Abstract
When exposed to certain stimuli, phagocytic cells (neutrophils and mononuclear phagocytes) undergo marked changes in the way they handle oxygen.1 Their rates of oxygen uptake increase greatly, they begin to produce large amounts of superoxide (O −2 ) and hydrogen peroxide (H2O2), and they begin to metabolize large quantities of glucose by way of the hexose monophosphate shunt. Because of the sharp increase in oxygen uptake, this series of changes has come to be known as the respiratory burst. Its purpose is to generate powerful microbicidal agents by the partial reduction of oxygen.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Babior BM, Crowley CA: Chronic granulomatous disease and other disorders of oxidative killing by phagocytes, in Stanburg JB, Wyngaarden JB, Fredrickson DS, et al (eds): Metabolic Basis of Inherited Diseases. New York, McGraw-Hill, 1983, pp 1956–1985.
Berk SL, Smith JK: Infectious diseases in the elderly. Med Clin North Am 67: 273–293, 1983.
Nagel JE, Pyle RS, Chrest FJ, et al: Oxidative metabolism and bactericidal capacity of poly-morphonuclear leukocytes from normal young and aged adults. J Gerontol 37: 529–534, 1982.
Corberand J, Ngyen F, Laharrague P, et al: Polymorphonuclear functions and aging in humans. J Am Geriatr Soc 29: 391–397, 1981.
Romeo D, Jug M, Zabucchi G, et al: Perturbation of leukocyte metabolism by non phagocytosable concanavalin A coupled beads. FEBS Lett 42: 90–95, 1974.
Johnston RB, Lehmeyer JE, Guthrie LA: Generation of superoxide anion and chemiluminescence by human monocytes during phagocytosis and on contact with surface-bound immunoglobulin G. J Exp Med 143: 1551–1563, 1976.
Baxter MA, Leslie RGQ, Reeves WG: The stimulation of superoxide anion production in guinea pig peritoneal macrophages and neutrophils by phorbol myristate acetate, opsonized zymosan and IgG2 containing soluble immune complexes. Immunology 48: 657–658, 1983.
Yagawa K, Kaku M, Ichinose Y, et al: Fc receptor mediated desensitization of superoxide (02~) generation response of guinea pig macrophages and polymorphonuclear leucocytes. Immunology 55: 629–638, 1985.
McPhail LC, Snyderman R: Activation of the respiratory burst enzyme in human poly-morphonuclear leukocytes by chemoattractants and other soluble stimuli. Evidence that the same oxidase is activated by different transductional mechanisms. J Clin Invest 72: 192–200, 1983.
Cohen HJ, Chovaniec ME: Superoxide generation by digitonin-stimulated guinea pig granulocytes: A basis for continuous assay monitoring superoxide production and for the study of the activation of the generating system. J Clin Invest 61: 1088–1096, 1978.
Bender JG, McPhail LC, Van Epps DE: Exposure of human neutrophils to chemotactic factors potentiates activation of the respiratory burst enzyme. J Immunol 130: 2316–2323, 1983.
Pick E, Keisari Y: Superoxide anion and hydrogen peroxide production by chemically elicited peritoneal macrophages. Induction by multiple nonphagocytic stimuli. Cell Immunol 59: 301–318, 1981.
Palmblad J, Gyllenhammar H, Lindgren JA, et al: Effects of leukotrienes and f-Met-Leu–Phe on oxidative metabolism of neutrophils and eosinophils. J Immunol 132: 3041–3045, 1984.
Bromberg Y, Pick E: Unsaturated fatty acids as second messengers of superoxide generation by macrophages. Cell Immunol 79: 240–252, 1983.
Clark RA: Extracellular effects of myeloperoxidase-hydrogen peroxide-halide system, in Weissmann G (ed): Advances in Inflammation Research. New York, Raven, 1983, vol 5, p 107.
Cerutti PA: Prooxidant states and tumor promotion. Science 227: 375–381, 1985.
Harman D: Aging: A theory based on free radical and radiation chemistry. J Gerontol 11: 298–299, 1956.
Harman D, Heidrick ML, Eddy DE: Free radical theory of aging. Effect of free-radical-reaction inhibitors on the immune response. J Am Geriatr Soc 25: 400–407, 1977.
