DOI: 10.1126/science.2541500. Role of Na + /H + Exchange by Interferon-γ in Enhanced Expression of JE and I-A β Genes

Role of Na + /H + Exchange by Interferon-γ in Enhanced Expression of JE and I-A β Genes

10.1126/science.2541500

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

The rapid transductional sequences initiated by interferon-γ (IFN-γ) on binding to its receptor regulate functional and genomic responses in many cells but are not well defined. Induction of macrophage activation is an example of such functional and genomic changes in response to IFN-γ. Addition of IFN-γ to murine macrophages, at activating concentrations, produced rapid (within 60 seconds) alkalinization of the cytosol and a concomitant, rapid influx of 22 Na + . Amiloride inhibited the ion fluxes and the accumulation of specific messenger RNA for two genes induced by IFN-γ (the early gene JE and the β chain of the class II major histocompatibility complex gene I-A). The data indicate that IFN-γ initiates rapid exchange of Na + and H + by means of the Na + /H + antiporter and that these amiloride-sensitive ion fluxes are important to some of the genomic effects of IFN-γ.

Bibliography

Prpic, V., Yu, S.-F., Figueiredo, F., Hollenbach, P. W., Gawdi, G., Herman, B., Uhing, R. J., & Adams, D. O. (1989). Role of Na + /H + Exchange by Interferon-Î³ in Enhanced Expression of JE and I-A Î² Genes. Science, 244(4903), 469â471.

Authors 8

Veronica Prpic (first)
Sheau-Fung Yu (additional)
Figueiredo Figueiredo (additional)
Paul W. Hollenbach (additional)
Gowind Gawdi (additional)
Brian Herman (additional)
Ronald J. Uhing (additional)
Dolph O. Adams (additional)

