG, Schmitt M, et al: Regulation of the oxidative response of human granulocytes to chemoattractants. J Biol Chem 260: 6541–6547, 1985.PubMedGoogle Scholar
  30. 30.
    Heyneman RA, Vercauteren RE: Activation of a NADPH oxidase from horse polymorphonuclear leukocytes in a cell-free system. J Leukocyte Biol 36: 751–759, 1984.PubMedGoogle Scholar
  31. 31.
    McPhail LC, Shirley PS, Clayton CC, et al: Activation of the respiratory burst enzyme from human neutrophils in a cell-free system. J Clin Invest 75: 1735–1739, 1985.PubMedGoogle Scholar
  32. 32.
    Curnutte JJ: Activation of human neutrophil nicotinamide adenine dinucleotide phosphate, reduced (triphosphopyridine nucleotide, reduced) oxidase by arachidonic acid in a cell-free system. J Clin Invest 75: 1740–1743, 1985.PubMedGoogle Scholar
  33. 33.
    Bromberg Y, Pick E: Activation of NADPH-dependent superoxide production in a cell-free system by sodium dodecyl sulphate. J Biol Chem 260: 13539–13545, 1985.PubMedGoogle Scholar
  34. 34.
    Babior BM, Kipnes RS: Superoxide-forming enzyme from human neutrophils: Evidence for a flavin requirement. Blood 50: 517–524, 1977.PubMedGoogle Scholar
  35. 35.
    Gabig TG: The NADPH-dependent O2- -generating oxidase from human neutrophils. Identification of a flavoprotein component that is deficient in a patient with chronic granulomatous disease. J Biol Chem 258: 6352–6356, 1983.PubMedGoogle Scholar
  36. 36.
    Gabig TG, Babior BM: The O2-forming oxidase responsible for the respiratory burst in human neutrophils. Properties of the solubilized enzyme. J Biol Chem 254: 9070–9074, 1979.PubMedGoogle Scholar
  37. 37.
    Gabig TG, Schervish EW, Santinga JT: Functional relationship of the cytochrome b to the superox- ide-generating oxidase of human neutrophils. J Biol Chem 257: 4114–4119, 1982.PubMedGoogle Scholar
  38. 38.
    Curnutte JT, Kipnes RS, Babior BM: Defect in pyridine nucleotide dependent superoxide production by a particulate fraction from the granulocytes of patients with chronic granulomatous disease. N Engl J Med 293: 628–632, 1975.PubMedGoogle Scholar
  39. 39.
    Green TR, Pratt KL: A reassessment of the product specificity of the NADPH: O2- oxidoreductase of human neutrophils. Biochem Biophys Res Commun 142: 213–220, 1987.PubMedGoogle Scholar
  40. 40.
    Misra HP, Fridovich I: The univalent reduction of oxygen by reduced flavins and quinones. J Biol Chem 247: 188–192, 1971.Google Scholar
  41. 41.
    Michelson AM: Chemical production of superoxide anions by reaction between riboflavin, oxygen and reduced nicotinamide adenine dinucleotide. Specificity of test for O2-, in Michelson AM, McCord JM, Fridovich I (eds): Superoxide and Superoxide Dismutase. London, Academic, 1977, p 87.Google Scholar
  42. 42.
    Tu SC, Romero FA, Wang LH: Uncoupling of the substrate monooxygenation and reduced pyridine nucleotide oxidation activities of salicylate hydroxylase by flavins. Arch Biochem Biophys 209: 423–432, 1981.PubMedGoogle Scholar
  43. 43.
    Kishore GM, Snell EE: Reactivity of an FAD-dependent oxygenase with free flavins: A new mode of uncoupling in flavoprotein oxygenases. Biochem Biophys Res Commun 87: 518–523, 1979.PubMedGoogle Scholar
  44. 44.
    Grover TA, Piette LH: Influence of flavin addition and removal on the formation of superoxide by NADPH-cytochrome P-450 reductase: A spin-trap study. Arch Biochem Biophys 212: 105–114, 1981.PubMedGoogle Scholar
  45. 45.