Harman D: Free radical theory of aging: Nutritional implications. Age 1: 143–150, 1978.
McPhail LC, Clayton CC, Snyderman R: The NADPH oxidase of human polymorphonuclear leukocytes. J Biol Chem 259: 5768–5775, 1984.
Babior BM: The respiratory burst of phagocytes. J Clin Invest 73: 599–601, 1984.
Tsunawaki S, Nathan CF: Enzymatic basis of macrophage activation. J Biol Chem 259:4305– 4312, 1984.
Baker SS, Cohen HJ: Altered oxidative metabolism in selenium deficient rat granulocytes. J Immunol 130: 2856–2860, 1983.
Karnofsky JR, Wright J, Miles-Richardson GE: Biochemical requirements for singlet oxygen production by purified human myeloperoxidase. J Clin Invest 74: 1489–1495, 1984.
Ito M, Karmali R, Krim M: Effect of interferon on chemiluminescence and hydroxyl radical production in murine macrophages stimulated by PMA. Immunology 56: 533–541, 1985.
Makinodan T, Kay MMB: Age influences on the immune system, in Kungel E, Dixon BC (eds): Advances of Immunology. New York, Academic, 1980, p 287.
Weksler ME: Senescence of the immune system. Med Clin North Am 67: 263–272, 1983.
Leibovitz BE, Siegel BV: Aspects of free radical reactions in biological systems: aging. J Gerontol 35: 45–56, 1980.
Nathan CF, Arrich BA, Murray MW et al: Tumor cell anti oxidant defenses. Inhibition of the glutathione redox cycle enhances macrophage mediated cytolysis. J Exp Med 153: 766–779, 1981.
Halliwell B: Superoxide dismutase, catalase and glutathione peroxidase: Solutions to the problems of living with 02. New Phytol 73: 1057–1068, 1974.
Piper PJ (ed): SRS-A and Leukotrienes. New York, Wiley, 1981.
Tappel AL: Lipid peroxidation damage to cell components. Fed Proc 32: 1870–1875, 1973.
Nohl H, Megner D: Do mitochondria produce oxygen radicals in vivo? Eur J Biochem 82:563– 567, 1978.
Sutherland RM, Rothstein A, Weed RI: Erythrocyte membrane sulfhydryl groups and cation permeability. J Cell Physiol 69: 185–196, 1967.
Goldman JM, Hadley ME: Sulfhydryl requirement for a-adrenergic receptor activity and MSH action in melanophores. J Pharm Exp Ther 182: 93–105, 1972.
East EJ, Chang RCC, Yu NT, et al: Human spectroscopic measurement of total sulfydryl in intact lens as affected by aging and ultraviolet radiation. J Biol Chem 253: 1436–1441, 1978.
Klebanoff SJ: Cytocidal mechanism of phagocytic cells, in Fougereau N, Dausset J (eds): Immunology 1980. London, Academic, 1980, vol 2: Progress Immunology, p 720.
Lehmeyer JE, Johnston RB: Effect of anti-inflammatory drugs and agents that elevate intracellular cyclic AMP on the release of toxic oxygen metabolites by phagocytes: Studies in a model of tissue bound IgG. Clin Immunol Immunopathol 9: 482–490, 1978.
Fülop T Jr, Fóris G, Leóvey A: Age related changes in cAMP and cGMP levels during phagocytosis in human polymorphonuclear leukocytes. Mech Ageing Dev 27: 233–237, 1984.
Abraham EC, Taylor JF, Lang CA: Influence of mouse age and erythrocyte age on glutathione metabolism. Biochem J 174: 819–825, 1978.
Thompson CD, Rea HM, Doesburg VM: Selenium concentrations and glutathione peroxidase activities in whole blood of New Zealand residents. Br J Nutr 37: 457–460, 1977.
Thompson CD, Rea HM, Robinson MF, et al: Low blood selenium concentrations and glutathione peroxidase activity in elderly people. Proc Univ Ote go Med School 55: 18–26, 1977.
Halliwell B: Biochemical mechanisms accounting for the toxic action of oxygen in living organisms: The key role of superoxide dismutase. Cell Biol Int Rep 2: 113–128, 1978.
Hazelton GA, Lang CA: Glutathione contents of tissues in the aging mouse. Biochem J 188: 25–30, 1980.
