Embryo-maternal relationships during the periimplantation period - new and old players

This review attempts to integrate available data on embryo-maternal communication during maternal recognition of pregnancy and implantation in the pig. Progesterone (P4) is an essential hormone that makes the uterus receptive to accept conceptuses for implantation and subsequent placentation. As well as P4, the receptive stage of the endometrium is further primed by paracrine factors secreted by the conceptus prior to and during implantation. Oestrogen secretion by elongating conceptuses on days 11 to 12 is necessary for the maternal recognition of pregnancy to protect the corpus luteum from regression. Oestrogens increase the expression of various uterine secretory proteins that are components of the histotroph, which in turn support conceptus growth and implantation. The PGE2 positive feedback loop in the endometrium contributes to an increased PGE2/PGF2α ratio during the peri-implantation period. Greater synthesis of prostacyclin by the uterus, along with activation of the VEGFreceptor system, may be involved in regulating the uterine vascular bed and blood flow, both being prerequisite for sufficient embryo nutrition. HOXA10 expressed by the endometrium may be involved in tissue remodelling and proliferation during conceptus implantation. LIF, IL6 and their receptors are present at the maternal-conceptus interface, and both cytokines increase the attachment and proliferation of trophoblast cells. TGFβ1 stimulates the synthesis of fibronectin, which is necessary for firm adhesion between trophoblast and maternal tissue. Moreover, cytokines regulate a maternal immune response that is permissive for successful pregnancy establishment.

[1]  E. Morawska,et al.  Regulation of prostacyclin synthase expression and prostacyclin content in the pig endometrium. , 2012, Theriogenology.

[2]  E. Morawska,et al.  Regulation of expression and role of leukemia inhibitory factor and interleukin-6 in the uterus of early pregnant pigs. , 2012, Theriogenology.

[3]  A. Fazleabas,et al.  Interaction of the conceptus and endometrium to establish pregnancy in mammals: role of interleukin 1β , 2012, Cell and Tissue Research.

[4]  B. Petroff,et al.  The effect of tumor necrosis factor α (TNFα), interleukin 1β (IL1β) and interleukin 6 (IL6) on endometrial PGF2α synthesis, metabolism and release in early-pregnant pigs. , 2012, Theriogenology.

[5]  E. Morawska,et al.  Effect of conceptus secretions on HOXA10 and PTGS2 gene expression, and PGE2 release in co-cultured luminal epithelial and stromal cells of the porcine endometrium at the time of early implantation. , 2011, Theriogenology.

[6]  M. Kaczmarek,et al.  Mechanisms for the establishment of pregnancy in the pig. , 2011, Reproduction in domestic animals = Zuchthygiene.

[7]  A. Waclawik.  Novel insights into the mechanisms of pregnancy establishment: regulation of prostaglandin synthesis and signaling in the pig. , 2011, Reproduction.

[8]  L. Anderson,et al.  Uterine Progesterone Receptor Expression, Conceptus Development, and Ovarian Function in Pigs Treated with RU 486 During Early Pregnancy1 , 2011, Biology of reproduction.

[9]  B. Wojciechowicz,et al.  Interleukin 1β-induced synthesis and secretion of prostaglandin E₂ in the porcine uterus during various periods of pregnancy and the estrous cycle. , 2010, Journal of physiology and pharmacology : an official journal of the Polish Physiological Society.

[10]  D. Erikson,et al.  Effects of long-term progesterone on developmental and functional aspects of porcine uterine epithelia and vasculature: progesterone alone does not support development of uterine glands comparable to that of pregnancy. , 2010, Reproduction.

[11]  M. Kaczmarek,et al.  Effect of steroids on HOXA10 mRNA and protein expression and prostaglandin production in the porcine endometrium. , 2010, The Journal of reproduction and development.

[12]  M. Kaczmarek,et al.  Endometrial and conceptus expression of HoxA10, transforming growth factor beta1, leukemia inhibitory factor, and prostaglandin H synthase-2 in early pregnant pigs with gonadotropin-induced estrus. , 2010, Domestic animal endocrinology.

[13]  T. Spencer,et al.  Activation of the transcription factor, nuclear factor kappa-B, during the estrous cycle and early pregnancy in the pig , 2010, Reproductive biology and endocrinology : RB&E.

[14]  G. Johnson,et al.  Transforming growth factor beta (TGFB) signaling is activated during porcine implantation: proposed role for latency-associated peptide interactions with integrins at the conceptus-maternal interface. , 2010, Reproduction.

[15]  Kyu-Tae Chang,et al.  Iloprost, a prostacyclin analogue, stimulates meiotic maturation and early embryonic development in pigs. , 2010, Reproduction, fertility, and development.

[16]  H. Jabbour,et al.  Estradiol-17beta, prostaglandin E2 (PGE2), and the PGE2 receptor are involved in PGE2 positive feedback loop in the porcine endometrium. , 2009, Endocrinology.

[17]  Guoyao Wu,et al.  Comparative aspects of implantation. , 2009, Reproduction.

[18]  M. Bogacki,et al.  Effect of the conceptus on uterine prostaglandin-F2alpha and prostaglandin-E2 release and synthesis during the periimplantation period in the pig. , 2009, Reproduction, fertility, and development.

[19]  D. Schams,et al.  Expression of VEGF-receptor system in conceptus during peri-implantation period and endometrial and luteal expression of soluble VEGFR-1 in the pig. , 2009, Theriogenology.

