Corpus Luteum Regression and Early Pregnancy Maintenance in Pigs

  • Adam J. Ziecik
  • Emilia Przygrodzka
  • Monika M. Kaczmarek


Development of the porcine corpus luteum (CL) requires the initial preovulatory LH surge and support of many biologically active agents including tonic secretion of LH, ovarian steroids, growth factors, and prostaglandins. A lack of embryo presence in the uterus leads to CL regression, characterized by disrupted progesterone production (functional luteolysis) and further degeneration of luteal and endothelial cells (structural luteolysis) triggered by prostaglandin F2α (PGF2α). The porcine CL expresses abundant levels of PGF2α receptors in the early and mid-luteal phase of the estrous cycle but remains insensitive to a single treatment of exogenous PGF2α until about day 12 of the estrous cycle. The nature of porcine CL resistance to PGF2α remains unknown, and the mechanism of luteolytic sensitivity acquisition involves infiltration of immune cells into the CL. Former theories of luteolysis inhibition and maternal recognition of pregnancy in the pig have proposed that possible mechanism for prevention of luteal regression is connected with a limited PGF2α supply to CL, evoked by its sequestering in the uterus. Later studies besides the increased synthesis of prostaglandin E2 (PGE2) by the conceptus and endometrium revealed simultaneously decreased expression of PGF2α synthesis enzymes. This chapter summarizes available knowledge on the porcine CL maintenance and regression and present our recent studies leading to a novel ‘two signal-switch’ hypothesis, based on the interplay of both PGF2α and PGE2 postreceptor signaling pathways. Several practical aspects of how to prolong and enhance CL function and improve pregnancy maintenance are also discussed.


Corpus luteum Luteolytic sensitivity Luteolysis inhibition Pregnancy establishment Embryo signals Prostaglandins Two-switches hypothesis Pig 


  1. 1.
    Alminana C, Heath PR, Wilikson S, Sanchez-Osorio J, Cuello C, Parrilla I, Gil MA, Vazguez JL, Vazguez JM, Roca J, Martinez EA, Fazeli A. Early developing pig embryos mediate their own environment in the maternal tract. PLoS One. 2012;7, e33625.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Bischof RJ, Brandon MR, Lee CS. Cellular immune responses in the pig uterus during pregnancy. J Reprod Immunol. 1995;29:161–78.PubMedCrossRefGoogle Scholar
  3. 3.
    Robertson SA, Mau VJ, Tremellen KP, Seamark RF. Role of high molecular weight seminal vesicle proteins in eliciting the uterine inflammatory response to semen in mice. J Reprod Fertil. 1996;107:265–77.PubMedCrossRefGoogle Scholar
  4. 4.
    Claus R. Physiological role of seminal components in the reproductive tract of the female pig. J Reprod Fertil Suppl. 1990;40:117–31.PubMedGoogle Scholar
  5. 5.
    Lovell JW, Getty R. Fate of semen in the uterus of the sow: histologic study of endometrium during the 27 hours after natural service. Am J Vet Res. 1968;29:609–25.PubMedGoogle Scholar
  6. 6.
    Rozeboom K, Troedsson MH, Crabo BG. Characterization of uterine leukocyte infiltration in gilts after artificial insemination. J Reprod Fertil. 1998;14:195–9.CrossRefGoogle Scholar
  7. 7.
    Bischof RJ, Lee CS, Brandon MR, Meeusen E. Inflammatory response in the pig uterus induced by seminal plasma. J Reprod Immunol. 1994;26:131–46.PubMedCrossRefGoogle Scholar
  8. 8.
    Robertson SA. Seminal fluid signaling in the female reproductive tract: lessons from rodents and pigs. J Anim Sci. 2007;85E(suppl):E36–44.Google Scholar
  9. 9.
    Taylor U, Schuberth HJ, Rath D, Michelmann HW, Sauter-Louis C, Zerbe H. Influence of inseminate components on porcine leucocyte migration in vitro and in vivo after pre and post-ovulatory insemination. Reprod Domestic Anim. 2009;44:180–8.CrossRefGoogle Scholar
  10. 10.
    O’Leary S, Jasper MJ, Warnes GM, Armstrong DT, Robertson SA. Seminal plasma regulates endometrial cytokine expression, leukocyte recruitment and embryo development in the pig. Reproduction. 2004;128:237–47.PubMedCrossRefGoogle Scholar
  11. 11.
