Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos

doi:10.1016/j.theriogenology.2005.09.028

Theriogenology

Volume 65, Issue 1, 7 January 2006, Pages 137-152

https://doi.org/10.1016/j.theriogenology.2005.09.028 Get rights and content

Abstract

It is generally accepted that mammalian preimplantation embryos are sensitive to their environment and that conditions of culture can affect future growth and developmental potential both pre- and postnatally. Evidence suggests that while culture conditions during bovine in vitro embryo production can impact somewhat on the developmental potential of the early embryo, the intrinsic quality of the oocyte is the key factor determining the proportion of oocytes developing to the blastocyst stage. In addition, evidence suggests that the period of post fertilization embryo culture is the most critical period affecting blastocyst quality assessed in terms of cryotolerance, gene expression pattern and ability to establish a pregnancy. This paper reviews the current literature, with emphasis on the bovine model, demonstrating evidence for an effect of post fertilization culture environment on embryo gene expression and quality.

Introduction

It is well recognised that bovine embryos derived in vivo, typically following superovulation, artificial insemination and non-surgical recovery, are of higher quality than those derived from in vitro maturation (IVM) fertilization (IVF) and culture (IVC). The superiority of in vivo derived embryos is reflected in the most recent published data from commercial cattle embryo transfer practice; in excess of half a million bovine embryos were transferred in 2003 [1], of which 82% (478,542) were in vivo derived using superovulation, artificial insemination and embryo recovery, the remaining 18% (106,220) being produced in vitro from oocytes recovered either from the ovaries of slaughtered cattle or using ovum pickup on live animals. More telling is the fact that of the in vivo derived embryos, approximately half (46.4%, 222,019) were transferred frozen compared with only 14% (14,828) of those produced in vitro, reflecting the poorer cryotolerance of such embryos [2].

Typically, in vitro produced embryos have darker cytoplasm and a lower buoyant density [3] as a consequence of their higher lipid content [4], a more fragile zona pellucida [5], reduced expression of intercellular communicative devices [6], differences in metabolism [7], [8] and a higher incidence of chromosome abnormalities [9], [10], [11]. In addition, many differences have been reported at the ultrastructural level [12], [13], [14], [15] which reflect some of the differences noted above. There are also major differences in gene expression patterns which will be discussed below.

The aim of this short review is to highlight the origin of some of the differences in embryos derived in vivo or in vitro and to describe their developmental characteristics. For the most part, the text is restricted to a discussion of development to the blastocyst stage as others will discuss fetal characteristics in more detail [16], [17], [18].

Section snippets

Indicators of embryo quality

Embryo morphology assessment, with all its drawbacks, is at present the most popular method for embryo selection prior to transfer for assisted reproduction in both cattle and humans. The primary criterion for embryo selection after human IVF is the morphological appearance based on a combination of cell number and fragmentation [19]. In the past few years, the possibilities of viable embryo selection at the early cleavage stages have been improved substantially by the introduction of

Role of the post-fertilization culture period—a few days can make a big difference

The in vitro production of cattle embryos is essentially a three-step process involving in vitro oocyte maturation, in vitro fertilization and in vitro culture. In terms of efficiency, in cattle, approximately 90% of immature oocytes, generally recovered from follicles at unknown stages of the oestrous cycle, undergo nuclear maturation in vitro from prophase I to metaphase II (the stage at which they would be ovulated in vivo); about 80% undergo fertilization following insemination and cleave

Conclusions

The early preimplantation period represents a window in development during which the embryo gene expression blueprint may be predisposed to aberrant programming. While embryos can exhibit plasticity in their ability to adapt to what are, in most cases, suboptimal in vitro conditions, their sensitivity to their environment can lead to long-term alterations in the characteristics of foetal and postnatal growth and development. There is now a considerable volume of evidence in the literature,

Acknowledgements

The authors acknowledge the funding agencies which have funded some or all of our original research: Health Research Board and Science Foundation Ireland. In addition, the continued excellent technical assistance of M. Wade and P. Duffy is very much appreciated.