    Winterbourn CC: Cytochrome c reduction by semiquinone radicals can be indirectly inhibited by superoxide dismutase. Arch Biochem Biophys 209: 159–167, 1981.PubMedGoogle Scholar
  46. 46.
    Glass GA, DeLisle DM, DeTogni P, et al: The respiratory burst oxidase of human neutrophils. Further studies of the purified enzyme. J Biol Chem 261: 13247–13251, 1986.PubMedGoogle Scholar
  47. 47.
    Kakinuma K, Fukuhara Y, Kaneda M: The respiratory burst of neutrophils. Separation of an FAD enzyme and its characterization. J Biol Chem 262: 12316–12322, 1987.PubMedGoogle Scholar
  48. 48.
    Bellavite, P, Jones OTG, Cross AR, et al: Composition of partially purified NADPH oxidase from pig neutrophils. Biochem J 223: 639–648, 1984.PubMedGoogle Scholar
  49. 49.
    Berton G, Papini E, Cassatella MA, et al: Partial purification of the superoxidase-generating system of macrophages. Possible association of the NADPH oxidase activity with a low-potential (-247 mV) cytochrome b. Biochim Biophys Acta 810: 164–173, 1985.PubMedGoogle Scholar
  50. 50.
    Bellavite P, Cassatella MA, Papini E, et al: Presence of cytochrome b -245 in NADPH oxidase preparations from human neutrophils. FEBS Lett 199: 159–163, 1986.PubMedGoogle Scholar
  51. 51.
    Doussiere J, Vignais PV: Purification and properties of an -generating oxidase from bovine polymorphonuclear neutrophils. Biochemistry 24: 7231–7239, 1985.PubMedGoogle Scholar
  52. 52.
    Cross AR, Parkinson JF, Jones OTG: The superoxide-generating oxidase of leucocytes. NADPH- dependent reduction of flavin and cytochrome b in solubilized preparations. Biochem J 223:337– 344, 1984.PubMedGoogle Scholar
  53. 53.
    Gabig TG, Lefker BA: Activation of the human neutrophil NADPH oxidase results in coupling of electron carrier function between ubiquinone-10 and cytochrome b559. J Biol Chem 260:3991– 3995, 1985.Google Scholar
  54. 54.
    Weening RS, Corbeel L,, de Boer M et al: Cytochrome b deficiency in an autosomal form of chronic granulomatous disease. A third form of chronic granulomatous disease recognized by monocyte hybridization. J Clin Invest 75: 915–920, 1985.PubMedGoogle Scholar
  55. 55.
    Segal AW, Jones OTG: Novel cytochrome b system in phagocytic vacuoles of human granulocytes. Nature (Lond) 276: 515–517, 1978.Google Scholar
  56. 56.
    Segal AW, Jones OTG, Webster D, et al: Absence of a newly described cytochrome b from neutrophils of patients with chronic granulomatous disease. Lancet 2: 446–449, 1978.PubMedGoogle Scholar
  57. 57.
    Segal AW, Jones OTG: Reduction and subsequent oxidation of a cytochrome b of human neutrophils after stimulation with phorbol myristate acetate. Biochem Biophys Res Commun 88: 130–134, 1979.PubMedGoogle Scholar
  58. 58.
    Borregaard N, Johansen KS, Esmann V: Quantitation of superoxide production in human pol morphonuclear leukocytes from normals and three types of chronic granulomatous disease. Biochem Biophys Res Commun 90: 214–219, 1979.PubMedGoogle Scholar
  59. 59.
    Segal AW, Cross AR, Garcia RC, et al: Absence of cytochrome 6-245 in chronic granulomatous disease: A multicenter European evaluation of its incidence and relevance. N Engl J Med 308:245– 251, 1983.PubMedGoogle Scholar
  60. 60.