    Kaczmarek MM, Krawczynski K, Blitek A, Kiewisz J, Schams D, Ziecik AJ. Seminal plasma affects prostaglandin synthesis in the porcine oviduct. Theriogenology. 2010;74:1207–20.PubMedCrossRefGoogle Scholar
  12. 12.
    Kaczmarek MM, Krawczynski K, Filant J. Seminal plasma affects prostaglandin synthesis and angiogenesis in the porcine uterus. Biol Reprod. 2013;88:72.PubMedCrossRefGoogle Scholar
  13. 13.
    Krawczynski K, Kaczmarek MM. Does seminal plasma affect angiogenesis in the porcine oviduct? Reprod Biol. 2012;12:347–54.PubMedCrossRefGoogle Scholar
  14. 14.
    O’Leary S, Jasper MJ, Robertson SA, Armstrong DT. Seminal plasma regulates ovarian progesterone production, leukocyte recruitment and follicular cell responses in the pig. Reproduction. 2006;132:147–58.PubMedCrossRefGoogle Scholar
  15. 15.
    Hunter RH, Poyser NL. Uterine secretion of prostaglandin F2a in anaesthetized pigs during the oestrous cycle and early pregnancy. Reprod Nutr Dev. 1982;22:1013–23.PubMedCrossRefGoogle Scholar
  16. 16.
    Care AS, Diener KR, Jasper MJ, Brown HM, Ingman WV, Robertson SA. Macrophages regulate corpus luteum development during embryo implantation in mice. J Clin Invest. 2013;123:3472–87.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Waberski D, Dohring A, Ardon F, Ritter N, Zerbe H, Schuberth H-J, Hewicker-Trautwein M, Weitze KF, Hunter RHF. Physiological routes from intra-uterine seminal contents to advancement of ovulation. Acta Vet Scand. 2006;48:13.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Krzymowski T, Stefańczyk-Krzymowska S. The oestrous cycle and early pregnancy-a new concept of local endocrine regulation. Vet J. 2004;168:285–96.Google Scholar
  19. 19.
    Stefańczyk-Krzymowska S, Krzymowski T. Local adjustment of blood and lymph circulation in the hormonal regulation of reproduction in female pigs: facts, conclusions and suggestions for future research. Reprod Biol. 2002;2:115–32.PubMedGoogle Scholar
  20. 20.
    Ziecik AJ, Wacławik A, Kaczmarek MM, Blitek A, Moza Jalali B, Andronowska A. Mechanisms for the establishment of pregnancy in the pig. Reprod Domest Anim. 2011;46(S3):31–41.PubMedCrossRefGoogle Scholar
  21. 21.
    du Du Mesnil Buisson F, Leglise PC. Effet de l’hypophysectomie sue les corps jaunes de la truie. Resultatas preliminaires. C R Hebd Seanc Acad Sci Paris. 1963;257:261–3.Google Scholar
  22. 22.
    Tilton JE, Foxcroft GR, Ziecik AJ, Coombs SL, Williams GL. Time of the preovulatory LH surge in the gilts and sow relative to the onset of behavioral estrus. Theriogeneology. 1982;18:227–36.CrossRefGoogle Scholar
  23. 23.
    Bazer FW, Geisert RD, Thatcher WW, Roberts RM. The establishment and maintenance of pregnancy. In: Cole DJA, Foxcroft GR, editors. Control of pig reproduction. London: Butterworth; 1982. p. 227–53.CrossRefGoogle Scholar
  24. 24.
    Szafranska B, Ziecik A. Active and passive immunization against luteinizing hormone in pigs. Acta Physiol Hung. 1989;74:253–8.PubMedGoogle Scholar
  25. 25.
    Przygrodzka E, Lopinska M, Ziecik AJ. Precision-cut luteal slices: a promising approach for studying luteal function in pigs. Reprod Biol. 2014;14:243–7.PubMedCrossRefGoogle Scholar
  26. 26.
    Conley AJ, Ford SP. Direct luteotrophic effect of oestradiol-17β on pig corpora lutea. J Reprod Fertil. 1989;87:125–31.PubMedCrossRefGoogle Scholar
  27. 27.
