Abstract
Phagocytic leukocytes, when appropriately stimulated, display a respiratory burst in which they consume oxygen and produce superoxide anions. Superoxide is produced by the phagocyte NADPH-oxidase system which is a multiprotein complex that is dissociated in quiescent cells and is assembled into the functional oxidase following stimulation of these cells. Also associated with the respiratory burst is the generation of other reactive oxygen species. The identity of components of the NADPH-oxidase system and their interactions are known in considerable molecular detail. Understanding of the regulation of superoxide production is less well known. This review also points out the important role of microscopy in complementing biochemical studies to understand better the cell biology of the phagocyte respiratory burst.
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References
Babior BM, Kipnes RS, Curnutte JT (1973) Biological defense mechanisms. The production of superoxide, a potential, a potential bactericidal agent. J Clin Invest 52:741–744
Baldridge CW, Gerard RW (1933) The extra respiration of phagocytosis. Am J Physiol 103:235–236
Briggs RT, Robinson JM, Karnovsky ML, Karnovsky MJ (1986) Superoxide production by polymorphonuclear leukocytes. A cytochemical approach. Histochemistry 84:371–378
Cross AR, Segal AW (2004) The NADPH oxidase of professional phagocytes—prototype of the NOX electron transport chain systems. Biochimica et Biophysica Acta 1657:1–22
Curnutte JT, Whitten DM, Babior BM (1974) Defective superoxide production by granulocytes from patients with chronic granulomatous disease. N Engl J Med 290:593–597
Dagher M-C, Pick E (2007) Opening the black box: lessons from cell-free systems on the phagocyte NADPH-oxidase. Biochimie 89:1123–1132
Hartfield PJ, Robinson JM (1990) Fluoride-mediated activation of the respiratory burst in electropermeabilized neutrophils. Biochim Biophys Acta 1054:176–180
Heyworth PG, Cross AR, Curnutte JT (2003) Chronic granulomatous disease. Curr Opin Immunol 15:578–584
Kheradmand K, Werner E, Tremble P, Symons M, Werb Z (1998) Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 280:898–902
Kindzelskii AL, Petty HR (2002) Apparent role of traveling metabolic waves in oxidant release by living neutrophils. Proc Natl Acad Sci USA 99:9207–9212
Kobayashi T, Robinson JM (1991) A novel intracellular compartment with unusual secretory properties in human neutrophils. J Cell Biol 113:743–756
Kobayashi T, Robinson JM, Seguchi H (1998) Identification of intracellular sites of superoxide production in stimulated neutrophils. J Cell Sci 111:81–91
Malech HL, Hickstein DD (2007) Genetics, biology and clinical management of myeloid cell primary immune deficiencies: chronic granulomatous disease and leukocyte adhesion deficiency. Curr Opin Hematol 14:29–36
Nathan CF (1987) Neutrophil activation on biological surfaces. Massive secretion of hydrogen peroxide in response to products of macrophages and lymphocytes. J Clin Invest 80:1550–1560
Nauseef WM (2004) Assembly of the phagocyte NADPH oxidase. Histochem Cell Biol 122:277–291
Robinson JM (2008) Reactive oxygen species in phagocytic leukocytes. Histochem Cell Biol 130:281–297
Robinson JM, Badwey JT (1995) The NADPH oxidase complex of phagocytic leukocytes: a biochemical and cytochemical view. Histochem Cell Biol 103:163–180
Robinson JM, Badwey JA, Karnovsky MJ, Karnovsky ML (1987) Cell surface dynamics of neutrophils stimulated with phorbol esters or retinoids. J Cell Biol 105:417–426
Robinson JM, Ohira T, Badwey JA (2004) Regulation of the NADPH-oxidase complex of phagocytic leukocytes. Recent insights from structural biology, molecular genetics, and microscopy. Histochem Cell Biol 122:293–304
Roos D, van Bruggen R, Meischl C (2003) Oxidative killing of microbes by neutrophils. Microbes Infect 5:1307–1315
Sbarra AJ, Karnovsky ML (1959) The biochemical basis of phagocytosis. I. Metabolic changes during the ingestion of particles by polymorphonuclear leukocytes. J Biol Chem 234:1335–1362
Sternweis PV, Gilman AG (1982) Aluminum: a requirement for the activation of the regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci USA 79:4888–4891
Suchard SJ, Boxer LA (1994) Exocytosis of a subpopulation of specific granules coincides with H2O2 production in adherent human neutrophils. J Immunol 152:290–300
Tarpey MM, Wink DA, Grisham MB (2004) Methods for the detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Physiol 286:R431–R444
Acknowledgments
The long and rewarding collaboration studying neutrophil biology with the late John A. Badwey is remembered with happiness while his untimely passing is sadly acknowledged. The references allowed in this article were limited in number; the author therefore apologizes to those whose work was not directly cited due to this limitation.
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Presented at the 50th Anniversary Symposium of the Society for Histochemistry, Interlaken, Switzerland, October 1–4, 2008.
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Robinson, J.M. Phagocytic leukocytes and reactive oxygen species. Histochem Cell Biol 131, 465–469 (2009). https://doi.org/10.1007/s00418-009-0565-5
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DOI: https://doi.org/10.1007/s00418-009-0565-5