Joselyn P: Biochemistry of the Thiol Group. London, Academic, 1972.
Tietze F: Enzymic method for quantitative determination of nanogram amounts of total and oxidised glutathione. Anal Biochem 27: 502–522, 1969.
Rupriak ATR, Quincey RV: Mechanism of action of a microsomal inhibitor of protein synthesis potentiated by GSSG. Biochem J 136: 335–342, 1973.
Stjernschantz J: The leukotrienes. J Med Biol 62: 215–230, 1984.
Ovrenius S, Ormstad K, Thor H, et al: Turnover and functions of glutathione studied with isolated hepatic and renal cells. Fed Proc 42: 3177–3188, 1983.
Fülop T Jr, Fóris G, Wórum I, et al: Age related variations of some PMNL functions. Mech Ageing Dev 29: 1–7, 1985.
Noelle JR, Lawrence DA: Determination of glutathione in lymphocyte and possible association of redox state and proliferative capacity of lymphocytes. Biochem J 198: 571–579, 1981.
Spielberg SP, Boxer LA, Oliver JM, et al: Oxidative damage to neutrophils in glutathione synthetase deficiency. Br J Haematol 42: 215–220, 1979.
Reiss U, Gershon D: Rat-liver superoxide dismutase: Purification and age-related modifications. Eur J Biochem 63: 617–623, 1976.
Sbarra AJ, Karnovsky ML: The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J Biol Chem 234: 1355–1361, 1959.
Curnutte JT, Babior BM: Biological defense mechanisms. The effect of bacteria and serum on superoxide production by granulocytes. J Clin Invest 53: 1662–1673, 1974.
Rouzer CA, Scott WA, Kempe J, et al: Prostaglandin synthesis by macrophages requires a specific receptor-ligand interaction. Proc Natl Acad Sci USA 77: 4279–4284, 1980.
Unkeles JC, Wright SD: Structure and modulation of Fc and complement receptors. Contemp Topics Immunobiol 14: 171–196, 1984.
Bonney RJ, Naruns P, Davies P, et al: Antigen-antibody complexes stimulate the synthesis and release of prostaglandins by mouse peritoneal macrophages. Prostaglandins 18: 605–618, 1979.
Corberand JX, Laharrague PF, Fillola G: Neutrophils are normal in normal aged humans. (Letter to the editor) J Leukocyte Biol 40: 333–335, 1986.
Perkins EH: Phagocytic activity of aged mice. J Reticuloendothel Soc 9: 642–643, 1971.
Palmblad J, Haak A: Aging does not change blood granulocyte bactericidal capacity and levels of complement factors 3 and 4. Gerontology 24: 381–387, 1978.
Fiilop T Jr, Foris G, Worum I, et al: Age dependent changes of the Fc7-receptor-mediated functions of human monocytes. Int Arch Allergy Appl Immunol 74: 76–79, 1984.
Fiilop T Jr, Foris G, Worum I, et al: Age dependent alterations of Fc-receptor-mediated effector functions of human polymorphonuclear leukocytes. Clin Exp Immunol 61: 425–432, 1985.
Aderem AA, Wright SD, Silverstein SC, Et Al: Ligated complement receptors do not activate the arachidonic acid cascade in resident peritoneal macrophages. J Exp Med 161: 617–622, 1985.
Fiilop T Jr, Hauck M, Kekessy D, Et Al: The physiologic significance of the glutathione redox cycle in resting and stimulated human PMNLs. Studies on PMNL obtained from healthy young and aged subjects, (in preparation).
Van Epps DE, Goodwin JS, Murphy S: Age dependent variations in polymorphonuclear leukocyte chemiluminescence. Infect Immun 22: 57–61, 1978.
Eschenbach C, Sebach G, Miiller-Lissner St: Nitroblau-tetrazolium-reduktionskapazitat von neutrophil granulocyten. Klin Woch 53: 1049–1056, 1975.
Snyderman R, Pike MC: Chemoattractant receptors on phagocytic cells, in Paul WE (ed): Annual Review of Immunology. Palo Alto, CA, Annual Reviews, 1984, vol 2, p 257.