    Ford SP, Christenson LK. Direct effects of oestradiol-17β and prostaglandin E2 in protecting pig corpora lutea from a luteolytic dose of prostaglandin F2α. J Reprod Fertil. 1991;93:203–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Geisert RD, Zavy MT, Moffatt RJ, Blair RM, Yellin T. Embryonic steroids and the establishment of pregnancy in pigs. J Reprod Fertil. 1990;40:293–305.Google Scholar
  29. 29.
    Gadsby J, Rose L, Sriperumbudur R, Ge Z. The role of intra-luteal factors in the control of the porcine corpus luteum. In: Ashworth CJ, Kraeling RR, editors. Control of pig reproduction, vol VII, Reproduction. Supplement 62. UK: Nottingham University Press; 2006. p. 69–83.Google Scholar
  30. 30.
    Christenson LK, Farley DB, Anderson LH, Ford SP. Luteal maintenance during early pregnancy in the pig: role for prostaglandin E2. Prostaglandins. 1994;47:61–75.PubMedCrossRefGoogle Scholar
  31. 31.
    Wuttke W, Spiess S, Knoke I, Pitzel L, Leonhardt S, Jarry H. Synergistic effects of prostaglandin F2alpha and tumor necrosis factor to induce luteolysis in the pig. Biol Reprod. 1998;58:1310–5.PubMedCrossRefGoogle Scholar
  32. 32.
    Moeljono MP, Thatcher WW, Bazer FW, Frank M, Owens LJ, Wilcom CJ. A study of prostaglandin F2alpha as the luteolysin in swine: II. Characterization and comparison of prostaglandin F, estrogens and progestin concentrations in utero-ovarian vein plasma of nonpregnant and pregnant gilts. Prostaglandins. 1977;14:543–55.PubMedCrossRefGoogle Scholar
  33. 33.
    Ziecik AJ, Kotwica G. Involvement of gonadotropins in induction of luteolysis in pigs. Reprod Biol. 2001;2001(1):33–50.Google Scholar
  34. 34.
    Carnahan KG, Prince BC, Mirando MA. Exogenous oxytocin stimulates uterine secretion of prostaglandin F2 alpha in cyclic and early pregnant swine. Biol Reprod. 1996;55:838–43.PubMedCrossRefGoogle Scholar
  35. 35.
    Ludwig TE, Sun BC, Carnahan KG, Uzumcu M, Yelich JV, Geisert RD, Mirando MA. Endometrial responsiveness to oxytocin during diestrus and early pregnancy in pigs is not controlled solely by changes in oxytocin receptor population density. Biol Reprod. 1998;58:769–77.PubMedCrossRefGoogle Scholar
  36. 36.
    Waclawik A, Blitek A, Ziecik AJ. Oxytocin and tumor necrosis factor α stimulate expression of prostaglandin E2 synthase and secretion of prostaglandin E2 by luminal epithelial cells of the porcine endometrium during early pregnancy. Reproduction. 2010;140:613–22.PubMedCrossRefGoogle Scholar
  37. 37.
    Blitek A, Ziecik AJ. Role of tumour necrosis factor alpha in stimulation of prostaglandins F(2alpha) and E(2) release by cultured porcine endometrial cells. Reprod Domestic Anim. 2006;41:562–7.CrossRefGoogle Scholar
  38. 38.
    Blitek A, Mendrzycka AU, Bieganska MK, Waclawik A, Ziecik AJ. Effect of steroids on basal and LH-stimulated prostaglandins F(2alpha) and E(2) release and cyclooxygenase-2 expression in cultured porcine endometrial stromal cells. Reprod Biol. 2007;7:73–88.PubMedGoogle Scholar
  39. 39.
    Whiteaker SS, Mirando MA, Becker WC, Hostetler CE. Detection of functional oxytocin receptors on endometrium of pigs. Biol Reprod. 1994;51:92–8.PubMedCrossRefGoogle Scholar
  40. 40.
    Whiteaker SS, Mirando MA, Becker WC, Peters DN. Relationship between phosphoinositide hydrolysis and prostaglandin F2 alpha secretion in vitro from endometrium of cyclic pigs on day 15 postestrus. Domestic Anim Endocrinol. 1995;12:95–104.CrossRefGoogle Scholar
  41. 41.