    Meerhof LJ, Roos D: Heterogeneity in chronic granulomatous disease detected with an improved nitroblue tetrazolium slide test. J Leukocyte Biol 39: 699–711, 1986.PubMedGoogle Scholar
  61. 61.
    Borregaard N, Cross AR, Herlin T, et al: A variant form of X-linked chronic granulomatous disease with normal nitroblue tetrazolium slide test and cytochrome 6. Eur J Clin Invest 13:243– 247, 1983.Google Scholar
  62. 62.
    Bohler M-C, Seger RA, Mouy R, et al: A study of 25 patients with chronic granulomatous disease: A new classification by correlating respiratory burst, cytochrome 6 and flavoprotein. J Clin Immunol 6: 136–145, 1986.PubMedGoogle Scholar
  63. 63.
    Iizuka T, Kanegasaki S, Makino R, et al: Pyridine and imidazole reversibly inhibit the respiratory burst in porcine and human neutrophils: Evidence for the involvement of cytochrome 6558 in the reaction. Biochem Biophys Res Commun 130: 621–626, 1985.PubMedGoogle Scholar
  64. 64.
    Cross AR, Parkinson JF, Jones OTG: Mechanism of the superoxide producing oxidase neutrophils. 02 is necessary for the fast reduction of cytochrome b-245 by NADPH. Biochem J 226: 881–884, 1985.PubMedGoogle Scholar
  65. 65.
    Parkos CA, Allen RA, Cochrane CG, et al: The quaternary structure of the plasma membrane b-type cytochrome of human granulocytes. Biochim Biophys Acta 932: 71–83, 1988.PubMedGoogle Scholar
  66. 66.
    Harper AM, Dunne MJ, Segal AW: Purification of cytochrome 6_245 from human neutrophils. Biochem J 219: 519–527, 1984.PubMedGoogle Scholar
  67. 67.
    Harper AM, Chaplin MF, Segal AW: Cytochrome 6-245 from human neutrophils is a glycoprotein. Biochem J 227: 783–788, 1985.PubMedGoogle Scholar
  68. 68.
    Segal AW: Absence of both cytochrome 6-245 subunits from neutrophils in X-linked chronic granulomatous disease. Nature (Lond) 326: 88–91, 1987.Google Scholar
  69. 69.
    Pember SO, Heyl BL, Kinkade JM, et al: Cytochrome 6558 from (bovine) granulocytes. Partial purification from Triton X-114 extracts and properties of the isolated cytochrome. J Biol Chem 259: 10590–10595, 1984.PubMedGoogle Scholar
  70. 70.
    Parkos CA, Allen RA, Cochrane CG, et al: Purified cytochrome b from human granulocyte plasma membrane is comprised of two polypeptides with relative molecular weights of 91,000 and 22,000. J Clin Invest 80: 732–742, 1987.PubMedGoogle Scholar
  71. 71.
    Lutter R, van Schaik MLJ, van Zwieten R, et al: Purification and partial characterization of the 6-type cytochrome from human polymorphonuclear leukocytes. J Biol Chem 260: 2237–2244, 1985.PubMedGoogle Scholar
  72. 72.
    Dinauer MC, Orkin SH, Brown R, et al: The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex. Nature 327: 717–720, 1987.PubMedGoogle Scholar
  73. 73.
    Royer-Pokora B, Kunkel LM, Monaco AP, et al: Cloning/ the gene for an inherited human disorder—chronic granulomatous disease—on the basis of its chromosomal localization. Nature (Lond) 322: 32–38, 1986.Google Scholar
  74. 74.
    Teahan C, Rowe P, Parker P, et al: The X-linked chronic granulomatous disease gene codes for the 0-chain of cytochrome 6-245. Nature 327: 720–721, 1987.PubMedGoogle Scholar
  75. 75.
    Shinagawa Y, Tanaka C, Teraoka A, et al: A new cytochrome in neutrophilic granules of rabbit leukocyte. J Biochem (Tokyo) 59: 622–624, 1966.Google Scholar
  76. 76.