Smolen JE, Korchak HM, Weissmann G: The roles of extracellular and intracellular calcium in lysosomal enzyme release and superoxide anion generation by human neutrophils. Biochem Bi- ophys Acta 677: 512 - 519, 1981.
Scully SP, Segal GB, Lichtman MA: Relationship of superoxide production to cytoplasmic free calcium in human monocytes. J Clin Invest 77: 1349–1356, 1986.
Torres M, Coates TD: Neutrophil cytoplasts: Relationships of superoxide release and calcium pools. Blood 64: 891–895, 1984.
Berridge MJ, Irvine RF: Inositol triphosphate a novel second messenger in cellular signal transduction. Nature (Lond) 312: 315–320, 1984.
Dougherty RW, Godfrey PP, Hoyle PC, et al: Secretagogue-induced phosphoinositide metabolism in human leukocytes. Biochem J 222: 307–315, 1984.
Snyderman R, Smith CD, Verghese MW: Model for leukocyte regulation by chemoattractant receptors: Roles of a guanine nucleotide regulatory protein and polyphosphinositide metabolism. J Leukocyte Biol 40: 785–800, 1986.
Snyderman R: Regulatory mechanisms of a chemoattractant receptor on leukocytes. Fed Proc 43: 2743–2748, 1984.
Vergehese MW, Smith CD, Charles LA, et al: A guanine nucleotide regulatory protein controls polyphosphoinositide metabolism Ca2+ mobilization and cellular responses to chemoattractants in human monocytes. J Immunol 137: 271–275, 1986.
Goldman DW, Chang FH, Gifford LA: Pertussis toxin inhibition of chemotactic factor-induced calcium mobilization and function in human polymorphonuclear leucocytes. J Exp Med 162:145– 156, 1985.
Krause KM, Schlegel W, Wollheim CB, et al: Chemotactic peptide activation of human neutrophils and HL-60 cells. Pertussis toxin reveals correlation between inositol triphosphate generation calcium ion transients and cellular activation. J Clin Invest 76: 1348–1354, 1985.
Pozzan TP, Lew D, Wollheim CB, et al: Is cytosolic free calcium regulating neutrophil activation? Science 221: 1413–1415, 1983.
Cockroft S, Bennett JP, Gomperts BD: F-met-leu-phe induced phosphatidylinositol turnover in rabbit neutrophils is dependent on extracellular calcium. FEBS Lett 110: 115–120, 1980.
Takenawa T, Hanma Y, Nagai Y: Role of Ca2+ in phosphatidylinositol response and arachidonic acid release in formylated tripeptide or Ca2+ ionophore A23187-stimulated guinea pig neutrophils. J Immunol 130: 2849–2857, 1983.
Wynkoop EM, Broekman J, Korchak HM, et al: Phospholipid metabolism in human neutrophils activated by N-formyl-methionyl-leucyl-phenylalanine. Biochem J 236: 829–837, 1986.
Hamma Y, Onozaki K, Hashimoto T, et al: Differential activation of phospholipids metabolism by formylated peptide and ionophore A23187 in guinea pig peritoneal macrophages. J Immunol 129: 1619–1624, 1982.
Smolen JE, Weissman G: Stimuli which provoke secretion of azurophil enzymes from human neutrophils induce increments in adenosine cyclic 3’–5’-monophosphate. Biochim Biophys Acta 672: 197–206, 1981.
Fiilop T Jr, Varga Z, Foris G, Kekessyl D: unpublished data.
Simchowitz L, Fischbein LC, Spilberg I, et al: Induction of transient elevation in intracellular levels of cAMP by chemotactic factors: An early event in human neutrophil activation. J Immunol 124: 1482–1491, 1980.
Hauck M, Fiilop T Jr, Foris G, et al: Divergent effects of human lymphokine-derived oligopeptides on PMNL function of young and aged healthy subjects. Int J Immunopharmacol 9: 3–8, 1987.
Fiilop T Jr, Kekessy D, Foris G: Impaired coupling of naloxone sensitive opiate receptors to adenylate cyclase in PMNL of aged male subjects. Int J Immunopharmacol 9: 651–657, 1987.
Miller RA: Immunodeficiency of ageing: Restorative effects of phorbol ester combined with calcium ionophore. J Immunol 137: 805–808, 1986.