    Kotwica G, Franczak A, Okrasa S, Kotwica J. Effect of an oxytocin antagonist on prostaglandin F2 alpha secretion and the course of luteolysis in sows. Acta Vet Hung. 1999;47:249–62.PubMedCrossRefGoogle Scholar
  42. 42.
    Gadsby JE, Balapure AK, Britt JH, Fitz TA. Prostaglandin F2 alpha receptors on enzyme-dissociated pig luteal cells throughout the estrous cycle. Endocrinology. 1990;126:787–95.PubMedCrossRefGoogle Scholar
  43. 43.
    Gadsby JE, Lovdal JA, Britt JH, Fitz TA. Prostaglandin F2 alpha receptor concentrations in corpora lutea of cycling, pregnant, and pseudopregnant pigs. Biol Reprod. 1993;49:604–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Diaz FJ, Crenshaw TD, Wiltbank MC. Prostaglandin F(2alpha) induces distinct physiological responses in porcine corpora lutea after acquisition of luteolytic capacity. Biol Reprod. 2000;63:1504–12.PubMedCrossRefGoogle Scholar
  45. 45.
    Diaz FJ, Wiltbank MC. Acquisition of luteolytic capacity: changes in prostaglandin F2alpha regulation of steroid hormone receptors and estradiol biosynthesis in pig corpora lutea. Biol Reprod. 2004;70:1333–9.PubMedCrossRefGoogle Scholar
  46. 46.
    Diaz FJ, Wiltbank MC. Acquisition of luteolytic capacity involves differential regulation by prostaglandin F2alpha of genes involved in progesterone biosynthesis in the porcine corpus luteum. Domestic Anim Endocrinol. 2005;28:172–89.CrossRefGoogle Scholar
  47. 47.
    Diaz FJ, Luo W, Wiltbank MC. Effect of decreasing intraluteal progesterone on sensitivity of the early porcine corpus luteum to the luteolytic actions of prostaglandin F2alpha. Biol Reprod. 2011;841:26–33.CrossRefGoogle Scholar
  48. 48.
    Diaz FJ, Luo W, Wiltbank MC. Prostaglandin F2a regulation of mRNA for activating protein 1 transcriptional factors in porcine corpora lutea (CL): lack of induction of JUN and JUND in CL without luteolytic capacity. Domestic Anim Endocrinol. 2013;44:98–108.CrossRefGoogle Scholar
  49. 49.
    Zorrilla LM, Irvin MS, Gadsby JE. Protein kinase C isoforms in the porcine corpus luteum: temporal and spatial expression patterns. Domestic Anim Endocrinol. 2009;36:173–85.CrossRefGoogle Scholar
  50. 50.
    Zorrilla LM, Sriperumbudur R, Gadsby JE. Endothelin-1, endothelin converting enzyme-1 and endothelin receptors in the porcine corpus luteum. Domestic Anim Endocrinol. 2010;38:75–85.CrossRefGoogle Scholar
  51. 51.
    Luo W, Diaz FJ, Wiltbank MC. Induction of mRNA for chemokines and chemokine receptors by prostaglandin F2a is dependent upon stage of the porcine corpus luteum and intraluteal progesterone. Endocrinology. 2011;152:2797–805.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Przygrodzka E, Witek KJ, Kaczmarek MM, Andronowska A, Ziecik AJ. Expression of factors associated with apoptosis in the porcine 1 corpus luteum throughout the luteal phase of the estrous cycle and early pregnancy: their possible involvement in acquisition of luteolytic sensitivity. Theriogenology. 2015;83:535–45.PubMedCrossRefGoogle Scholar
  53. 53.
    Przygrodzka E, Kaczmarek MM, Kaczyński P, Zięcik AJ. Steroid hormones, prostanoids and angiogenic systems during rescue of the corpus luteum in pigs. Reproduction. 2016;151:135–47.PubMedCrossRefGoogle Scholar
  54. 54.
    Zorrilla LM, D’Annibale MA, Swing SE, Gadsby JE. Expression of genes associated with apoptosis in the porcine corpus luteum during the oestrous cycle. Reprod Domestic Anim. 2013;48:755–61.CrossRefGoogle Scholar
  55. 55.