[20]  H. Jabbour,et al.  Estradiol-17 (cid:1) , Prostaglandin E 2 (PGE 2 ), and the PGE 2 Receptor Are Involved in PGE 2 Positive Feedback Loop in the Porcine Endometrium , 2009 .

[21]  D. Schams,et al.  Assessment of VEGF-receptor system expression in the porcine endometrial stromal cells in response to insulin-like growth factor-I, relaxin, oxytocin and prostaglandin E2 , 2008, Molecular and Cellular Endocrinology.

[22]  F. Bazer,et al.  Uterine MHC Class I Molecules and β2-Microglobulin Are Regulated by Progesterone and Conceptus Interferons during Pig Pregnancy1 , 2008, The Journal of Immunology.

[23]  D. Schams,et al.  Expression of the vascular endothelial growth factor‐receptor system in the porcine endometrium throughout the estrous cycle and early pregnancy , 2008, Molecular reproduction and development.

[24]  G. Johnson,et al.  Pig conceptuses secrete estrogen and interferons to differentially regulate uterine STAT1 in a temporal and cell type-specific manner. , 2007, Endocrinology.

[25]  A. Ziecik,et al.  Differential expression of prostaglandin (PG) synthesis enzymes in conceptus during peri-implantation period and endometrial expression of carbonyl reductase/PG 9-ketoreductase in the pig. , 2007, The Journal of endocrinology.

[26]  U. DeSilva,et al.  Expression of Porcine Endometrial Prostaglandin Synthase During the Estrous Cycle and Early Pregnancy, and Following Endocrine Disruption of Pregnancy1 , 2006, Biology of reproduction.

[27]  T. Stadejek,et al.  Expression of cyclooxygenase-1 and -2 in the porcine endometrium during the oestrous cycle and early pregnancy. , 2006, Reproduction in domestic animals = Zuchthygiene.

[28]  B. Murphy,et al.  Modulation of peroxisome proliferator-activated receptor δ and γ transcripts in swine endometrial tissue during early gestation , 2006 .

[29]  L. Brokken,et al.  Molecular cloning and spatiotemporal expression of prostaglandin F synthase and microsomal prostaglandin E synthase-1 in porcine endometrium. , 2006, Endocrinology.

[30]  F. Bazer,et al.  Functional effects of transforming growth factor beta on adhesive properties of porcine trophectoderm. , 2005, Endocrinology.

[31]  T. Krzymowski,et al.  The oestrous cycle and early pregnancy--a new concept of local endocrine regulation. , 2004, Veterinary journal.

[32]  T. Spencer,et al.  Progesterone and Placental Hormone Actions on the Uterus: Insights from Domestic Animals1 , 2004, Biology of reproduction.

[33]  J. Ross,et al.  Characterization of the Interleukin-1β System During Porcine Trophoblastic Elongation and Early Placental Attachment1 , 2003, Biology of reproduction.

[34]  George M Church,et al.  Gene expression profiling reveals progesterone-mediated cell cycle and immunoregulatory roles of Hoxa-10 in the preimplantation uterus. , 2003, Molecular endocrinology.

[35]  R. Einspanier,et al.  Regulation of the VEGF-system in the endometrium during steroid-replacement and early pregnancy of pigs. , 2003, Experimental and clinical endocrinology & diabetes : official journal, German Society of Endocrinology [and] German Diabetes Association.

[36]  T. Modric,et al.  Pregnancy-dependent expression of leukaemia inhibitory factor (LIF), LIF receptor-beta and interleukin-6 (IL-6) messenger ribonucleic acids in the porcine female reproductive tract. , 2000, Placenta.

[37]  Anupma Gupta,et al.  Beta transforming growth factors (TGFβ) at the porcine conceptus- maternal interface. Part II: Uterine TGFβ bioactivity and expression of immunoreactive TGFβs (TGFβ1, TGFβ2, and TGFβ3) and their receptors (type I and type II) , 1998 .

[38]  J. Godkin,et al.  Transforming growth factor β and the endometrium , 1998 .

[39]  I. Anegon,et al.  Presence of leukaemia inhibitory factor and interleukin 6 in porcine uterine secretions prior to conceptus attachment. , 1994, Cytokine.

[40]  G. H. Watson,et al.  Immunocytochemical localization and changes in endometrial progestin receptor protein during the porcine oestrous cycle and early pregnancy. , 1994, Reproduction, fertility, and development.

[41]  F. Bazer,et al.  Production of two species of interferon by Large White and Meishan pig conceptuses during the peri-attachment period. , 1991, Journal of Reproduction and Fertility.

[42]  R. Blair,et al.  Embryonic steroids and the establishment of pregnancy in pigs. , 2020, Journal of reproduction and fertility. Supplement.

[43]  S. Ford,et al.  Direct luteotrophic effect of oestradiol-17β on pig corpora lutea , 1989 .

[44]  R. Seamark,et al.  Steroid hormones in uterine washings and in plasma of gilts between days 9 and 15 after oestrus and between days 9 and 15 after coitus. , 1985, Journal of reproduction and fertility.

[45]  S. Ford,et al.  Local and systemic effects of intrauterine estradiol-17 beta on luteal function of nonpregnant sows. , 1982, Journal of animal science.

[46]  C. Polge,et al.  Oestradiol administration raises luteal LH receptor levels in intact and hysterectomized pigs. , 1982, Journal of reproduction and fertility.

[47]  F. Bazer,et al.  Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium. , 1977, Prostaglandins.