Domestic Animal Endocrinology
Volume 39, Issue 2 , Pages 116-130 , August 2010

Expression of luteal estrogen receptor, interleukin-1, and apoptosis-associated genes after PGF administration in rabbits at different stages of pseudopregnancy

  • M. Maranesi

      Affiliations

    • Department of Veterinary Biopathological Science, Laboratory of Biotechnology, Section of Physiology, University of Perugia, Italy
  • ,
  • M. Zerani

      Affiliations

    • School of Veterinary Medicine Science, University of Camerino, Matelica, Italy
  • ,
  • L. Lilli

      Affiliations

    • Department of Veterinary Biopathological Science, Laboratory of Biotechnology, Section of Physiology, University of Perugia, Italy
  • ,
  • C. Dall'Aglio

      Affiliations

    • Section of Anatomy, University of Perugia, Italy
  • ,
  • G. Brecchia

      Affiliations

    • Department of Veterinary Biopathological Science, Laboratory of Biotechnology, Section of Physiology, University of Perugia, Italy
  • ,
  • A. Gobbetti

      Affiliations

    • School of Bioscence and Biotechnology, University of Camerino, Italy
  • ,
  • C. Boiti

      Affiliations

    • Department of Veterinary Biopathological Science, Laboratory of Biotechnology, Section of Physiology, University of Perugia, Italy
    • Corresponding Author InformationAddress correspondence to: Department of Veterinary Biopathological Science, University of Perugia, S. Costanzo 4, I-06126 Perugia, Italy; Phone: +39-075-5857639; Fax: +39-075-5857654