    Hehnke KE, Christenson LK, Ford SP, Taylor M. Macrophage infiltration into to porcine corpus luteum during prostaglandin F-induced luteolysis. Biol Reprod. 1994;50:10–5.PubMedCrossRefGoogle Scholar
  56. 56.
    Zhao Y, Burbach JA, Roby KF, Terranova PF, Brannian JD. Macrophages are the major source of tumor necrosis factor alpha in the porcine corpus luteum. Biol Reprod. 1998;59:1385–91.PubMedCrossRefGoogle Scholar
  57. 57.
    Perry JS, Heap RB, Amoroso EC. Steroid hormone production by pig blastocysts. Nature (Lond). 1973;245:45–7.CrossRefGoogle Scholar
  58. 58.
    Garverick HA, Polge C, Flint AP. Oestradiol administration raises luteal LH receptor levels in intact and hysterectomized pigs. J Reprod Fertil. 1982;66:371–7.PubMedCrossRefGoogle Scholar
  59. 59.
    Bazer FW, Thatcher WW. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. Prostaglandins. 1977;14:397–400.PubMedCrossRefGoogle Scholar
  60. 60.
    Waclawik A, Jabbour HN, Blitek A, Ziecik AJ. Estradiol-17-beta, prostaglandin E2 (PGE2) and the prostaglandin E2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. Endocrinology. 2009;150:3823–32.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Waclawik A, Ziecik AJ. Differential expression of prostaglandin synthesis enzymes in conceptus during periimplantation period and endometrial expression of carbonyl reductase/prostaglandin 9-ketoreductase in the pig. J Endocrinol. 2007;194:499–510.Google Scholar
  62. 62.
    Geisert RD, Brenner RM, Moffatt J, Harney JP, Yellin T, Bazer FW. Changes in oestrogen receptor protein, mRNA expression and localization in the endometrium of cyclic and pregnant gilts. Reprod Fertil Dev. 1993;5:247–60.PubMedCrossRefGoogle Scholar
  63. 63.
    Kautz E, Gram A, Aslan S, Ay SS, Selçuk M, Kanca H, Koldaş E, Akal E, Karakaş K, Findik M, Boos A, Kowalewski MP. Expression of genes involved in the embryo-maternal interaction in the early-pregnant canine uterus. Reproduction. 2014;8:703–17.CrossRefGoogle Scholar
  64. 64.
    Heap RB, Flint APF, Hartman PE, Gadsby JE, Staples LD, Ackalnd N, Hamon N. Oestrogen production in early pregnancy. J Endocrinol Suppl. 1981;89:77P–94.Google Scholar
  65. 65.
    Frank M, Bazer FW, Thatcher WW, Wilcox CJ. A study of prostaglandin F2alpha as the luteolysin in swine: III effects of estradiol valerate on prostaglandin F, progestins, estrone and estradiol concentrations in the utero-ovarian vein of nonpregnant gilts. Prostaglandins. 1977;14:1183–96.PubMedCrossRefGoogle Scholar
  66. 66.
    Krzymowski T, Czarnocki J, Koziorowski M, Stefańczyk-Krzymowska S. Counter current transfer of 3H-PGF in the mesometrium: a possible mechanism for prevention of luteal regression. Anim Reprod Sci. 1986;11:259–72.CrossRefGoogle Scholar
  67. 67.
    Waclawik A, Rivero-Muller A, Blitek A, Kaczmarek MM, Brokken LJ, Watanabe K, Rahman NA, Ziecik AJ. Molecular cloning and spatio-temporal expression of prostaglandin F synthase and microsomal prostaglandin E synthase-1 in porcine endometrium. Endocrinology. 2006;147:210–21.PubMedCrossRefGoogle Scholar
  68. 68.
    Franczak A, Kotwica G, Kurowicka B, Oponowicz A, Wocławek-Potocka I, Petroff BK. Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E2 and F2α by porcine myometrium during luteolysis and early pregnancy. Theriogenology. 2006;66:1049–56.Google Scholar
  69. 69.
    Davis DL, Blair RM. Studies of uterine secretions and products of primary cultures of endometrial cell in pigs. J Reprod Fertil Suppl. 1993;48:143–55.PubMedGoogle Scholar
  70. 70.
