Peri-implantation Hormonal Milieu: Elucidating Mechanisms of Abnormal Placentation and Fetal Growth

Overview

Journal Biol Reprod

Publisher Oxford University Press

Specialty Reproductive Medicine

Date 2013 Dec 20

PMID 24352558

Citations 35

Authors

Monica A Mainigi

Devvora Olalere

Irina Burd

Carmen Sapienza

Marisa Bartolomei

Christos Coutifaris

Affiliations

Soon will be listed here.

Abstract

Assisted reproductive technologies (ART) have been associated with several adverse perinatal outcomes involving placentation and fetal growth. It is critical to examine each intervention individually in order to assess its relationship to the described adverse perinatal outcomes. One intervention ubiquitously used in ART is superovulation with gonadotropins. Superovulation results in significant changes in the hormonal milieu, which persist during the peri-implantation and early placentation periods. Epidemiologic evidence suggests that the treatment-induced peri-implantation maternal environment plays a critical role in perinatal outcomes. In this study, using the mouse model, we have isolated the exposure to the peri-implantation period, and we examine the effect of superovulation on placentation and fetal growth. We report that the nonphysiologic peri-implantation maternal hormonal environment resulting from gonadotropin stimulation appears to have a direct effect on fetal growth, trophoblast differentiation, and gene expression. This appears to be mediated, at least in part, through trophoblast expansion and invasion. Although the specific molecular and cellular mechanism(s) leading to these observations remain to be elucidated, identifying this modifiable risk factor will not only allow us to improve perinatal outcomes with ART, but help us understand the pathophysiology contributing to these outcomes.

Citing Articles

High concentration of estrogen resulted by COH may affect the secretion of pro-angiogenic factors in uNK cells by downregulating the expression of IL-11 in decidual stromal cells.

Mu H, Yu H, Yan S, Lu J, Mao J, Sun D J Assist Reprod Genet. 2024; 41(11):3189-3200.

PMID: 39276273 PMC: 11621274. DOI: 10.1007/s10815-024-03241-3.

Transcriptome profiling reveals superovulation with the gonadotropin-releasing hormone agonist trigger impaired embryo implantation in mice.

Li M, Han J, Yang N, Li X, Wu X Front Endocrinol (Lausanne). 2024; 15:1354435.

PMID: 38469140 PMC: 10925639. DOI: 10.3389/fendo.2024.1354435.

Factors affecting superovulation induction in goats (): An analysis of various approaches.

Khan S, Jamal M, Khan I, Ullah I, Jabbar A, Khan N Front Vet Sci. 2023; 10:1152103.

PMID: 37035816 PMC: 10079885. DOI: 10.3389/fvets.2023.1152103.

Ovarian Stimulation in Mice Resulted in Abnormal Placentation through Its Effects on Proliferation and Cytokine Production of Uterine NK Cells.

Ma R, Jin N, Lei H, Dong J, Xiong Y, Qian C Int J Mol Sci. 2023; 24(6).

PMID: 36982985 PMC: 10054838. DOI: 10.3390/ijms24065907.

E2 level > 2950 pg/ml on hCG trigger day is an independent predictor for birthweight loss of full-term singletons born after fresh embryo transfers in non-PCOS patients.

Wu J, Zhang H, Wang X Reprod Biol Endocrinol. 2022; 20(1):162.

PMID: 36411437 PMC: 9677889. DOI: 10.1186/s12958-022-01027-9.

References

Kalra S, Ratcliffe S, Coutifaris C, Molinaro T, Barnhart K . Ovarian stimulation and low birth weight in newborns conceived through in vitro fertilization. Obstet Gynecol. 2011; 118(4):863-71. PMC: 3178887. DOI: 10.1097/AOG.0b013e31822be65f. View

Shiura H, Nakamura K, Hikichi T, Hino T, Oda K, Suzuki-Migishima R . Paternal deletion of Meg1/Grb10 DMR causes maternalization of the Meg1/Grb10 cluster in mouse proximal Chromosome 11 leading to severe pre- and postnatal growth retardation. Hum Mol Genet. 2009; 18(8):1424-38. DOI: 10.1093/hmg/ddp049. View

Garfield A, Cowley M, Smith F, Moorwood K, Stewart-Cox J, Gilroy K . Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature. 2011; 469(7331):534-8. PMC: 3031026. DOI: 10.1038/nature09651. View

Hansen M, Kurinczuk J, Bower C, Webb S . The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med. 2002; 346(10):725-30. DOI: 10.1056/NEJMoa010035. View

