The Role of Superoxide Anion and Hydrogen Peroxide in Phagocytosis-associated Oxidative Metabolic Reactions

Overview

Journal J Clin Invest

Specialty General Medicine

Date 1975 Sep 1

PMID 169293

Citations 51

Authors

R L Baehner

S K Murrmann

J Davis

R B JOHNSTON Jr

Affiliations

Soon will be listed here.

Abstract

The contribution of hydrogen peroxide (H2O2) and one of its unstable intermediates, superoxide anion (O2), to the oxidative reactions that occur in phagocytizing leukocytes was explored by depleting these cells of O2. This was accomplished by allowing them to phagocytize latex particles coated with superoxide dismutase (SOD), which catalyzes the generation of H2O2 from O2. Although the rate and extent of phagocytosis of latex coated with bovine serum albumin was similar to latex coated with SOD, the rate of oxygen consumption, [14C]formate oxidation, [1-14C]glucose oxidation, and iodination of zymosan particles was significantly enhanced by SOD. In contrast, the rate and extent of reduction of nitroblue tetrazolium (NBT) was diminished by 60%. These studies indicate that the majority of NBT reduction by leukocytes is due to O2, whereas stimulation of the hexose monophosphate shunt and iodination of ingested particles requires H2O2 generated from the increased reduction of oxygen by phagocytizing leukocytes.

Citing Articles

Immunomodulatory Effects of Radon Inhalation on Lipopolysaccharide-Induced Inflammation in Mice.

Kataoka T, Naoe S, Murakami K, Fujimoto Y, Yukimine R, Tanaka A Int J Environ Res Public Health. 2022; 19(17).

PMID: 36078348 PMC: 9518351. DOI: 10.3390/ijerph191710632.

Looking Back at the Early Stages of Redox Biology.

Flohe L Antioxidants (Basel). 2020; 9(12).

PMID: 33317108 PMC: 7763103. DOI: 10.3390/antiox9121254.

X-Irradiation at 0.5 Gy after the forced swim test reduces forced swimming-induced immobility in mice.

Kataoka T, Shuto H, Yano J, Naoe S, Ishida T, Nakada T J Radiat Res. 2020; 61(4):517-523.

PMID: 32346734 PMC: 7336566. DOI: 10.1093/jrr/rraa022.

Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition).

Cossarizza A, Chang H, Radbruch A, Acs A, Adam D, Adam-Klages S Eur J Immunol. 2019; 49(10):1457-1973.

PMID: 31633216 PMC: 7350392. DOI: 10.1002/eji.201970107.

Guidelines for the use of flow cytometry and cell sorting in immunological studies.

Cossarizza A, Chang H, Radbruch A, Akdis M, Andra I, Annunziato F Eur J Immunol. 2017; 47(10):1584-1797.

PMID: 29023707 PMC: 9165548. DOI: 10.1002/eji.201646632.

References

Baehner R, Nathan D, Karnovsky M . Correction of metabolic deficiencies in the leukocytes of patients with chronic granulomatous disease. J Clin Invest. 1970; 49(5):865-70. PMC: 535758. DOI: 10.1172/JCI106305. View

McCord J, Fridovich I . Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem. 1969; 244(22):6049-55. View

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

Karnovsky M . Metabolic basis of phagocytic activity. Physiol Rev. 1962; 42:143-68. DOI: 10.1152/physrev.1962.42.1.143. View

Reed P . Glutathione and the hexose monophosphate shunt in phagocytizing and hydrogen peroxide-treated rat leukocytes. J Biol Chem. 1969; 244(9):2459-64. View

JOHNSTON Jr R, Keele Jr B, Misra H, Lehmeyer J, Webb L, Baehner R . The role of superoxide anion generation in phagocytic bactericidal activity. Studies with normal and chronic granulomatous disease leukocytes. J Clin Invest. 1975; 55(6):1357-72. PMC: 301891. DOI: 10.1172/JCI108055. View

Karnovsky M . Chronic granulomatous disease--pieces of a cellular and molecular puzzle. Fed Proc. 1973; 32(4):1527-33. View

Babior B, Kipnes R, Curnutte J . Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent. J Clin Invest. 1973; 52(3):741-4. PMC: 302313. DOI: 10.1172/JCI107236. View

Baehner R, Nathan D . Quantitative nitroblue tetrazolium test in chronic granulomatous disease. N Engl J Med. 1968; 278(18):971-6. DOI: 10.1056/NEJM196805022781801. View

10.

Baehner R, Gilman N, Karnovsky M . Respiration and glucose oxidation in human and guinea pig leukocytes: comparative studies. J Clin Invest. 1970; 49(4):692-700. PMC: 322524. DOI: 10.1172/JCI106281. View

11.

Webb L, Keele Jr B, JOHNSTON Jr R . Inhibition of phagocytosis-associated chemiluminescence by superoxide dismutase. Infect Immun. 1974; 9(6):1051-6. PMC: 414931. DOI: 10.1128/iai.9.6.1051-1056.1974. View

12.

Paul B, Sbarra A . The role of the phagocyte in host-parasite interactions. 13. The direct quantitative estimation of H2O2 in phagocytizing cells. Biochim Biophys Acta. 1968; 156(1):168-78. DOI: 10.1016/0304-4165(68)90116-5. View

13.

JOHNSTON Jr R, Baehner R . Improvement of leukocyte bactericidal activity in chronic granulomatous disease. Blood. 1970; 35(3):350-5. View

14.

Pincus S, Klebanoff S . Quantitative leukocyte iodination. N Engl J Med. 1971; 284(14):744-50. DOI: 10.1056/NEJM197104082841402. View

15.

Allen R, STJERNHOLM R, Steele R . Evidence for the generation of an electronic excitation state(s) in human polymorphonuclear leukocytes and its participation in bactericidal activity. Biochem Biophys Res Commun. 1972; 47(4):679-84. DOI: 10.1016/0006-291x(72)90545-1. View

16.

Klebanoff S, Hamon C . Role of myeloperoxidase-mediated antimicrobial systems in intact leukocytes. J Reticuloendothel Soc. 1972; 12(2):170-96. View

17.

Baehner R, Nathan D, Castle W . Oxidant injury of caucasian glucose-6-phosphate dehydrogenase-deficient red blood cells by phagocytosing leukocytes during infection. J Clin Invest. 1971; 50(12):2466-73. PMC: 292196. DOI: 10.1172/JCI106747. View

18.

Karnovsky M . The metabolism of leukocytes. Semin Hematol. 1968; 5(2):156-65. View