Progesterone inhibits inducible nitric oxide synthase gene expression and nitric oxide production in murine macrophages

Journal of Leukocyte Biology

Volumn 59, Issue 3, 1996, Pages 442-450

  Miller, Lance ^a   Alley, Evan W ^a   Murphy, William J ^a   Russell, Stephen W ^a   Hunt, Joan S ^b  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

Author keywords

Effector molecules; Female sex steroids; Houst defense; Mouse

Indexed keywords

DEXAMETHASONE; ESTRADIOL; GAMMA INTERFERON; LIPOPOLYSACCHARIDE; LUCIFERASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROGESTERONE;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; GENE EXPRESSION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE;

EID: 0029866697     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.59.3.442     Document Type: Article

References (47)

1. Auger, M.J., Ross, J.A. (1992) The biology of the macrophage. In The Macrophage (C.E. Lewis, J.O'D. MeGee, eds.), Oxford Univ. Press, Oxford, 3.
2. Denis, M. (1994) Human monocytes/macrophages: NO or NO? J. Leukoc. Biol., 55, 682-684.
3. Marletta, M.A., Yoon, P.S., Iyengar, R., Leaf, C.D., Wishnok, J.S. (1988) Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemisty 27, 8706-8711.
4. Snyder, S.H., Bredt, D.S. (1992) Biological roles of nitric oxide. Sci. Am., 68-76.
5. Adams, D.O., Hamilton, T.A. (1992) Molecular basis of macrophage activation: diversity and its origins. In The Macrophage (C.E. Lewis, J.O'D. McGee, eds.), Oxford Univ. Press, Oxford, 75.
6. Zheng, Y., Zhou, Z.Z., Lyttle, C.R., Teusher, C. (1988) Immunochemical characterization of the estrogen-stimulated leukocyte influx in the immature rat uterus. J. Leukoc Biol. 44, 27-32.
7. Wang, J.M., Griffin, J.D., Rambaldi, A., Chen, Z.G., Mantovani, A. (1988) Induction of monocyte migration by recombinant macrophage colony-stimulating factor. J. Immunol. 141, 575-579.
8. Friedman, D., Nettl, F.M., Schreiber, A.D. (1985) Effect of estradiol and steroid analogues on the clearance of immunoglobulin G-coated erythrocytes. J. Clin. Invest. 75, 162-167.
9. Schreiber, A.D., Nettl, F.M., Sanders, M.C., King, M., Szabolcs, P., Friedman, D., Gomez, F. (1988) Effect of endogenous and synthetic sex steroids on the clearance of antibody-coated cells. J. Immunol. 141, 2959-2966.
10. Flynn, A. (1986) Expression of Ia and the production of interleukin-1 by peritoneal exudate macrophages activated in vivo by steroids. Life Sci. 38, 2455-2460.
11. Polan, M.L., Loukides, J., Nelson, P., Carding, S., Diamond, M., Walsh, A., Bottomly, K. (1989) Progesterone and estradiol modulate interleukin-1β messenger ribonucleic acid levels in cultured human peripheral monocytes. J. Clin. Endocrinol. Metab. 89, 1200-1205.
12. Polan, M.L., Daniele, A., Kuo, A. (1988) Gonadal steroids modulate human monocyte interleukin-1 (IL-1) activity. Fertil. Steril. 49, 964-968.
13. Stock, J.L., Coderre, J.A.., McDonald, B., Rosenwasser, L.J. (1989) Effects of estrogen in vivo and in vitro on spontaneous interleukin-1 release by monocytes from post-menopausal women. J. Clin. Endocrinol. Metab. 68, 364-369.
14. Leung, K.P., Russell, S.W., LeBlanc, P.A., Calballer, S. (1985) Heterogeneity among macrophages cultured from mouse bone marrow. Cell Tissue Res. 239, 693-701.