    Akinlosotu BA, Diehl JR, Gimenez T. Sparing effects of intrauterine treatment with prostaglandin E2 on luteal function in cycling gilts. Prostaglandins. 1986;32:291–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Schneider TM, Tilton JE, Okrasa S, Mah J, Weigl RM, Williams GL. The effect of intrauterine infusions of prostaglandin E2 on luteal function in nonpregnant gilts. Theriogenology. 1983;20:509–20.PubMedCrossRefGoogle Scholar
  72. 72.
    Okrasa S, Tilton JE, Weigl RM. Utero-ovarian venous concentrations of prostaglandin E2 (PGE2) and prostaglandin F2a (PGF2a) following PGE2 intrauterine infusions. Prostaglandins. 1985;30:851–6.PubMedCrossRefGoogle Scholar
  73. 73.
    Stefanczyk-Krzymowska S, Wasowska B, Chłopek J, Gilun P, Grzegorzewski W, Radomski M. Retrograde and local destination transfer of uterine prostaglandin E2 in early pregnant sow and its physiological consequences. Prostaglandins Other Lipid Mediat. 2006;81:71–9.PubMedCrossRefGoogle Scholar
  74. 74.
    Engmann L, Losel R, Wehling M, Peluso JJ. Progesterone regulation of human granulose/luteal cell viability by an RU486-independent mechanism. J Clin Endocrinol Metab. 2006;91:4962–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Geisert RD, Yelich JV. Regulation of conceptus development and attachment in pigs. J Reprod Fertil Suppl. 1997;52:133–49.PubMedGoogle Scholar
  76. 76.
    Waclawik A, Kaczmarek MM, Kowalczyk AE, Bogacki M, Ziecik AJ. Expression of prostaglandin synthesis pathway enzymes in the porcine corpus luteum during the oestrous cycle and early pregnancy. Theriogenology. 2008;70:145–52.Google Scholar
  77. 77.
    Spencer TE, Forde N, Dorniak P, Hansen TR, Romero JJ, Lonergan P. Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction. 2013;146:377–87.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Seo H, Choi Y, Shim J, Yoo I, Ka H. Prostaglandin transporters ABCC4 and SLCO2A1 in the uterine endometrium and conceptus during pregnancy in pigs. Biol Reprod. 2014;90:1–10.CrossRefGoogle Scholar
  79. 79.
    Wasielak M, Kaminska K, Bogacki M. Effect of the conceptus on uterine prostaglandin-F2α and prostaglandin-E2 release and synthesis during the periimplantation period in the pig. Reprod Fertil Dev. 2009;21:1–9.CrossRefGoogle Scholar
  80. 80.
    Wiepz GL, Wiltbank MC, Nett TM, Niswender GD, Sawyer HR. Receptors for prostaglandin F2 alpha and E2 in ovine corpora lutea during maternal recognition of pregnancy. Biol Reprod. 1992;47:984–91.Google Scholar
  81. 81.
    Davis JS, Rueda BR. The corpus luteum: an ovarian structure with maternal instincts and suicidal tendencies. Front Biosci. 2002;7:1949–78.CrossRefGoogle Scholar
  82. 82.
    Zannoni A, Bernardini C, Rada T, Ribeiro LA, Forni M, Bacci ML. Prostaglandin F2-alpha receptor (FPr) expression on porcine corpus luteum microvascular endothelial cells (pCL-MVECs). Reprod Biol Endocrinol. 2007;5:31.Google Scholar
  83. 83.
    Shirasuna K, Akabane Y, Beindorff N, Nagai K, Sasaki M, Shimizu T, Bollwein H, Meidan R, Miyamoto A. Expression of prostaglandin F2α (PGF2α) receptor and its isoforms in the bovine corpus luteum during the estrous cycle and PGF2α-induced luteolysis. Domestic Anim Endocrinol. 2012;43:227–38.Google Scholar
  84. 84.
    Zalman Y, Klipper E, Farberov S, Mondal M, Wee G, Folger JK, Smith GW, Meidan R. Regulation of angiogenesis-related prostaglandin F2alpha-induced genes in the bovine corpus luteum. Biol Reprod. 2012;86:1–10.CrossRefGoogle Scholar
  85. 85.
    Waclawik A. Novel insights into the mechanisms of pregnancy establishment: regulation of prostaglandin synthesis and signaling in the pig. Reproduction. 2011;142:389–99.PubMedCrossRefGoogle Scholar
  86. 86.
