Aglepristone (RU534) effects on luteal function of pseudopregnant rabbits: Steroid receptors, enzymatic activities, and hormone productions in corpus luteum and uterus

Animal Reproduction Science

Volumn 138, Issue 1-2, 2013, Pages 118-132

  Parillo, Francesco ^a   Dall'Aglio, Cecilia ^b   Brecchia, Gabriele ^b   Maranesi, Margherita ^b   Polisca, Angela ^b   Boiti, Cristiano ^b   Zerani, Massimo ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Corpus luteum; Cyclooxygenase; Estrogen receptor; PGE2 9 ketoreductase; Progesterone receptor; Prostaglandins

Indexed keywords

ORYCTOLAGUS CUNICULUS;

15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; AGLEPRISTONE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ESTRANE DERIVATIVE; ESTROGEN RECEPTOR; PROGESTERONE; PROGESTERONE RECEPTOR; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN-E2 9-REDUCTASE;

ANIMAL; BLOOD; CORPUS LUTEUM; ENZYMOLOGY; FEMALE; IMMUNOHISTOCHEMISTRY; LUTEAL PHASE; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY; PSEUDOPREGNANCY; RABBIT; UTERUS; VETERINARY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CORPUS LUTEUM; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; DINOPROST; DINOPROSTONE; ESTRENES; FEMALE; HYDROXYPROSTAGLANDIN DEHYDROGENASES; IMMUNOHISTOCHEMISTRY; LUTEAL PHASE; PROGESTERONE; PSEUDOPREGNANCY; RABBITS; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; STATISTICS, NONPARAMETRIC; UTERUS;

EID: 84880042103     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2013.02.001     Document Type: Article

References (76)