15. Morrison, D.C., Leive, L. (1975) Fractions of lipopolysaccharide from Escherichia coli 0111:B4 prepared by two extraction procedures. J. Biol. Chem. 250, 2911-2919.
16. Ding, A.H., Nathan, C.F., Stuehr, D.J. (1988) Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: Comparison of activating cytokines and evidence for independent production. J. Immunol. 141, 2407-2412.
17. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Meth. 65, 55-63.
18. Cassady, A.I., Stacey, K.J., Nimmo, K.A., Murphy, K.M., von der Ahe, D., Pearson, D., Botteri, F.M., Nagamine, Y., Hume, D.A. (1991) Constitutive expression of the urokinase plasminogen activator gene in murine RAW 264 macrophages involves distal and 5′ non-coding sequences that are conserved between mouse and pig. Nucl. Acids Res. 19, 6839-6847.
19. Lowenstein, C.J., Alley, E.W., Raval, P., Snowman, A.M., Snyder, S.H., Russell S.W., Murphy W.J. (1993) Macrophage nitric oxide synthase gene: Two upstream regions mediate induction by interferon γ and lipopolysaccharide. Proc. Natl. Acad. Sci. USA 90, 9730-9734.
20. Chen, H.-L., Kamath, R., Pace, J.L., Russell, S.W., Hunt, J.S. (1994) Expression of the interferon-γ receptor gene in mouse placentas is related to stage of gestation and is restricted to specific subpopulations of trophoblast cells. Placenta 15, 109-121.
21. Hou, Q., Gorski, J. (1993) Estrogen receptor and progesterone receptor genes are expressed differentially in mouse embryos during preimplantation development. Proc. Natl. Acad. Sci. USA 90, 9460-9464.
22. Yagel, S., Hurwitz, A., Rosenn, B., Keizer, N. (1987) Progesterone enhancement of prostaglandin E2 production by fetal placental macrophages. Am. J. Reprod. Immunol. Microbiol. 14, 45-48.
23. Marotta, P., Sautebin, L., Di Rosa, M. (1992) Modulation of the induction of nitric oxide synthase by eicosanoids in the marine macrophage cell line J774. Br. J. Pharmacol. 107, 640-641.
24. Schuurs, A.H., Schuurs, W.M., Verhuel, H.A.M. (1990) Effects of gender and sex steroids on the immune response. J. Steroid Biochem. 35, 157-172.
25. Grossman, C.J. (1985) Interactions between the gonadal steroids and the immune system. Science 227, 257-261.
26. McCormack, J.T., Greewald, G.S. (1974) Progesterone and oestradiol-17β concentrations in the peripheral plasma during pregnancy in the mouse. J. Endocrinol. 62, 101-107.
27. Runnebaum, B., Stober, I., Zander, J. (1975) Progesterone, 20α-dihydroprogesterone and 20β-dihydroprogesterone in mother and child at birth. Acta Endocrinol. 80, 569-573.
28. Runnebaum, B., Zander, J. (1971) Progesterone and 20α-dihydroprogesterone in human myometrium during pregnancy. Acta Endocrinol. 66 (Suppl. 150), 1.
29. Frasier-Jessen, M.R., Kovacs, E.J. (1995) Estrogen modulation of JE/monocyte chemoattractant protein-1 mRNA expression in murine macrophages. J. Immunol. 154, 1838-1845.
30. Di Rosa, M., Radomski, M., Carnuccio, R., Moncada, S. (1990) Glucocorticoids inhibit the induction of nitric oxide synthase in macrophages. Biochem. Biophys. Res. Commun. 172, 1246-1251.
31. Chao, T.C., Van Alten, P.J., Greager, J.A.., Walter, R.J. (1991) Effect of female sex hormones on tumor necrosis factor production and oxidative metabolism of rat peritoneal macrophages. J. Leukoc. Biol. (Suppl.) 53