Doherty A, MANN M, Tremblay K, Bartolomei M, Schultz R . Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000; 62(6):1526-35. DOI: 10.1095/biolreprod62.6.1526. View

Fortier A, Lopes F, Darricarrere N, Martel J, Trasler J . Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Hum Mol Genet. 2008; 17(11):1653-65. DOI: 10.1093/hmg/ddn055. View

Kim Y, Ku S, Jee B, Suh C, Kim S, Choi Y . Dynamics of early estradiol production may be associated with outcomes of in vitro fertilization. Fertil Steril. 2010; 94(7):2868-70. DOI: 10.1016/j.fertnstert.2010.06.070. View

Farhi J, Ben-Haroush A, Ben Haroush A, Andrawus N, Pinkas H, Sapir O . High serum oestradiol concentrations in IVF cycles increase the risk of pregnancy complications related to abnormal placentation. Reprod Biomed Online. 2010; 21(3):331-7. DOI: 10.1016/j.rbmo.2010.04.022. View

Omland A, Bjercke S, Ertzeid G, Fedorcsak P, Oldereid N, Storeng R . Intracytoplasmic sperm injection (ICSI) in unexplained and stage I endometriosis-associated infertility after fertilization failure with in vitro fertilization (IVF). J Assist Reprod Genet. 2006; 23(7-8):351-7. DOI: 10.1007/s10815-006-9060-2. View

10.

Hubayter Z, Muasher S . Luteal supplementation in in vitro fertilization: more questions than answers. Fertil Steril. 2008; 89(4):749-58. DOI: 10.1016/j.fertnstert.2008.02.095. View

11.

Turan N, Katari S, Gerson L, Chalian R, Foster M, Gaughan J . Inter- and intra-individual variation in allele-specific DNA methylation and gene expression in children conceived using assisted reproductive technology. PLoS Genet. 2010; 6(7):e1001033. PMC: 2908687. DOI: 10.1371/journal.pgen.1001033. View

12.

Gosden R, Trasler J, Lucifero D, Faddy M . Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet. 2003; 361(9373):1975-7. DOI: 10.1016/S0140-6736(03)13592-1. View

13.

Joo B, Park S, An B, Kim K, Moon S, Moon H . Serum estradiol levels during controlled ovarian hyperstimulation influence the pregnancy outcome of in vitro fertilization in a concentration-dependent manner. Fertil Steril. 2009; 93(2):442-6. DOI: 10.1016/j.fertnstert.2009.02.066. View

14.

Chen X, Wen S, Bottomley J, Smith G, Leader A, Walker M . In vitro fertilization is associated with an increased risk for preeclampsia. Hypertens Pregnancy. 2009; 28(1):1-12. DOI: 10.1080/10641950802001859. View

15.

Katari S, Turan N, Bibikova M, Erinle O, Chalian R, Foster M . DNA methylation and gene expression differences in children conceived in vitro or in vivo. Hum Mol Genet. 2009; 18(20):3769-78. PMC: 2748887. DOI: 10.1093/hmg/ddp319. View

16.

Mutter W, Karumanchi S . Molecular mechanisms of preeclampsia. Microvasc Res. 2007; 75(1):1-8. PMC: 2241748. DOI: 10.1016/j.mvr.2007.04.009. View

17.

Scott K, Yamazaki Y, Yamamoto M, Lin Y, Melhorn S, Krause E . Glucose parameters are altered in mouse offspring produced by assisted reproductive technologies and somatic cell nuclear transfer. Biol Reprod. 2010; 83(2):220-7. PMC: 2907285. DOI: 10.1095/biolreprod.109.082826. View

18.

Schieve L, Meikle S, Ferre C, Peterson H, Jeng G, Wilcox L . Low and very low birth weight in infants conceived with use of assisted reproductive technology. N Engl J Med. 2002; 346(10):731-7. DOI: 10.1056/NEJMoa010806. View

19.

Ceelen M, van Weissenbruch M, Prein J, Smit J, Vermeiden J, Spreeuwenberg M . Growth during infancy and early childhood in relation to blood pressure and body fat measures at age 8-18 years of IVF children and spontaneously conceived controls born to subfertile parents. Hum Reprod. 2009; 24(11):2788-95. DOI: 10.1093/humrep/dep273. View

20.

Shapiro B, Daneshmand S, Garner F, Aguirre M, Hudson C, Thomas S . Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: a prospective randomized trial comparing fresh and frozen-thawed embryo transfer in normal responders. Fertil Steril. 2011; 96(2):344-8. DOI: 10.1016/j.fertnstert.2011.05.050. View