1. Anacker C., Zunszain P.A., Cattaneo A., Carvalho L.A., Garabedian M.J., Thuret S., Price J., Pariante C.M. Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol. Psychiatry 2011, 16:738-750.
2. Anzaldua S.R., Mendoza-Rodríguez C.A., Camacho-Arroyo I., Cerbón M., Pérez-Martínez M. Progesterone receptor immunoreactivity differs in the uterus of pseudopregnant and medroxyprogesterone acetate-treated rabbits. Anim. Reprod. Sci. 2010, 120:173-178.
3. Arck P., Hansen P.J., Mulac Jericevic B., Piccinni M.P., Szekeres-Bartho J. Progesterone during pregnancy: endocrine-immune cross talk in mammalian species and the role of stress. Am. J. Reprod. Immunol. 2007, 58:268-279.
4. Arioua R.K., Feral C., Benhaim A., Delarue B., Leymarie P. Luteotrophic factors in hyperstimulated pseudopregnant rabbit: I-evidence for aromatase activity in luteal tissue and luteal cells. J. Endocrinol. 1997, 154:249-257.
5. Ashley R.L., Arreguin-Arevalo J.A., Nett T.M. Binding characteristics of the ovine membrane progesterone receptor alpha and expression of the receptor during the estrous cycle. Reprod. Biol. Endocrinol. 2009, 7:42.
6. Asakawa M.G., Goldschmidt M.H., Une Y., Nomura Y. The immunohistochemical evaluation of estrogen receptor-alpha and progesterone receptors of normal, hyperplastic, and neoplastic endometrium in 88 pet rabbits. Vet. Pathol. 2008, 45:217-225.
7. Baranda-Avila N., Cardoso-Rangel M.E., Cerbón M., Camacho-Arroyo I., Mendoza-Rodríguez C.A., Villaseñor-Gaona H., Anzaldúa-Arce S.R. Differential expression of estrogen receptor alpha gene in the ampullae and isthmus regions of the rabbit oviduct during early pregnancy. Anim. Reprod. Sci. 2010, 121:286-293.
8. Beyer C., Hoffman K.L., González-Flores O. Neuroendocrine regulation of estrous behavior in the rabbit: similarities and differences with the rat. Horm. Behav. 2007, 52:2-11.
9. Boiti C., Canali C., Zerani M., Gobbetti A. Changes in refractoriness of rabbit corpora lutea to a prostaglandin F2alpha analogue, alfaprostol, during pseudopregnancy. Prostaglandins Other Lipid Mediat. 1998, 56:255-264.
10. Boiti C., Canali C., Brecchia G., Zanon F., Facchin E. Effects of induced endometritis on the life-span of corpora lutea in pseudopregnant rabbits and incidence of spontaneous uterine infections related to fertility of breeding does. Theriogenology 1999, 52:1123-1132.
11. Boiti C., Zampini D., Zerani M., Guelfi G., Gobbetti A. Prostaglandin receptors and role of G protein-activated pathways on corpora lutea of pseudopregnant rabbit in vitro. J. Endocrinol. 2001, 168:141-151.
12. Boiti C., Maranesi M., Dall'Aglio C., Pascucci L., Brecchia G., Gobbetti A., Zerani M. Vasoactive peptides in the luteolytic process activated by PGF2alpha in pseudopregnant rabbits at different luteal stages. Biol. Reprod. 2007, 77:156-164.
13. Bramley T.A., Menzies G.S. Subcellular fractionation of the porcine corpus luteum: sequestration of progesterone in a unique particulate fraction. J. Endocrinol. 1988, 117:341-354.
14. Browning J.Y., Keyes P.F., Wolf R.C. Comparison of serum progesterone, 20α-dihydroprogesterone, and estradiol-17β in pregnant and pseudopregnant rabbits: evidence for postimplantation recognition of pregnancy. Biol. Reprod. 1980, 23:1014-1019.
15. Carlson J.C., Hahn P., So K., Chan A. Studies on prostaglandin and luteolysis in the pseudopregnant rabbit. Endocr. Res. 1990, 16:193-204.
16. Chang C.C., Wang W.C., Bardin C.W. Termination of early pregnancy in the rat, rabbit, and hamster with RU 486 and anordrin. Contraception 1993, 47:597-608.
17. Chen S.H., Dharmarajan A.M., Wallach E.E., Mastroyannis C. RU486 inhibits ovulation, fertilization and early embryonic development in rabbits: in vivo and in vitro studies. Fertil. Steril. 1985, 64:627-633.
18. Chwalisz K., Hegele-Hartung C., Fritzemeier K.H., Beier H.M., Elger W. Inhibition of the estradiol-mediated endometrial gland formation by the antigestagen onapristone in rabbits: relationship to uterine estrogen receptors. Endocrinology 1991, 129:312-322.
19. Clark R.D. Glucocorticoid receptor antagonists. Curr. Top. Med. Chem. 2008, 9:813-838.
20. Condon J.C., Hardy D.B., Kovaric K., Mendelson C.R. Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factor-kappaB may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol. 2006, 20:764-775.
21. Conneely O.M., Mulac-Jericevic B., DeMayo F., Lydon J.P., O'Malley B.W. Reproductive functions of progesterone receptors. Recent Prog. Horm. Res. 2002, 57:339-355.
22. D'Haeseleer M., Simoens P., Van den Broeck W. Cell-specific localization of progesterone receptors in the bovine ovary at different stages of the oestrous cycle. Anim. Reprod. Sci. 2007, 98:271-281.
23. 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.
24. Dharmarajan A.M., Zanagnolo V.L., Dasko L.M., Zirkin B.R., Ewing L.L., Wallach E.E. Estradiol regulation of the rabbit corpus luteum: in vivo and in vitro studies. Endocrinology 1991, 128:2678-2684.