    Lee JH, McCracken JA, Stanley JA, Nithy TK, Banu SK, Arosh JA. Intraluteal prostaglandin biosynthesis and signaling are selectively directed towards PGF2α during luteolysis but towards PGE2 during the establishment of pregnancy in sheep. Biol Reprod. 2012;87:1–14.CrossRefGoogle Scholar
  87. 87.
    Mamluk R, Defer N, Hanoune J, Meidan R. Molecular identification of adenyl cyclase 3 in bovine corpus luteum and its regulation by prostaglandin F2α-induced signaling pathways. Endocrinology. 1999;140:4601–8.PubMedGoogle Scholar
  88. 88.
    Bos CL, Richel DJ, Ritsema T, Peppelenbosch MP, Versteeg HH. Prostanoids and prostanoid receptors in signal transduction. Int J Biochem Cell Biol. 2004;36:1187–205.PubMedCrossRefGoogle Scholar
  89. 89.
    Hsi LC, Eling TE. Inhibition of EGF-dependent mitogenesis by prostaglandin E2 in Syrian hamster embryo fibroblasts. Prostag Leukotr Essent Fatty Acids. 1998;58:271–81.CrossRefGoogle Scholar
  90. 90.
    Kowalczyk AE, Kaczmarek MM, Schams D, Ziecik AJ. Effect of prostaglandin E(2) and tumor necrosis factor alpha on the VEGF-receptor system expression in cultured porcine luteal cells. Mol Reprod Dev. 2008;75:1558–66.PubMedCrossRefGoogle Scholar
  91. 91.
    Kaczmarek MM, Kiewisz J, Schams D, Ziecik AJ. Expression of VEGF-receptor system in conceptus during peri-implantation period and endometrial and luteal expression of soluble VEGFR-1 in the pig. Theriogenology. 2009;71:1298–306.PubMedCrossRefGoogle Scholar
  92. 92.
    Taniguchi H, Komiyama J, Viger RS, Okuda K. The expression of the nuclear receptors NR5A1 and NR5A2 and transcription factor GATA6 correlates with steroidogenic gene expression in the bovine corpus luteum. Mol Reprod Dev. 2009;76:873–80.PubMedCrossRefGoogle Scholar
  93. 93.
    Hughes AL, Powell DW, Bard M, Eckstein J, Barbuch R, Link AJ. Dap1/PGRMC1 binds and regulates cytochrome P450 enzymes. Cell Metab. 2007;5:143–9.PubMedCrossRefGoogle Scholar
  94. 94.
    Lambert E, Williams DH, Lynch PB, Hanrahan TJ, McGeady TA, Austin FH, Boland MP, Roche JF. The extent and timing of prenatal loss in gilts. Theriogenology. 1991;36:655–65.PubMedCrossRefGoogle Scholar
  95. 95.
    Jindal R, Cosgrove JR, Foxcroft GR. Progesterone mediates nutritionally induced effects on embryonic survival in gilts. J Anim Sci. 1997;75:1063–70.PubMedCrossRefGoogle Scholar
  96. 96.
    Day BN, Pologe C. Effects of progesterone on fertilization and egg transport in the pig. J Reprod Fertil. 1968;17:227–30.PubMedCrossRefGoogle Scholar
  97. 97.
    Mao J, Foxcroft GR. Progesterone therapy during early pregnancy and embryonal survival in primiparous weaned sows. J Anim Sci. 1998;76:1922–8.PubMedCrossRefGoogle Scholar
  98. 98.
    Bolzan E, Andronowska A, Bodek G, Morawska-Pucinska E, Krawczynski K, Dabrowski A, Ziecik AJ. The novel effect of hCG administration on luteal function maintenance during the estrous cycle/pregnancy and early embryo development in the pig. Pol J Vet Sci. 2013;116:323–32.Google Scholar
  99. 99.
    Guthrie HD, Bolt DJ. Changes in plasma estrogen, luteinizing hormone, follicle stimulating hormone and 13,14-dihydro-15-ketoprostaglandin F2α during blockade of luteolysis in pigs after human chorionic gonadotropin treatment. J Anim Sci. 1983;52:993–1000.CrossRefGoogle Scholar
  100. 100.