References 

  1. Lytton FDC, Poyser NL. Concentrations of PGF and PGE-2 in the uterine venous blood of rabbits during pseudopregnancy and pregnancy. J Reprod Fertil. 1982;64:421–429
  2. Webb R, Woad KJ, Armstrong DG. Corpus luteum (CL) function: local control mechanism. Domest Anim Endocrinol. 2002;23:277–285
  3. Boiti C, Zerani M, Zampini D, Gobbetti A. Nitric oxide synthase activity and progesterone release by isolated corpora lutea of rabbits in early- and mid-luteal phase of pseudopregnancy are differently modulated by prostaglandin E-2 and prostaglandin F-2α via adenylate cyclase and phospholipase C. J Endocrinol. 2000;164:179–186
  4. Boiti C, Guelfi G, Zampini D, Brecchia G, Gobbetti A, Zerani M. Regulation of nitric-oxide synthase isoforms and role of nitric oxide during prostaglandin F2α-induced luteolysis in rabbits. Reproduction. 2003;125:807–816
  5. Boiti C, Guelfi G, Brecchia G, Dall'Aglio C, Ceccarelli P, Maranesi M, et al. Role of endothelin-1 system in the luteolytic process of pseudopregnant rabbits. Endocrinology. 2005;146:1293–1300
  6. Boiti C, Maranesi M, Dall'Aglio C, Pascucci L, Brecchia G, Gobbetti A, et al. Vasoactive peptides in the luteolytic process activated by PGF2alpha in pseudopregnant rabbits at different luteal stages. Biol Reprod. 2007;77:156–164
  7. Zerani M, Dall'Aglio C, Maranesi M, Gobbetti A, Brecchia G, Mercati F, et al. Intraluteal regulation of prostaglandin F2 alpha-induced prostaglandin biosynthesis in pseudopregnant rabbits. Reproduction. 2007;133:1005–1016
  8. Diaz FJ, Wiltbank MC. Acquisition of luteolytic capacity involves differential regulation by prostaglandin F2α of genes involved in progesterone biosynthesis in the porcine corpus luteum. Domest Anim Endocrinol. 2005;28:172–189
  9. Tsai SJ, Wiltbank MC. Prostaglandin F2α regulates distinct physiological changes in early and mid-cycle bovine corpora lutea. Biol Reprod. 1998;58:346–352
  10. Boiti C, Canali C, Zerani M, Gobbetti A. Changes in refractoriness of rabbit corpora lutea to a prostaglandin F2α analogue, alfaprostol, during pseudopregnancy. Prostaglandins. 1998;56:255–264
  11. Krusche CA, Vloet TD, Herrier A, Black S, Beier HM. Functional and structural regression of the rabbit corpus luteum is associated with altered luteal immune cell phenotypes and cytokine expression patterns. Histochem Cell Biol. 2002;118:479–489
  12. Boiti C, Guelfi G, Zerani M, Zampini D, Brecchia G, Gobbetti A. Expression patterns of cytokines, p53, and nitric oxide synthase isoenzymes in corpora lutea of pseudopregnant rabbits during spontaneous luteolysis. Reproduction. 2004;127:229–238
  13. Del Vecchio RP, Sutherland WD. Prostaglandin and progesterone production by bovine luteal cells incubated in the presence or absence of the accessory cells of the corpus luteum and treated with interleukin-1beta, indomethacin and luteinizing hormone. Reprod Fertil Dev. 1997;9:651–658
  14. Goodman SB, Kugu K, Chen SH, Preutthipan S, Tilly KI, Tilly JL, et al. Estradiol-mediated suppression of apoptosis in the rabbit corpus luteum with a shift in expression of Bcl-2 family members favoring cellular survival. Biol Reprod. 1998;59:820–827
  15. Leon L, Jeannin JF, Bettaieb A. Post-translational modifications induced by nitric oxide (NO): implication in cancer cells apoptosis. Nitric Oxide. 2008;19:77–83
  16. Preutthipan S, Chen SH, Tilly JL, Kugu K, Lareu RR, Dharmarajan AM. Inhibition of nitric oxide synthesis potentiates apoptosis in the rabbit corpus luteum. Reprod Biomed Online. 2004;9:264–270
  17. Dall'Aglio C, Ceccarelli P, Pascucci L, Brecchia G, Boiti C. Receptors for leptin and estrogen in the subcommissural organ of rabbits are differentially modulated by fasting. Brain Res. 2006;1124:62–69
  18. Zerani M, Boiti C, Zampini D, Brecchia G, Dall'Aglio C, Ceccarelli P, et al. Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. J Endocrinol. 2004;183:279–288
  19. Sugino N, Okuda K. Species-related differences in the mechanism of apoptosis during structural luteolysis. J Reprod Dev. 2007;53:977–986
  20. Dharmarajan AM, Goodman SB, Atiya N, Parkinson SP, Lareu RR, Tilly KI, et al. Role of apoptosis in functional luteolysis in the pregnant rabbit corpus luteum: evidence of a role for placental-derived factors in promoting luteal cell survival. Apoptosis. 2004;9:807–814
  21. Nicosia SV, Diaz J, Nicosia RF, Saunders BO, Muro-Cacho C. Cell proliferation and apoptosis during development and aging of the rabbit corpus luteum. Ann Clin Lab Sci. 1995;25:143–157
  22. Schams D, Berisha B. Steroids as local regulators of ovarian activity in domestic animals. Domest Anim Endocrinol. 2002;23:53–65
  23. Monje P, Boland R. Subcellular distribution of native estrogen receptor α and β isoforms in rabbit uterus and ovary. J Cell Biochem. 2001;82:467–479
  24. Yuh KC, Keyes PL. Relationships between estrogen receptor and estradiol-stimulated progesterone synthesis in the rabbit corpus luteum. Biol Reprod. 1982;27:1049–1054
  25. Adashi EY. The potential relevance of cytokines to ovarian physiology: the emerging role of resident ovarian cells of the white blood cell series. Endocrinol Rev. 1990;11:454–464