25. Durlej M., Tabarowski Z., Slomczynska M. Immunohistochemical study on differential distribution of progesterone receptor A and progesterone receptor B within the porcine ovary. Anim. Reprod. Sci. 2010, 121:167-173.
26. Gava N., Clarke C.L., Byth K., Arnett-Mansfield R.L., deFazio A. Expression of progesterone receptors A and B in the mouse ovary during the estrous cycle. Endocrinology 2004, 145:3487-3494.
27. Giangrande P.H., McDonnell D.P. The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Recent Prog. Horm. Res. 1999, 54:291-313.
28. Gobbetti A., Boiti C., Canali C., Zerani M. Nitric oxide synthase acutely regulates progesterone production by in vitro cultured rabbit corpora lutea. J. Endocrinol. 1999, 160:275-283.
29. Hegele-Hartung C., Chwalisz K., Beier H.M. Distribution of estrogen and progesteron receptors in the uterus: an immunohistochemical study in the immature and adult pseudopregnant rabbit. Histochemistry 1992, 97:39-50.
30. Hoffman K.L., González-Mariscal G. Progesterone receptor activation signals behavioral transitions across the reproductive cycle of the female rabbit. Horm. Behav. 2006, 50:154-168.
31. Kanayama K., Sankai T., Nariai K., Endo T. Blockade of ovulation in rabbits by RU-486, a competitive progesterone antagonist. J. Vet. Med. Sci. 1996, 58:275-276.
32. Keyes P.L., Kostyo J.L., Towns R. The autonomy of the rabbit corpus luteum. J. Endocrinol. 1994, 143:423-431.
33. Korte J.M., Isola J. An immunocytochemical study of the progesterone receptor in rabbit ovary. Mol. Cell. Endocrinol. 1988, 58:93-101.
34. Kuiper G.G., Carlsson B., Grandien K., Emmark E., Haggblad J., Nilsson S., Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138:863-870.
35. Levine J.E., Chappell P.E., Schneider J.S., Sleiter N.C., Szabo M. Progesterone receptors as neuroendocrine integrators. Front. Neuroendocrinol. 2001, 22:69-106.
36. Li Y.F., Huang C.J., Klindt J., Anderson L.L. Divergent effects of antiprogesterone, RU 486, on progesterone, relaxin, and prolactin secretion in pregnant and hysterectomized pigs with aging corpora lutea. Endocrinology 1991, 129:2907-2914.
37. Lytton F.D.C., Poyser N.L. Concentrations of PGF-2α and PGE-2 in the uterine venous blood of rabbits during pseudopregnancy and pregnancy. J. Reprod. Fertil. 1982, 64:421-429.
38. Maranesi M., Zerani M., Lilli L., Dall'Aglio C., Brecchia G., Gobbetti A., Boiti C. Expression of luteal estrogen receptor, interleukin-1, and apoptosis-associated genes after PGF2alpha administration in rabbits at different stages of pseudopregnancy. Domest. Anim. Endocrinol. 2010, 39:116-130.
39. 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.
40. Mills T.M., Stopper V.S. The intraovarian progesterone modulation of follicle development in the rabbit ovary. Steroids 1989, 54:471-480.
41. Mulac-Jericevic B., Conneely O.M. Reproductive tissue selective actions of progesterone receptors. Reproduction 2004, 128:139-146.
42. Nakamura Y., Tamura H., Ono M., Shimamura K., Sugino N., Numa F., Ueda K., Kato H. A study of the luteolytic mechanism if the antiprogesterone RU486 during the late-luteal phase in pseudopregnant rats. J. Endocrinol. 1996, 150:93-98.
43. Niswender G.D., Juengel J.L., Silva P.J., Rollyson M.K., McIntush E.W. Mechanisms controlling the function and life span of the corpus luteum. Physiol. Rev. 2000, 80:1-29.
44. Ozalp G.R., Cali{dotless}şkan C., Seyrek-İntaş K., Wehrend A. Effects of the progesterone receptor antagonist aglepristone on implantation administered on days 6 and 7 after mating in rabbits. Reprod. Domest. Anim. 2009, 45:505-508.
45. Parillo F., Catone G., Boiti C., Zerani M. Immunopresence and enzymatic activity of nitric oxide synthases, cyclooxygenases and PGE2-9-ketoreductase and in vitro production of PGF2α, PGE2 and testosterone in the testis of adult and prepubertal alpaca (Lama pacos). Gen. Comp. Endocrinol. 2011, 171:381-388.
46. Parillo F., Catone G., Maranesi M., Gobbetti A., Gasparrini B., Russo M., Boiti C., Zerani M. Immunolocalization, gene expression, and enzymatic activity of cyclooxygenases, prostaglandin E2-9-Ketoreductase, and nitric oxide synthases in Mediterranean buffalo (Bubalus bubalis) corpora lutea during diestrus. Microsc. Res. Tech. 2012, 75:1682-1690.
47. Parillo F., Catone G., Gobbetti A., Zerani M. Cell localization of ACTH, dopamine, and GnRH receptors and PPARγ in bovine corpora lutea during diestrus. Acta Sci. Vet. 2013, 41:1129.
48. Peluso J.J. Multiplicity of progesterone's actions and receptors in the mammalian ovary. Biol. Reprod. 2006, 75:2-8.
49. Peluso J.J. Non-genomic actions of progesterone in the normal and neoplastic mammalian ovary. Semin. Reprod. Med. 2007, 25:198-207.
50. Peiró R., Herrler A., Santacreu M.A., Merchán M., Argente M.J., García M.L., Folch J.M., Blasco A. Expression of progesterone receptor related to the polymorphism in the PGR gene in the rabbit reproductive tract. J. Anim. Sci. 2010, 8:421-427.