    Ellicott AR, Dziuk PJ. Minimum daily dose of progesterone and plasma concentration for maintenance of pregnancy in ovariectomized gilts. Biol Reprod. 1973;9:300–4.PubMedGoogle Scholar
  101. 101.
    Tilton JE, Schmidt AE, Weigl RM, Ziecik AJ. Ovarian steroid secretion changes after hCG stimulation in early pregnant pigs. Theriogenology. 1989;32:623–31.PubMedCrossRefGoogle Scholar
  102. 102.
    Stone BA, Heap PA, Seamark RF. Changes in peripheral progestagen levels in early pregnant gilts following injection of human chorionic gonadotrophin. J Endocrinol. 1987;115:161–7.PubMedCrossRefGoogle Scholar
  103. 103.
    Khan TH, Beck NF, Khalid M. The effects of GnRH analogue (buserelin) or hCG (Chorulon) on day 12 of pregnancy on ovarian function, plasma hormone concentrations, conceptus growth and placentation in ewes and ewe lambs. Anim Reprod Sci. 2007;102:247–57.PubMedCrossRefGoogle Scholar
  104. 104.
    Rajamahendran R, Sianangama PC. Effect of human chorionic gonadotrophin on dominant follicles in cows: formation of accessory corpora lutea, progesterone production and pregnancy rates. J Reprod Fertil. 1992;95:577–84.PubMedCrossRefGoogle Scholar
  105. 105.
    Chłopek J, Gilun P, Tabęcka Łonczyńska A, Koziorowski M, Stefańczyk-Krzymowska S. The effect of intravaginal application of estradiol and progesterone on porcine embryo development. Pol J Vet Sci. 2008;11(4):287–93.PubMedGoogle Scholar
  106. 106.
    Pope WF, Lawyer MS, Butler WR, Foote RH, First NL. Dose-response shift in the ability of gilts to remain pregnant following exogenous estradiol-17beta exposure. J Anim Sci. 1986;63:1208–10.PubMedCrossRefGoogle Scholar
  107. 107.
    Webel SK, Reimers TJ, Dziuk PJ. The lack of relationship between plasma progesterone levels and number of embryos and their survival in the pig. Biol Reprod. 1975;13:177–86.PubMedCrossRefGoogle Scholar
  108. 108.
    Ziecik AJ, Lopinska M, Przygrodzka E, Wasielak M, Kempa W. Effect of hCG and intravaginal application of estradiol and prostaglandin E2 on pregnancy rate and litter size in gilts and sows. Anim Sci Pap Rep. 2014;32:5–13.Google Scholar
  109. 109.
    Geisert RD, Zavy MT, Wettemenn RP, Biggers BG. Length of pseudopregnancy and pattern of uterine protein release and influenced by time and duration of oestrogen administration in the pig. J Reprod Fertil. 1987;79:163–72.PubMedCrossRefGoogle Scholar
  110. 110.
    Kidder HE, Casida LE, Grummer RH. Some effects of estrogen injections on estrual cycle of gilts. J Anim Sci. 1995;14:470–4.CrossRefGoogle Scholar
  111. 111.
    Pusateri AE, Wilson ME, Diekman MA. Maternal recognition of pregnancy in swine. II. Plasma concentrations of progesterone and 13,14-dihydro-15-keto-prostaglandin F2 alpha during the estrous cycle and during short and long pseudopregnancy in gilts. Biol Reprod. 1996;55(3):590–7.PubMedCrossRefGoogle Scholar
  112. 112.
    Ziecik A, Doboszynska T, Dusza L. Concentrations of LH, prolactin and progesterone in early-pregnant and oestradiol treated pigs. Anim Reprod Sci. 1986;10:215–24.CrossRefGoogle Scholar
  113. 113.
    Przygrodzka E, Andronowska A, Janowski T, Zięcik AJ. The effect of vaginal administration of prostaglandin (PG) E2 and/or 17β-estradiol (E2) 1 on luteal function and histological characteristics of the cervix in cyclic pigs. Pol J Vet Sci. 2014;17:123–30.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Adam J. Ziecik
    • 1
  • Emilia Przygrodzka
    • 1
  • Monika M. Kaczmarek
    • 1
  1. 1.Department of Hormonal Action Mechanisms/Molecular Biology LaboratoryInstitute of Animal Reproduction and Food Research of Polish Academy of SciencesOlsztynPoland

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