32. Ding, A., Nathan, C.F., Graycar, J., Derynck, R., Stuehr, D.J., Srimal, S. (1990) Macrophage deactivating factor and transforming growth factors-β1 -β2, and -β3 inhibit induction of macrophage nitrogen oxide synthesis by IFN-γ. J. Immunol. 145, 940-944.
33. Al-Ramadi, B.K., Meissler, J.J., Huang, D., Eisenstein, T.K. (1992) Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur. J. Immunol. 22, 2249-2254.
34. McCall, T.B., Palmer, R.M.J., Moncada, S. (1992) Interleukin-8 inhibits the induction of nitric oxide synthase in rat peritoneal neutrophils. Biochem. Biophys. Res. Commun. 186, 680-685.
35. Cunha, F.Q., Moncada, S., Liew, F.Y. (1992) Interleukin-10 (IL-10) inhibits the induction of nitric oxide synthase by interferon-γ in murine macrophages. Biochem. Biophys. Res. Commun. 182, 1155-1159.
36. Vodovotz, Y., Bogdan, C., Paik, J., Xie, Q.-W., Nathan, C. (1993) Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor-β. J. Exp. Med. 178, 605-614.
37. Bogdan, C., Vodovotz, Y., Paik, J., Qiao-wen, X., Nathan, C. (1994) Mechanism of suppression of nitric oxide synthase expression by interleukin-4 in primary mouse macrophages. J. Leukoc. Biol. 55, 227-233.
38. Weusten, J.J., Blankenstein, M.A., Gmelig-Meyling, F.H., Scuurman, H.J., Kater, L., Thijssen, J.H. (1986) Presence of oestrogen receptors in human blood mononuclear cells and thymocytes. Acta Endocrinol. 112, 409-414.
39. Gulshan, S., McCruden, A.B., Stimson, W.H. (1990) Oestrogen receptors in macrophages. Scand. J. Immunol. 31, 691-697.
40. Muroi, M., Muroi, Y., Yamamoto, K., Suzuki, T. (1993) Influence of 3′ half-site sequence of NF-κB motifs on the binding of lipopolysaccharide-activatable macrophage NF-κB proteins. J. Biol. Chem. 268, 19534-19539.
41. Clemens, L.E., Siteri, P.K., Stites, D.P. (1979) Mechanism of immunosuppression of progesterone on maternal lymphocyte activation during pregnancy. J. Immunol. 122, 1978-1985.
42. Von der Ahe, D., Janich, S., Scheidereit, C., Renkawitz, R., Schutz, G., Beato, M. (1985) Glucocorticoid and progesterone receptors bind same sites in two hormonally regulated promoters. Nature 313, 707-709.
43. Cuchacovich, M., Rosa, W., Mena, M., Vanenzuela, C., Gatica, H., Tehernitchin, A.N. (1991) Intraarticular progesterone inhibits 3H-dexamethasone binding to synovial cells from patients with rheumatoid arthritis. A study by dry radioautographic technique. J. Rheumatol. 18, 962-967.
44. Bradley, J., Voorhis, V., Anderson, D.J., Hill, J.A. (1989) The effects of RU486 on immune function and steroid-induced immunosuppression in vitro. J. Clin. Endocrinol. Metab. 69, 1195-1199.
45. Hunt, J.S., Chen, H.L., Yang, Y., Roby, K.F., Garcia, F.U. (1994) Tumor necrosis factor α: Potential relationships with cancers of the female reproductive tract. In Immunobiology of reproduction (J.S. Hunt, ed.), Springer-Verlag, New York, 136-149.
46. Inman, R.D. (1978) Immunologic sex differences and the female predominance in systemic lupus erythematosus. Arthr. Rheumatol. 21, 849-852.
47. Vandenbroucke, J.P., Valkenburg, H.A., Boersma, J.W., Cats, A., Festen, J.J.M., Huber-Bruning, O., Rasker, J.J. (1982) Oral contraceptives and rheumatoid arthritis: further evidence for a preventive effect. Lancet 2, 839-842.