Induction of Phagocyte Cytochrome B Heavy Chain Gene Expression by Interferon Gamma

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1988 Jul 1

PMID 2839835

Citations 40

Authors

P E Newburger

R A Ezekowitz

C Whitney

J Wright

S H Orkin

Affiliations

Soon will be listed here.

Abstract

Phagocytic cells, such as macrophages and polymorphonuclear leukocytes, produce a "respiratory burst" in which oxygen is reduced to superoxide and other active oxygen species responsible for many of the microbicidal, tumoricidal, and inflammatory activities of these cells. Interferon gamma has been shown to augment phagocyte superoxide production, but the molecular mechanisms underlying this effect have remained unknown. Recently a key component of the oxidase, phagocyte cytochrome b, has been characterized as a heterodimer of a 91-kDa glycoprotein and a 22-kDa polypeptide. The present studies examined the effects of human recombinant interferon gamma on the expression of the genes for these components of the cytochrome b. In vitro treatment with interferon gamma substantially increases the level of phagocyte cytochrome b heavy chain gene transcripts in normal polymorphonuclear leukocytes, normal monocyte-derived macrophages, and the monocytic leukemia cell line THP-1. Light chain gene transcripts are less affected. In monocyte-derived macrophages and THP-1 cells, the enhanced expression of the heavy chain gene appears in large part attributable to increased rates of transcription. Treatment of monocyte-derived macrophages with human recombinant interferon alpha (a down-regulator of the respiratory burst) decreased the heavy chain transcript levels; interferon beta produced no detectable change. These findings demonstrate the responsiveness of one essential component of the phagocyte oxidase system to activation by interferon gamma and provide a rationale for its use to augment phagocytic function in chronic granulomatous disease.

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References

Clark I, Hunt N, Butcher G, Cowden W . Inhibition of murine malaria (Plasmodium chabaudi) in vivo by recombinant interferon-gamma or tumor necrosis factor, and its enhancement by butylated hydroxyanisole. J Immunol. 1987; 139(10):3493-6. View

Cassatella M, Cappelli R, Della Bianca V, Grzeskowiak M, Dusi S, Berton G . Interferon-gamma activates human neutrophil oxygen metabolism and exocytosis. Immunology. 1988; 63(3):499-506. PMC: 1454770. View

Parkos C, Dinauer M, Walker L, Allen R, Jesaitis A, Orkin S . Primary structure and unique expression of the 22-kilodalton light chain of human neutrophil cytochrome b. Proc Natl Acad Sci U S A. 1988; 85(10):3319-23. PMC: 280200. DOI: 10.1073/pnas.85.10.3319. View

Tsunawaki S, Nathan C . Enzymatic basis of macrophage activation. Kinetic analysis of superoxide production in lysates of resident and activated mouse peritoneal macrophages and granulocytes. J Biol Chem. 1984; 259(7):4305-12. View

Baehner R, Nathan D . Leukocyte oxidase: defective activity in chronic granulomatous disease. Science. 1967; 155(3764):835-6. DOI: 10.1126/science.155.3764.835. View

Segal A, Jones O, Webster D, Allison A . Absence of a newly described cytochrome b from neutrophils of patients with chronic granulomatous disease. Lancet. 1978; 2(8087):446-9. DOI: 10.1016/s0140-6736(78)91445-9. View

Tsuchiya S, Yamabe M, Yamaguchi Y, Kobayashi Y, Konno T, Tada K . Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int J Cancer. 1980; 26(2):171-6. DOI: 10.1002/ijc.2910260208. View

Cross A, Higson F, Jones O, Harper A, Segal A . The enzymic reduction and kinetics of oxidation of cytochrome b-245 of neutrophils. Biochem J. 1982; 204(2):479-85. PMC: 1158375. DOI: 10.1042/bj2040479. View

Woods D, Markham A, Ricker A, Goldberger G, Colten H . Isolation of cDNA clones for the human complement protein factor B, a class III major histocompatibility complex gene product. Proc Natl Acad Sci U S A. 1982; 79(18):5661-5. PMC: 346964. DOI: 10.1073/pnas.79.18.5661. View

10.

Segal A, Cross A, Garcia R, Borregaard N, Valerius N, Soothill J . Absence of cytochrome b-245 in chronic granulomatous disease. A multicenter European evaluation of its incidence and relevance. N Engl J Med. 1983; 308(5):245-51. DOI: 10.1056/NEJM198302033080503. View

11.

Weil J, Epstein C, Epstein L, Sedmak J, Sabran J, Grossberg S . A unique set of polypeptides is induced by gamma interferon in addition to those induced in common with alpha and beta interferons. Nature. 1983; 301(5899):437-9. DOI: 10.1038/301437a0. View

12.

MICHELSON A, Markham A, Orkin S . Isolation and DNA sequence of a full-length cDNA clone for human X chromosome-encoded phosphoglycerate kinase. Proc Natl Acad Sci U S A. 1983; 80(2):472-6. PMC: 393400. DOI: 10.1073/pnas.80.2.472. View

13.

Murray H, Nathan C . Suppression of macrophage antimicrobial activity by a tumor cell product. J Immunol. 1983; 131(1):384-7. View

14.

Nathan C, Murray H, Wiebe M, Rubin B . Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med. 1983; 158(3):670-89. PMC: 2187114. DOI: 10.1084/jem.158.3.670. View

15.

Newburger P, Speier C, Borregaard N, Walsh C, Whitin J, Simons E . Development of the superoxide-generating system during differentiation of the HL-60 human promyelocytic leukemia cell line. J Biol Chem. 1984; 259(6):3771-6. View

16.

McPhail L, CLAYTON C, Snyderman R . The NADPH oxidase of human polymorphonuclear leukocytes. Evidence for regulation by multiple signals. J Biol Chem. 1984; 259(9):5768-75. View

17.

Babior B . Oxidants from phagocytes: agents of defense and destruction. Blood. 1984; 64(5):959-66. View

18.

Friedman R, Manly S, McMahon M, Kerr I, Stark G . Transcriptional and posttranscriptional regulation of interferon-induced gene expression in human cells. Cell. 1984; 38(3):745-55. DOI: 10.1016/0092-8674(84)90270-8. View

19.

Guthrie L, McPhail L, Henson P, JOHNSTON Jr R . Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxide-producing enzyme. J Exp Med. 1984; 160(6):1656-71. PMC: 2187529. DOI: 10.1084/jem.160.6.1656. View

20.

Haslett C, Guthrie L, Kopaniak M, JOHNSTON Jr R, Henson P . Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am J Pathol. 1985; 119(1):101-10. PMC: 1888083. View