    Cross AR, Jones OTG, Harper AM, et al: Oxidation-reduction properties of the cytochrome 6 found in the plasma membrane fraction of human neutrophils. A possible oxidase in the respiratory burst. Biochem J 194: 599–606, 1981.PubMedGoogle Scholar
  77. 77.
    Morel F, Vignais PV: Examination of the oxidase function of the 6-type cytochrome in human polymorphonuclear leucocytes. Biochim Biophys Acta 764: 213–225, 1984.PubMedGoogle Scholar
  78. 78.
    Cross AR, Higson FK, Jones OTG, et al: The enzymatic reduction and kinetics of oxidation of cytochrome 6-245 of neutrophils. Biochem J 204: 479–485, 1982.PubMedGoogle Scholar
  79. 79.
    Cooper MR, DeChatelet LR, McCall CE, et al: Complete deficiency of leukocyte glucose-6- phosphate dehydrogenase with defective bactericidal activity. J Clin Invest 51: 769–778, 1972.PubMedGoogle Scholar
  80. 80.
    Baehner RL, Johnston RB, Nathan DC: Comperative study of the metabolic and bactericidal characteristics of severly glucose-6-phosphate dehydrogenase-deficient polymorphonuclear leukocytes and leukocytes from children with chronic granulomatous disease. J Reticuloendothel Soc 12: 150–169, 1972.PubMedGoogle Scholar
  81. 81.
    Babior BM, Curnutte JT, Kipnes RS: Pyridine nucleotide-dependent superoxide production by a cell-free system from human granulocytes. J Clin Invest 56: 1035–1042, 1975.PubMedGoogle Scholar
  82. 82.
    Umei T, Takeshige K, Minakami S: NADPH binding component of neutrophil superoxide-generat- ing oxidase. J Biol Chem 261: 5229–5232, 1986.PubMedGoogle Scholar
  83. 83.
    Doussière J, Laporte F, Vignais PV: Photolabeling of a O2--generating protein in bovine polymorphonuclear neurophils by an arylazido NADP+ analog. Biochem Biophys Res Commun 139: 85–93, 1986.PubMedGoogle Scholar
  84. 84.
    Singer TP, Edmondson DE: Flavoproteins. Overview, in Fleischer S, Packer L (eds): Methods in Enzymology. New York, Academic, 1978, vol 53: Biomembranes. PartD. Biological Oxidations, Mitochondrial and Microbial Systems, p 397.Google Scholar
  85. 85.
    Walsh C: Scope of chemical redox transformations catalyzed by flavoenzymes, in Massey V, Williams CH (eds): Flavins and Flavoproteins. Amsterdam, Elsevier, 1982, p 121.Google Scholar
  86. 86.
    Cross AR, Jones OTG: The effect of the inhibitor diphenylene iodonium on the superoxide- generating system of neutrophils. Biochem J 237: 111–116, 1986.PubMedGoogle Scholar
  87. 87.
    Gabig TG, Lefker BA: Catalytic properties of the resolved flavoprotein and cytochrome b components of the NADPH dependent O2- generating oxidase from human neutrophils. Biochem Biophys Res Commun 118: 430–436, 1984.PubMedGoogle Scholar
  88. 88.
    Kakinuma K, Kaneda M, Chiba T, et al: Electron spin resonance studies on a flavoprotein in neutrophil plasma membranes. Redox potentials of the flavin and its participation in NADPH oxidase. J Biol Chem 261: 9426–9432, 1986.PubMedGoogle Scholar
  89. 89.
    Cross AR, Jones OTG, Garcia R, et al: The association of FAD with the cytochrome b-245 of human neutrophils. Biochem J 253: 759–763, 1982.Google Scholar
  90. 90.
    Gabig TG, Lefker BA: X-linked recessive and apparent autosomal recessive chronic gran-ulomatous disease: FAD and cytochrome b559 content of neutrophil oxidase fractions from patients and family members. Blood (suppl 1 ) 62: 80, 1983.Google Scholar
  91. 91.