51. Perrot-Applanat M., Logeat F., Groyer-Picard M.T., Milgrom E. Immunocytochemical study of mammalian progesterone receptor using monoclonal antibodies. Endocrinology 1985, 116:1473-1484.
52. Philibert D., Deraedt R., Teutsch G. RU 38486: a potent antiglucorticoid in vivo. Proceedings of the VII International Congress of Pharmacology 1981, 668.
53. Polisca A., Scotti L., Orlandi R., Brecchia G., Maranesi M., Zerani M., Boiti C. Aglepristone (RU534) administration to non-pregnant bitches in the mid-luteal phase induces early luteal regression. Theriogenology 2010, 74:672-681.
54. Rae M.T., Menzies G.S., McNeilly A.S., Woad K., Webb R., Bramley T.A. Specific non-genomic, membrane-localized binding sites for progesterone in the bovine corpus luteum. Biol. Reprod. 1998, 58:1394-1406.
55. Rekawiecki R., Kowalik M.K., Slonina D., Kotwica J. Regulation of progesterone synthesis and action in bovine corpus luteum. J. Physiol. Pharmacol. 2008, 59:75-89.
56. Rothchild I. The corpus luteum revisited: are the paradoxical effects of RU486 a clue to how progesterone stimulates its own secretion?. Biol. Reprod. 1996, 55:1-4.
57. Sar M., Welsch F. Differential expression of estrogen receptor-beta and estrogen receptor-alpha in the rat ovary. Endocrinology 1999, 140:963-971.
58. Sakumoto R., Vermehren M., Kenngott R.A., Okuda K., Sinowatz F. Changes in the levels of progesterone receptor mRNA and protein in the bovine corpus luteum during the estrous cycle. J. Reprod. Develop. 2010, 56:219-222.
59. Schteingart D.E. Drugs in the medical treatment of Cushing's syndrome. Expert Opin. Emerg. Drugs 2009, 14:661-671.
60. Scott R.S., Rennie P.I.C. Factors controlling the life span of the corpora lutea in the pseudopregnant rabbit. J. Reprod. Fertil. 1970, 23:415-422.
61. Spitz I.M. Progesterone antagonists and progesterone receptor modulators: an overview. Steroids 2003, 68:981-993.
62. Spitz I.M. Mifepristone: where do we come from and where are we going? Clinical development over a quarter of a century. Contraception 2010, 82:442-452.
63. Stocco C., Telleria C., Gibori G. The molecular control of corpus luteum formation, function, and regression. Endocr. Rev. 2007, 28:117-149.
64. Stradaioli G., Verini-Supplizi A., Monaci M., Canali C., Boiti C. Effects of different doses of PMSG on ovarian response and in vitro embryo development in rabbit. World Rabbit Sci. 1997, 3:143-148.
65. Telleria C.M. Can luteal regression be reversed?. Reprod. Biol. Endocrinol. 2006, 4:53.
66. Thomas P. Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol. 2008, 29:292-312.
67. Uilenbroek Th.J., van der Schoot P., Matthej J.A.M., Swarts J.M. Luteolytic and antiluteolytic effect of the antiprogestagen RU486 in pseudopregnant rats. J. Endocrinol. 1995, 145:449-454.
68. Webb R., Woad K.J., Armstrong D.G. Corpus luteum (CL) function: local control mechanism. Domest. Anim. Endocrinol. 2002, 23:277-285.
69. Zailong C., Stocco C. Expression and regulation of progestin membrane receptors in the rat corpus luteum. Endocrinology 2005, 146:5522-5532.
70. Zerani M., Boiti C., Zampini D., Brecchia G., Dall'Aglio C., Ceccarelli P., Gobbetti A. Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. J. Endocrinol. 2004, 183:279-288.
71. Zerani M., Dall'Aglio C., Maranesi M., Gobbetti A., Brecchia G., Mercati F., Boiti C. Intraluteal regulation of prostaglandin F2alpha -induced biosynthesis in pseudopregnant rabbits. Reproduction 2007, 133:1005-1016.
72. Zerani M., Parillo F., Brecchia G., Guelfi G., Dall'Aglio C., Lilli L., Maranesi M., Gobbetti A., Boiti C. Expression of type I GNRH receptor and in vivo and in vitro GNRH-I effects in corpora lutea of pseudopregnant rabbits. J. Endocrinol. 2010, 207:289-300.
73. Zerani M., Catone G., Quassinti L., Maccari E., Bramucci M., Gobbetti A., Maranesi M., Boiti C., Parillo F. In vitro effects of gonadotropin-releasing hormone (GnRH) on Leydig cells of adult alpaca (Lama pacos) testis: GnRH receptor immunolocalization, testosterone and prostaglandin synthesis, and cyclooxygenase activities. Domest. Anim. Endocrinol. 2011, 40:51-59.
74. Zerani M., Catone G., Maranesi M., Gobbetti A., Boiti C., Parillo F. Gonadotropin-releasing hormone 1 directly affects corpora lutea lifespan in mediterranean buffalo (Bubalus bubalis) during diestrus: presence and in vitro effects on enzymatic and hormonal activities. Biol. Reprod. 2012, 87:1-8.
75. Zerani M., Maranesi M., Brecchia G., Gobbetti A., Boiti C., Parillo F. Evidence for a luteotropic role of peroxisome proliferator-activated receptor gamma: expression and in vitro effects on enzymatic and hormonal activities in corpora lutea of pseudopregnant rabbits. Biol. Reprod. 2013, 10.1095/biolreprod.112.107383.
76. Zerani M., Catone G., Betti G., Parillo F. Immunopresence and functional activity of prostaglandin-endoperoxide synthases and nitric oxide synthases in bovine corpora lutea during diestrus. Folia Morphol. 2013, 72:205-216.