McLauglin B, O’Malley K, Cotter TG: Age related differences in granulocyte chemotaxis and degranulation. Clin Sci 70: 59–62, 1986.
Tam CF, Walford RL: Cyclic nucleotide levels in resting and mitogen-stimulated spleen cell suspensions from young and aged mice. Mech Ageing Dev 7: 309–320, 1978.
Castagne M, Takai Y, Kaibuchi, Et Al: Direct activation of calcium activated, phospholipid dependent protein kinase by tumor promoting phorbol esters. J Biol Chem 257: 7847–7853, 1982.
Wilson E, Olcott MC, Bell RM, et al: Inhibition of the oxidative burst in human neutrophils by sphingoid long chain basis. J Biol Chem 261: 12616–12623, 1986.
Gerard C, McPhail LC, Marfat A, et al: Role of protein kinases in stimulation of human poly-morphonuclear leukocyte oxidative metabolism by various agonists. Differential effects of a novel protein kinase inhibitor. J Clin Invest 77: 61–65, 1986.
Cox CC, Dougherty RW, Ganong BR, et al: Differential stimulation of the respiratory burst and lysosomal enzyme secretion in human polymorphonuclear leukocytes by synthetic diacylglycerols. J Immunol 136: 4611–4616, 1986.
McPhail L, Henson P, Johnston R: Respiratory burst enzyme in human neutrophils. J Clin Invest 67: 710–716, 1981.
McPhail LC, Henson PM, Johnston RB: Respiratory burst enzyme in human neutrophils. Evidence for multiple mechanisms of action. J Clin Invest 67: 710–716, 1981.
Williams JD, Lee TH, Lewis RA, et al: Intracellular retention of the 5-lipoxygenase pathway product leukotriene B4, by human neutrophils activated with unopsonized zymosan. J Immunol 134: 2624–2630, 1985.
Fujita I, Irita K, Takeshige K, et al: Diacylglycerol, 1-oleyl 2 acetyl-glycerol, stimulates superox- ide-generation from human neutrophils. Biochem Biophys Res Commun 120: 318–324, 1984.
Wolfson M, McPhail LC, Nasrallah VN, et al: Phorbol myristate acetate mediates redistribution of protein kinase C in human neutrophils: Potential role in the activation of the respiratory burst enzyme. J Immunol 135: 2057–2062, 1985.
Nathan CF, Bruckner LM, Silverstein SC, et al: Extracellular cytolysis by activated macrophages and granulocytes. II. Hydrogen peroxide as a mediator of cytotoxicity. J Exp Med 149: 84–100, 1979.
Clark RA, Klebanoff SJ: Chemotactic factor inactivation by the myeloperoxidase-hydrogen perox- ide-halide system: An inflammatory control mechanism. J Clin Invest 64: 913–920, 1979.
Pryor WA: Free radical pathology. Chem Eng News 49: 34–51, 1971.
Zs.Nagy I, Pieri C, Givli C, Et Al: Effects of centrophenoxine on the monovalent electrolyte contents of the large brain cortical cells of old rats. Gerontology 25: 94–102, 1979.
Semsei I, Zs.Nagy I: Effects of ionic strength on the activity of superoxide dismutase in vitro. Arch Gerontol Geriatr 3: 287–295, 1984.
Vanella A, Geremia E, D’Urso, Et Al: Superoxide dismutase activities in aging rat brain. Gerontology 28: 108–113, 1982.
Tolmasoff JM, Ono T, Cutler RG: Superoxide dismutase correlation with life-span and specific metabolic rate in primate species. Proc Natl Acad Sci USA 77: 2777–2781, 1980.
Cufler RG: Superoxide dismutase, longevity and opecific metabolic rate. Gerontology 29:113– 120, 1983.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1988 Plenum Press, New York
About this chapter
Cite this chapter
Fülöp, T., Fóris, G., Nagy, J.T., Varga, Z., Leövey, A. (1988). The Respiratory Burst and Aging. In: Sbarra, A.J., Strauss, R.R. (eds) The Respiratory Burst and Its Physiological Significance. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5496-3_20
Download citation
DOI: https://doi.org/10.1007/978-1-4684-5496-3_20
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4684-5498-7
Online ISBN: 978-1-4684-5496-3
eBook Packages: Springer Book Archive