References 33 Referenced 65

ADAMS, D.O., THE CELL BIOLOGY OF MACROPHAGE ACTIVATION, ANNUAL REVIEW OF IMMUNOLOGY 2: 283 (1984). (10.1146/annurev.iy.02.040184.001435) / ANNUAL REVIEW OF IMMUNOLOGY (1984)
ADAMS, D.O., MOLECULAR TRANSDUCTIONAL MECHANISMS BY WHICH IFN-GAMMA AND OTHER SIGNALS REGULATE MACROPHAGE DEVELOPMENT, IMMUNOLOGICAL REVIEWS 97: 5 (1987). (10.1111/j.1600-065X.1987.tb00514.x) / IMMUNOLOGICAL REVIEWS (1987)
Adams, D. O., Inflammation: Basic Principles and Clinical Correlates: 471 (1988). / Inflammation: Basic Principles and Clinical Correlates (1988)
10.1021/bi00591a005
10.1073/pnas.81.7.1991
10.1016/0092-8674(83)90037-5
FERTSCHRUGGIO, D, INDUCTION OF MACROPHAGE IA-ANTIGEN EXPRESSION BY RIFN-GAMMA AND DOWN-REGULATION BY IFN-ALPHA IFN-BETA AND DEXAMETHASONE ARE REGULATED TRANSCRIPTIONALLY, JOURNAL OF IMMUNOLOGY 141: 1582 (1988). (10.4049/jimmunol.141.5.1582) / JOURNAL OF IMMUNOLOGY (1988)
FIGUEIREDONETO F unpublished data.
10.1126/science.3726537
FRELIN, C, MOLECULAR-PROPERTIES OF AMILORIDE ACTION AND OF ITS NA+ TRANSPORTING TARGETS, KIDNEY INTERNATIONAL 32: 785 (1987). (10.1038/ki.1987.277) / KIDNEY INTERNATIONAL (1987)
HALL, D.J., PLATELET-DERIVED GROWTH FACTOR-INDUCIBLE GENES RESPOND DIFFERENTIALLY TO AT LEAST 2 DISTINCT INTRACELLULAR 2ND MESSENGERS, JOURNAL OF BIOLOGICAL CHEMISTRY 262: 15302 (1987). (10.1016/S0021-9258(18)48175-6) / JOURNAL OF BIOLOGICAL CHEMISTRY (1987)
HAMILTON, T. A., IMMUNOLOGY TODAY 8: 151 (1987). (10.1016/0167-5699(87)90145-9) / IMMUNOLOGY TODAY (1987)
HAMILTON, T.A., MALEYLATED-BSA SUPPRESSES IFN-GAMMA-MEDIATED IA EXPRESSION IN MURINE PERITONEAL-MACROPHAGES, JOURNAL OF IMMUNOLOGY 138: 4063 (1987). (10.4049/jimmunol.138.12.4063) / JOURNAL OF IMMUNOLOGY (1987)
HERMAN, B, PLATELET-DERIVED GROWTH FACTOR-INDUCED ALTERATIONS IN VINCULIN DISTRIBUTION IN PORCINE VASCULAR SMOOTH-MUSCLE CELLS, CELL MOTILITY AND THE CYTOSKELETON 8: 91 (1987). (10.1002/cm.970080202) / CELL MOTILITY AND THE CYTOSKELETON (1987)
INTRONA, M, THE EFFECT OF LPS ON EXPRESSION OF THE EARLY COMPETENCE GENE-JE AND GENE-KC IN MURINE PERITONEAL-MACROPHAGES, JOURNAL OF IMMUNOLOGY 138: 3891 (1987). (10.4049/jimmunol.138.11.3891) / JOURNAL OF IMMUNOLOGY (1987)
KLEYMAN, T.R., AMILORIDE AND ITS ANALOGS AS TOOLS IN THE STUDY OF ION-TRANSPORT, JOURNAL OF MEMBRANE BIOLOGY 105: 1 (1988). (10.1007/BF01871102) / JOURNAL OF MEMBRANE BIOLOGY (1988)
KOERNER, T.J., THE EARLY COMPETENCE GENES JE AND KC ARE DIFFERENTIALLY REGULATED IN MURINE PERITONEAL-MACROPHAGES IN RESPONSE TO LIPOPOLYSACCHARIDE, BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS 149: 969 (1987). (10.1016/0006-291X(87)90503-1) / BIOCHEMICAL AND BIOPHYSICAL RESEARCH COMMUNICATIONS (1987)
KOERNER, T.J., SUPPRESSED EXPRESSION OF SURFACE IA ON MACROPHAGES BY LIPOPOLYSACCHARIDE - EVIDENCE FOR REGULATION AT THE LEVEL OF ACCUMULATION OF MESSENGER-RNA, JOURNAL OF IMMUNOLOGY 139: 239 (1987). (10.4049/jimmunol.139.1.239) / JOURNAL OF IMMUNOLOGY (1987)
KOERNER, T.J., YEAR IMUNOL 4: 1 (1988). / YEAR IMUNOL (1988)
MOOLENAAR, W.H., EFFECTS OF GROWTH-FACTORS ON INTRACELLULAR PH REGULATION, ANNUAL REVIEW OF PHYSIOLOGY 48: 363 (1986). (10.1146/annurev.ph.48.030186.002051) / ANNUAL REVIEW OF PHYSIOLOGY (1986)
PESTKA, S, INTERFERONS AND THEIR ACTIONS, ANNUAL REVIEW OF BIOCHEMISTRY 56: 727 (1987). (10.1146/annurev.bi.56.070187.003455) / ANNUAL REVIEW OF BIOCHEMISTRY (1987)
PRPIC V unpublished data.
REVEL, M, TRENDS IN BIOCHEMICAL SCIENCES 11: 166 (1986). (10.1016/0968-0004(86)90134-9) / TRENDS IN BIOCHEMICAL SCIENCES (1986)
RINK, T.J., CYTOPLASMIC PH AND FREE MG-2+ IN LYMPHOCYTES, JOURNAL OF CELL BIOLOGY 95: 189 (1982). (10.1083/jcb.95.1.189) / JOURNAL OF CELL BIOLOGY (1982)
ROLLINS, B.J., CLONING AND EXPRESSION OF JE, A GENE INDUCIBLE BY PLATELET-DERIVED GROWTH-FACTOR AND WHOSE PRODUCT HAS CYTOKINE-LIKE PROPERTIES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 85: 3738 (1988). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1988)
ROSA, F.M., REGULATION OF HLA-DR GENE BY IFN-GAMMA - TRANSCRIPTIONAL AND POST-TRANSCRIPTIONAL CONTROL, JOURNAL OF IMMUNOLOGY 140: 1660 (1988). (10.4049/jimmunol.140.5.1660) / JOURNAL OF IMMUNOLOGY (1988)
10.1126/science.3018928
SEBALDT R.J. unpublished data.
SMITH, L.L., RECOMBINANT MURINE INTERFERON-GAMMA-INDUCED DIFFERENTIATION OF PRE-B LYMPHOCYTES IS ASSOCIATED WITH NA+/H+ EXCHANGE-DEPENDENT AND EXCHANGE-INDEPENDENT CYTOPLASMIC ALKALINIZATION, JOURNAL OF BIOLOGICAL CHEMISTRY 263: 7359 (1988). (10.1016/S0021-9258(18)68650-8) / JOURNAL OF BIOLOGICAL CHEMISTRY (1988)
SOMERS, S.D., PHORBOL ESTERS AND CALCIUM IONOPHORE CAN PRIME MURINE PERITONEAL-MACROPHAGES FOR TUMOR-CELL DESTRUCTION, JOURNAL OF IMMUNOLOGY 136: 4199 (1986). (10.4049/jimmunol.136.11.4199) / JOURNAL OF IMMUNOLOGY (1986)
10.1016/0076-6879(83)00060-9
UNANUE, E.R., ANTIGEN-PRESENTING FUNCTION OF THE MACROPHAGE, ANNUAL REVIEW OF IMMUNOLOGY 2: 395 (1984). (10.1146/annurev.iy.02.040184.002143) / ANNUAL REVIEW OF IMMUNOLOGY (1984)
10.1126/science.2429366

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 5:21 p.m.)
Deposited	1 year, 7 months ago (Jan. 12, 2024, 5:31 p.m.)
Indexed	1 year, 2 months ago (June 17, 2024, 3:56 p.m.)
Issued	36 years, 4 months ago (April 28, 1989)
Published	36 years, 4 months ago (April 28, 1989)
Published Print	36 years, 4 months ago (April 28, 1989)

Funders 0

None

BibTeX

@article{Prpic_1989, title={Role of Na + /H + Exchange by Interferon-γ in Enhanced Expression of JE and I-A β Genes}, volume={244}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.2541500}, DOI={10.1126/science.2541500}, number={4903}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Prpic, Veronica and Yu, Sheau-Fung and Figueiredo, Figueiredo and Hollenbach, Paul W. and Gawdi, Gowind and Herman, Brian and Uhing, Ronald J. and Adams, Dolph O.}, year={1989}, month=apr, pages={469–471} }

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