Skip to main content
SpringerLink
Log in

Lipopolysaccharide-induced increases in porcine serum cortisol and progesterone concentrations are not mediated solely by prostaglandin F2α

  • Original Articles
  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

The increase in steroid hormone blood levels in response to bacterial lipopolysaccharide (LPS) appears to be an important mechanism by which mammalian species regulate inflammation. This study examined changes in serum concentrations of cortisol, progesterone, and 13,14-dihydro-15-keto-prostaglandin F2α (PGFM) in diestrous pigs following the intravenous injection of LPS and determined whether indomethacin would attenuate these changes. Serum cortisol and progesterone concentrations increased (P<0.05) within 30 min after the administration of LPS, and the increases in steroid hormones were accompanied by a sharp, transient increase (P<0.05) in PGFM levels. In the presence of indomethacin, serum PGFM levels did not change (P>0.05); however, LPS enhanced (P<0.05) cortisol and progesterone concentrations, although the increases were delayed. Serum concentrations of cortisol acutely increased (P<0.05) immediately following both infusions of indomethacin. In summary, cortisol and progesterone concentrations increased irrespective of serum PGFM concentrations, thereby indicating that prostaglandin F2α was not the sole mediator of LPS-induced changes in cortisol and progesterone concentrations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Culbertson, R., andB. I. Osburn. 1980. The biological effects of bacterial endotoxin: A short review.Vet. Sci. Commun. 4:3–14.

    Google Scholar 

  2. Michalek, S. M., R. N. Moore, J. R. McGhee, D. L. Rosenstreich, andS. E. Mergen-Hagen. 1980. The primary role of lymphoreticular cells in the mediation of host responses to bacterial endotoxin.J. Infect. Dis. 141:55–63.

    PubMed  Google Scholar 

  3. Wright, S. D., R. A. Ramos, P. S. Tobias, R. J. Ulevitch, andJ. C. Mathison. 1990. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein.Science.249:1431–1433.

    PubMed  Google Scholar 

  4. Andersson, J., S. Nagy, L. Bjork, J. Abrams, S. Holm, andU. Andersson. 1992. Bacterial toxin-induced cytokine production studied at the single-cell level.Immunol. Rev. 127:69–96.

    PubMed  Google Scholar 

  5. Nathan, C. F. 1987. Secretory products of macrophages.J. Clin. Invest. 79:319–326.

    PubMed  Google Scholar 

  6. Olson, N. C., W. L. Salzer, andC. E. McCall. 1988. Part 2: Physiological aspects of endotoxemia.Mol. Aspects Med. 10:551–629.

    Google Scholar 

  7. Dinarello, C. A. 1991. The proinflammatory cytokines interleukin-1 and tumor necrosis factor and treatment of the septic shock syndrome.J. Infect. Dis. 163:1177–1184.

    PubMed  Google Scholar 

  8. Wright, L. J., M. B. Lipsett, G. T. Ross, andS. M. Wolff. 1972. Effects of dexamethasone and aspirin on the responses to endotoxin in man.J. Clin. Endocrinol. 34:13–17.

    Google Scholar 

  9. Munck, A., P. M. Guyre, andN. J. Holbrook. 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions.Endocrinol. Rev. 5:25–44.

    Google Scholar 

  10. Gilbert, R. O., W. T. K. Bosu, andA. T. Peter. 1990. The effect ofEscherichia coli endotoxin on luteal function in Holstein heifers.Theriogenology.33:645–651.

    Google Scholar 

  11. Christeff, N., M. C. Auclair, C. Benassayag, A. Carli, andE. A. Nunez. 1987. Endotoxin-induced changes in sex steroid hormone levels in male rats.J. Steroid Biochem. 26:67–71.

    PubMed  Google Scholar 

  12. Richards, R. G., G. W.Almond, and C. A.Smith. 1990. Effects of endotoxemia on steroid and luteinizing hormone concentrations in diestrous gilts. Program of the 11th International Pig Veterinary Society, 1–5 July 1990, at Lausanne, Switzerland. 434.

  13. Stites, D. P., andP. K. Siiteri. 1983. Steroids as immunosuppressants in pregnancy.Immunol. Rev. 75:117–138.

    PubMed  Google Scholar 

  14. Yasuda, N., andM. A. Greer. 1978. Evidence that the hypothalamus mediates endotoxin stimulation of adrenocorticotropic hormone secretion.Endocrinology.102:947–953.

    PubMed  Google Scholar 

  15. Sapolsky, R., C. Rivier, G. Yamamoto, P. Plotsky, andW. Vale. 1987. Interleukin-1 stimulates the secretion of hypothalamic corticotropin-releasing factor.Science. 238:522–524.

    PubMed  Google Scholar 

  16. Bernardini, R., T. C. Kamilaris, A. E. Calogero, E. O. Johnson, M. T. Gomez, P. W. Gold, andG. P. Chrousos. 1990. Interactions between tumor necrosis factor-α, hypothalamic corticotropin-releasing hormone, and adrenocorticotropin secretion in the rat.Endocrinology.126:2876–2881.