    Borregaard N, Tauber AI: Subcellular localizations of the human neutrophil NADPH oxidase. Cytochrome and associated flavoprotein. J Biol Chem 259: 47–52, 1984.PubMedGoogle Scholar
  92. 92.
    Ohno Y, Buescher ES, Roberts R, et al: Réévaluation of cytochrome b and flavine adenine dinucleotide in neutrophils from patients with chronic granulomatous disease and description of a family with probable autosomal recessive inheritance of cytochrome b deficiency. Blood 67:1132– 1138, 1986.PubMedGoogle Scholar
  93. 93.
    Hamers MN,, de Boer M, Meerhof LJ et al: Complementation in monocyte hybrids revealing genetic heterogeneity in chronic granulomatous disease. Nature (Lond) 307: 553–555, 1984.Google Scholar
  94. 94.
    Roos D, Voetman AA, Meerhof LJ: Functional activity of enucleated human polymorphonuclear leukocytes. J Cell Biol 97: 368–377, 1983.PubMedGoogle Scholar
  95. 95.
    Segal AW, Heyworth PG, Cockcroft S, et al: Stimulated neutrophils from patients with autosomal recessive chronic granulomatous disease fail to phosphorylate a Mr 44,000 protein. Nature (Lond) 316: 547–549, 1985.Google Scholar
  96. 96.
    Hancock JT, Jones OTG: The inhibition by diphenyleneiodonium and its analogues of superoxide generation by macrophages. Biochem J 242: 103–107, 1987.PubMedGoogle Scholar
  97. 97.
    Millard JA, Gerard KW, Schneider DL: The isolation from rat peritoneal leukocytes of plasma membrane enriched in alkaline phosphatase and a b-type cytochrome. Biochem Biophys Res Commun 90: 312–319, 1979.PubMedGoogle Scholar
  98. 98.
    Crawford DR, Schneider DL: Identification of ubiquinone-50 in human neutrophils and its role in microbicidal events. J Biol Chem 257: 6662–6668, 1982.PubMedGoogle Scholar
  99. 99.
    Crawford DR, Schneider DL: Evidence that a quinone may be required for the production of superoxide and hydrogen peroxide in neutrophils. Biochem Biophys Res Commun 99: 1277–1286, 1981.PubMedGoogle Scholar
  100. 100.
    Cunningham CC, DeChatelet LR, Spach PI, et al: Identification and quantitation of electron- transport components in human polymorphonuclear neutrophils. Biochim Biophys Acta 682:430– 435, 1982.PubMedGoogle Scholar
  101. 101.
    Sloan EP, Crawford DR, Schneider DL: Isolation of plasma membrane from human neutrophils and determination of cytochrome b and quinone content. J Exp Med 153: 1316–1328, 1981.PubMedGoogle Scholar
  102. 102.
    Crawford DR, Schneider DL: Ubiquinone content and respiratory burst activity of latex-filled phagolysosomes isolated from human neutrophils and evidence for the probable involvement of a third granule. J Biol Chem 258: 5363–5367, 1983.PubMedGoogle Scholar
  103. 103.
    Hamers MN, Lutter R, van Zwieten R, et al: Characterization of the of H2O2- generating system in human neutrophils, in Bors W, Saran M, Tait D (eds): Oxygen Radicals in Chemistry and Biology. Berlin, Walter de Gruyter, 1984, p 843.Google Scholar
  104. 104.
    Cross AR, Jones OTG, Garcia R, et al: The subscellular localization of ubiquinone in human neutrophils. Biochem J 216: 765–768, 1983.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • Dirk Roos
    • 1
  • René Lutter
    • 1
  • Ben G. J. M. Bolscher
    • 1
  1. 1.Central Laboratory of the Netherlands Red Cross Blood Transfusion Service and Laboratory of Experimental and Clinical ImmunologyUniversity of AmsterdamAmsterdamThe Netherlands

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