  26. Bagavandoss P, Wiggins RC, Kunkel SL, Remick DG, Keyes PL. Tumor necrosis factor production and accumulation of inflammatory cells in the corpus luteum of pseudopregnancy and pregnancy in rabbits. Biol Reprod. 1990;42:367–376
  27. Takehara Y, Dharmarajan AM, Kaufman G, Wallach EE. Effect of interleukin 1β on ovulation in the in vitro perfused rabbit ovary. Endocrinology. 1994;134:1788–1793
  28. Bréard E, Delarue B, Benhaïm A, Féral C, Leymarie P. Inhibition by gonadotropins of interleukin-1 production by rabbit granulosa and theca cells: effects on gonadotropin-induced progesterone production. Eur J Endocrinol. 1998;138:328–336
  29. Koering MJ. Luteolysis in normal and prostaglandin F2α-treated pseudopregnant rabbits. J Reprod Fertil. 1974;40:259–267
  30. Estevez A, Tognetti T, Rearte B, Sander V, Motta AB. Interleukin1-beta in the functional luteolysis (Relationship with the nitric oxide system). Prostaglandins Leukot Essent Fatty Acids. 2002;67:411–417
  31. Townson DH, O'Connor CL, Pru JK. Expression of monocyte chemoattractant protein-1 and distribution of immune cell populations in the bovine corpus luteum throughout the estrous cycle. Biol Reprod. 2002;66:361–366
  32. Gérard N, Caillaud M, Martoriati A, Goudet G, Lalmanach AC. The interleukin-1 system and female reproduction. J Endocrinol. 2004;180:203–212
  33. Narko K, Ritvos O, Ristmaki A. Induction of cyclooxygenase-2 and prostaglandin F2α receptor expression by interleukin-1β in cultured human granulose-luteal cells. Endocrinology. 1997;138:3638–3644
  34. Ignarro LJ. Physiology and pathophysiology of nitric oxide. Kidney Int Suppl. 1996;55:S2–S5
  35. Motta AB, Estevez A, Franchi A, Perez-Martinez S, Farina M, Ribeiro ML, et al. Regulation of lipid peroxidation by nitric oxide and PGF during luteal regression in rats. Reproduction. 2001;121:631–637
  36. Cobbs CS, Samanta M, Harkins LE, Gillespie GY, Merrick BA, MacMillan-Crow LA. Evidence for peroxynitrite-mediated modifications to p53 in human gliomas: possible functional consequences. Arch Biochem Biophys. 2001;394:167–172
  37. Taylor BS, Kim YM, Wang Q, Shapiro RA, Billiar TR, Geller D. Nitric oxide down-regulates hepatocyte-inducible nitric oxide synthase gene expression. Arch Surg. 1997;132:1177–1183
  38. Nakamura T, Sakamoto K. Reactive oxygen species up-regulates cyclooxygenase-2, p53, and Bax mRNA expression in bovine luteal cells. Biochem Biophys Res Commun. 2001;284:203–201
  39. Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev. 1994;74:139–162
  40. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 1991;51:6304–6311
  41. Liebermann DA, Hoffman B, Vesely D. p53 induced growth arrest versus apoptosis and its modulation by survival cytokines. Cell Cycle. 2007;6:166–170
  42. Sot B, Freund SM, Fersht AR. Comparative biophysical characterization of p53 with the pro-apoptotic BAK and the anti-apoptotic BCL-xL. J Biol Chem. 2007;282:29193–29200
  43. Lazou A, Iliodromitis EK, Cieslak D, Voskarides K, Mousikos S, Bofilis E, et al. Ischemic but not mechanical preconditioning attenuates ischemia/reperfusion induced myocardial apoptosis in anaesthetized rabbits: the role of Bcl-2 family proteins and ERK1/2. Apoptosis. 2006;11:2195–2204
  44. Li SX, Cui N, Zhang CL, Zhao XL, Yu SF, Xie KQ. Effect of subchronic exposure to acrylamide induced on the expression of bcl-2, bax and caspase-3 in the rat nervous system. Toxicology. 2006;217:46–53
  45. Rueda BR, Tilly KI, Botros IW, Jolly PD, Hansen TR, Hoyer PB, et al. Increased bax and interleukin-1β-converting enzyme messenger ribonucleic acid levels coincide with apoptosis in the bovine corpus luteum during structural regression. Biol Reprod. 1997;56:186–193
  46. Yadav VK, Lakshmi G, Medhamurthy R. Prostaglandin F2alpha-mediated activation of apoptotic signaling cascades in the corpus luteum during apoptosis: involvement of caspase-activated DNase. J Biol Chem. 2005;18280:10357–10367
  47. Gürsoy E, Ergin K, Başaloğlu H, Koca Y, Seyrek K. Expression and localisation of Bcl-2 and Bax proteins in developing rat ovary. Res Vet Sci. 2008;84:56–61
  48. Goyeneche AA, Martinez IL, Deis RP, Gibori G, Telleria CM. In vivo hormonal environment leads to differential susceptibility of the corpus luteum to apoptosis in vitro. Biol Reprod. 2003;68:2322–2330
  49. Riedlinger G, Okagaki R, Wagner KU, Rucker EB, Oka T, Miyoshi K, et al. Bcl-x is not required for maintenance of follicles and corpus luteum in the postnatal mouse ovary. Biol Reprod. 2002;66:438–444
  50. Trott EA, Plouffe L, Hansen K, McDonough PG, George P, Khan I. The role of p53 tumor suppressor gene and bcl-2 protooncogene in rat corpus luteum death. Am J Obstet Gynecol. 1997;177:327–331
  51. Vaskivuo TE, Ottander U, Oduwole O, Isomaa V, Vihko P, Olofsson JI, et al. Role of apoptosis, apoptosis-related factors and 17beta-hydroxysteroid dehydrogenases in human corpus luteum regression. Mol Cell Endocrinol. 2002;194:191–200
  52. Dharmarajan AM, Mastroyannis C, Yoshimura Y, Atlas SJ, Wallach EE, Zirkin BR. Quantitative light microscopic analysis of corpus luteum growth during pseudopregnancy in the rabbit. Biol Reprod. 1988;38:863–870

PII: S0739-7240(10)00037-8

doi: 10.1016/j.domaniend.2010.03.001

Domestic Animal Endocrinology
Volume 39, Issue 2 , Pages 116-130 , August 2010