    PubMed  Google Scholar 

  17. Navarra, P., S. Tsagarakis, M. S. Faria, L. H. Rees, G. M. Besser, andA. B. Grossman. 1990. Interleukins-1 and -6 stimulate the release of corticotropin-releasing hormone-41 from rat hypothalamus in vitro via the eicosanoid cyclooxygenase pathway.Endocrinology.128:37–44.

    Google Scholar 

  18. Hedge, G. A., andS. D. Hanson. 1972. The effects of prostaglandins on adrenocorticotropin secretion.Endocrinology.91:925–933.

    PubMed  Google Scholar 

  19. Bernardini, R., A. Chiarenza, A. E. Calogero, P. W. Gold, andG. P. Chrousos. 1989. Arachidonic acid metabolites modulate rat hypothalamic corticotropin-releasing hormone secretion in vitro.Neuroendocrinology 50:708–715.

    PubMed  Google Scholar 

  20. Sharp, B. M., andS. G. Matta. 1993. Prostaglandins mediate the adrenocorticotropin response to tumor necrosis factor in rats.Endocrinology 132:269–274.

    PubMed  Google Scholar 

  21. Berghorn, K. A., L. A. Edgerton, G. L. Cromwell, andT. S. Stahly. 1989. Serum progesterone and luteinizing hormone following prostaglandin F2α during the sow's estrous cycle.Anim. Reprod. Sci. 19:273–282.

    Google Scholar 

  22. Gadsby, J. E., C. A. Smith, andG. W. Almond. 1991. Acute stimulatory effects of prostaglandin F2α on serum progesterone concentrations in pregnant and pseudopregnant pigs.Prostaglandins 41:419–432.

    PubMed  Google Scholar 

  23. Mattioli, M., G. Galeati, A. Prandi, andE. Seren. 1985. Effect of PGF-2α on progesterone production in swine luteal cells at different stages of the luteal phase.Prostaglandin Leukotriene Med. 17:43–54.

    Google Scholar 

  24. Wiesak, T., M. G. Hunter, andG. R. Foxcroft. 1992. Effect of prostaglandins in luteal function during early pregnancy in pigs.J. Reprod. Fertil. 95:831–840.

    PubMed  Google Scholar 

  25. Smith, C. A., andM. D. Ficken. 1991. Non-surgical cannulation of the vena cava for chronic blood collection in mature swine.Lab. Anim. Sci. 41:274–278.

    PubMed  Google Scholar 

  26. Almond, G. W., andG. D. Dial. 1990. Steroid hormone and luteinizing hormone concentrations in the anestrous sow.Can. J. Vet. Res. 54:209–214.

    PubMed  Google Scholar 

  27. Smith, C. A., G. W. Almond, andK. L. Esbenshade. 1992. Effects of exogenous estradiol-17β on luteinizing hormone, progesterone, and estradiol-17β concentrations before and after prostaglandin F2α-induced termination of pregnancy and pseudopregnancy in gilts.J. Anim. Sci. 70:518–524.

    PubMed  Google Scholar 

  28. Peter, A. T., W. T. K. Bosu, andR. J. DeDecker. 1989. Suppression of preovulatory luteinizing hormone surges in heifers after intrauterine infusions ofEscherichia coli endotoxin.Am. J. Vet. Res. 50:368–373.

    PubMed  Google Scholar 

  29. Massart-Leen, A. M., C. Burvenich, G. Vandeputte-Van Messom, andH. Hilderson. 1992. Partial prostaglandin-mediated mechanism controlling the release of cortisol in plasma after intravenous administration of endotoxins.Dom. Anim. Endocrinol. 9:273–283.

    Google Scholar 

  30. Santos, A. A., M. R. Scheltinga, E. L. Lynch, E. F. Brown, P. Lawton, E. Chambers, J. Browning, C. A. Dinarello, S. M. Wolff, andD. W. Wilmore. 1993. Elaboration of interleukin 1-receptor antagonist is not attenuated by glucocorticoids after endotoxin.Arch. Surg. 128:138–144.

    Google Scholar 

  31. Shuster, D. E., andR. J. Harmon. 1992. High cortisol concentrations and mediation of the hypogalactia during endotoxin-induced mastitis.J. Dairy Sci. 75:739–746.

    PubMed  Google Scholar 

  32. Polan, M. L., A. Daniele, andA. Kuo. 1988. Gonadal steroids modulate human monocyte interleukin-1 activity.Fertil. Steril. 49:964–968.

    PubMed  Google Scholar 

  33. Snyers, L., L. De Wit, andJ. Content. 1990. Glucocorticoid up-regulation of high-affinity interleukin 6 receptors on human epithelial cells.Proc. Natl. Acad. Sci. U.S.A. 87:2838–2842.

    PubMed  Google Scholar 

  34. Hallford, D. M., R. P. Wettermann, E. J. Turman, andI. T. Omtvedt. 1975. Luteal function in gilts after prostaglandin F2α.J. Anim. Sci. 41:1706–1710.

    PubMed  Google Scholar 

  35. Gadsby, J. E., A. K. Balapure, J. H. Britt, andT. A. Fitz. 1990. Prostaglandin F2α receptors on enzyme-dissociated pig luteal cells throughout the estrous cycle.Endocrinology 126:787–795.

    PubMed  Google Scholar 

  36. Rampacek, G. B., R. R. Kraeling, E. S. Fonda, andC. R. Barb. 1984. Comparison of physiological indicators of chronic stress in confined and nonconfined gilts.J. Anim. Sci. 58:401–408.

    PubMed  Google Scholar 

  37. Richards, R. G., andG. W. Almond. 1990. Endocrine changes associated with endotoxemia in diestrous gilts. Program of the 23rd Annual Meeting of the Society for the Study of Reproduction, 15–18 July 1990, at Knoxville, TN,Biol. Reprod. 42:108.

    Google Scholar 

  38. Kraeling, R. R., G. B. Rampacek, andT. E. Kiser. 1981. Corpus luteum function after indomethacin treatment during the estrous cycle and following hysterectomy in the gilt.Biol. Reprod. 25:511–518.

    PubMed  Google Scholar 

  39. Spinedi, E., M. O. Suescun, R. Hadid, T. Daneva, andR. C. Gaillard. 1992. Effects of gonadectomy and sex hormone therapy on the endotoxin-stimulated hypothalamo-pituitary-adrenal axis: Evidence for a neuroendocrine-immunological sexual dimorphism.Endocrinology 131:2430–2436.

    PubMed  Google Scholar 

  40. Michie, H. R., J. A. Majzoub, S. T. O'Dwyer, A. Revhaug, andD. W. Wilmore. 1990. Both cyclooxygenase-dependent and cyclooxygenase-independent pathways mediate the neuroendocrine response in humans.Surgery 108:254–261.

    PubMed  Google Scholar 

  41. Akira, S., andT. Kishimoto. 1992. IL-6 and NF-IL6 in acute-phase response and viral infection.Immunol. Rev. 127:25–50.

    PubMed  Google Scholar 

  42. Adashi, E. Y., C. E. Resnick, J. N. Packman, A. Hurwitz, andD. W. Payne. 1990. Cytokine-mediated regulation of ovarian function: Tumor necrosis factorα inhibits gonadotro-pin-supported progesterone accumulation by differentiating and luteinized murine granulosa cells.Am. J. Obstet. Gynecol. 162:889–899.

    PubMed  Google Scholar 

  43. Benyo, D. F., andJ. L. Pate. 1992. Tumor necrosis factor-α alters bovine luteal cell synthetic capacity and viability.Endocrinology 130:854–860.

    PubMed  Google Scholar 

  44. Pitzel, L. andW. Wuttke. 1993. Effects and interactions of prostaglandin F2α, oxytocin, and cytokines on steroidogenesis of porcine luteal cells.Endocrinology 132:751–756.

    PubMed  Google Scholar 

  45. Tekpetey, F. R., H. Engelhardt, andD. T. Armstrong. 1993. Differential modulation of porcine theca, granulosa, and luteal cell steroidogenesis in vitro by tumor necrosis factor.Biol. Reprod. 48:936–943.

    PubMed  Google Scholar 

  46. Rivier, C., andW. Vale. 1989. In the rat, interleukin-1α acts at the level of the brain and the gonads to interfere with gonadotropin and sex steroid secretion.Endocrinology 124:2105–2109.

    PubMed  Google Scholar 

  47. Hume, D. A., D. Halpin, H. Charlton, andS. Gordon. 1984. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: Macrophages of endocrine organs.Proc. Natl. Acad. Sci. U.S.A. 81:4174–4177.

    PubMed  Google Scholar 

  48. Adashi, E. Y. 1990. The potential relevance of cytokines to ovarian physiology: The emerging role of resident ovarian cells of the white blood cell series.Endocrinol. Rev. 11:454–464.

    Google Scholar 

  49. Kirsch, T. M., A. C. Friedman, R. L. Vogel, andG. L. Flickinger. 1981. Macrophages in corpora lutea of mice: Characterization and effects on steroid secretion.Biol. Reprod. 25:629–638.

    PubMed  Google Scholar 

  50. Halme, J., M. G. Hammond, C. H. Syrop, andL. M. Talbert. 1985. Peritoneal macrophages modulate human granulosa-luteal cell progesterone production.J. Clin. Endocrinol. Metab. 61:912–916.

    PubMed  Google Scholar 

  51. Chen, T. T., T. A. Lane, M. C. Doody, andM. R. Caudle. 1992. The effect of peritoneal macrophage-derived factor(s) on ovarian progesterone secretion and LH receptors: The role of calcium.Am. J. Reprod. Immunol. 28:43–50.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Food Animal and Equine Medicine College of Veterinary Medicine, North Carolina State University, 27606, Raleigh, North Carolina

    R. Gregg Richards & Glen W. Almond

Authors
  1. R. Gregg Richards
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Glen W. Almond
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Richards, R.G., Almond, G.W. Lipopolysaccharide-induced increases in porcine serum cortisol and progesterone concentrations are not mediated solely by prostaglandin F2α . Inflammation 18, 203–214 (1994). https://doi.org/10.1007/BF01534561

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01534561

Keywords

Search

Navigation