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Periconceptional maternal dietary patterns contribute to embryonic growth and development. No knowledge is available about the impact of periconceptional maternal ultra-processed food consumption on embryonic growth. Therefore, the aim of the present study is to investigate the impact of periconceptional maternal ultra-processed food consumption on embryonic growth using repeated crown-rump length (CRL) and embryonic volume (EV) measurements.
This study is embedded in the ongoing prospective observational Rotterdam periconceptional cohort (Predict Study). A total of 701 pregnancies, of which 446 were conceived after natural conception and 255 after IVF or ICSI treatment were included. Women were at least 18 years of age and were recruited at the outpatient clinic before 13⁺⁰ weeks of gestation. CRL and EV were measured using three-dimensional ultrasound datasets and virtual reality techniques at the 7th, 9th and 11th week of gestation. The food frequency questionnaire of each participant was used to calculate the percentage of maternal energy consumed from ultra-processed foods (PEI-UPF) for each participant. The association between PEI-UPF and the first trimester CRL and EV measurements was studied with linear mixed models and adjusted for potential confounders including maternal factors, gestational age, foetal sex, and total energy intake.
PEI-UPF ranged from 16% to 88%. In fully adjusted linear mixed models, a 10% increase in maternal PEI-UPF was significantly associated with smaller growth trajectories of CRL and EV (b −0.041 √mm (95% confidence interval (CI) −0.074 to −0.008), P = 0.02 and b −0.016 ∛cm (95% CI -0.030 to −0.001), P = 0.04, respectively). When additionally adjusted for micronutrient content of diet (vitamins B1, B2, B6, B11 and B12, and zinc), the associations for the CRL and EV measurements lost significance.
Periconceptional maternal consumption of ultra-processed foods is associated with smaller embryonic growth. Interventions promoting healthy food practices during pregnancy could be beneficial for embryonic growth.
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Citation Excerpt :
Thus, quality refers to not only the morphological appearance, but also to the speed of development. In addition to the kinetics of development, male and female embryos differ in terms of metabolism, gene expression [19,29–31], epigenetic patterns [32], and stress responses [33,34]. Differences in how female and male embryos deal with various types of stress have been reported elsewhere.
Male and female embryos are known to be different in developmental kinetics, metabolism, gene expression, and epigenetic patterns. Therefore, the objective of this study was to clarify whether the morphological criteria used to select embryos for cryopreservation lead to a deviation in the male:female ratio, and whether vitrification effects vary according to embryo sex. Initially, five sires were tested to evaluate the effect of the bull on embryo development, sex ratio, speed of development, and response to cryopreservation. Results showed that bulls affected (P < 0.05) embryo production, response to cryopreservation, and sex ratio. Then, one bull was selected, and used to produce embryos in vitro to characterize the responses of male and female embryos to vitrification. Results suggested that male and female embryos have the same morphological responses to vitrification, as no differences (P > 0.05) were observed between the two sexes in post-warming survival and re-expansion rates. However, their molecular responses as evaluated by gene expression (FOSL1, HSPB1, CASP3, CASP8, HSPA5, HSPA1A, G6PD, and PGK1) analysis indicated an effect of sex on vitrification; vitrified female embryos exhibited higher mRNA levels of HSPA1A, CASP3, and G6PD compared to their male counterparts. In conclusion, bulls affected embryo production, speed of development, sex ratio, and response to cryopreservation. Male and female embryos differed in their molecular responses to vitrification; and also, deviations in the male:female ratio when selecting embryos for cryopreservation were confirmed.
Methylation-reprogrammed AGTR1 results in increased vasoconstriction by angiotensin II in human umbilical cord vessel following in vitro fertilization-embryo transfer
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Assisted reproductive technologies (ART) have been widely used to treat infertility, which may impact on fetuses and offspring. This study investigated the effects of in vitro fertilization-embryo transfer (IVF-ET) on angiotensin II (AII)-mediated vasoconstrictions in umbilical cord vein, and explored possible reprogrammed methylation mechanism.
Human umbilical cords were randomly divided into ordinary pregnancy and IVF-ET pregnancy. Vascular studies with AII as well as its specific receptor antagonists losartan and PD123,319 were conducted. Real-time quantitative PCR, Western blotting, and methylation analysis by bisulfite sequencing were performed with the cord vessel samples.
In IVF-ET group, the maximal response to AII in umbilical vessels was significantly greater than that in the ordinary pregnancy. Using losartan and PD123,319, angiotensin receptor subtype 1 (AT1R) was found mainly responsible for the enhanced contraction in the umbilical vein of IVF-ET pregnancy. Decreased mRNA expression of DNMT3A was found in umbilical vein of IVF-ET group. Hypomethylation of the AGTR1 gene (gene encoding AT1R) in the umbilical veins of the IVF group was found. The data suggested that the IVF-ET treatments altered AII-mediated vasoconstrictions in umbilical veins, which could be partially attributed to the increased expression of AT1R.
The hypo-methylation of the AGTR1 gene caused by IVF-ET might play important roles in altered vasoconstrictions, impacting on cardiovascular systems in the long run.

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Effect of culture environment on gene expression and developmental characteristics in IVF-derived embryos

Abstract

Introduction

Section snippets

Indicators of embryo quality

Role of the post-fertilization culture period—a few days can make a big difference

Conclusions

Acknowledgements

Theriogenology

Theriogenology

Anim Reprod Sci

Theriogenology

Reprod Biomed Online

Reprod Biomed Online

Theriogenology

Theriogenology

J Reprod Immunol

Fertil Steril

Hum Immunol

Reprod Biomed Online

Fertil Steril

Theriogenology

Theriogenology

Anim Reprod Sci

Theriogenology

Anim Reprod Sci

International Embryo Transfer Society: Data Retrieval Committee Annual Report

Embryo Transfer Newsletter

Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality

Mol Reprod Dev

Differences in lipid composition between in vivo- and in vitro-produced bovine embryos [abstract]

Theriogenology

Intracellular communication in in vivo- and in vitro-produced bovine embryos

Biol Reprod

Energy metabolism in preimplantation bovine embryos derived in vitro or in vivo

Biol Reprod

A high proportion of bovine blastocysts produced in vitro are mixoploid

Biol Reprod

Assessing chromosomal abnormalities by FISH analysis in 2-cell bovine embryos derived from in vitro and in vivo fertilization [abstract]

Theriogenology

Effect of the post-fertilization culture environment on the incidence of chromosome aberrations in bovine blastocysts

Biol Reprod

Ultrastructural morphometry of bovine compact morulae produced in vivo or in vitro

Biol Reprod

Ultrastructural morphometry of bovine blastocysts produced in vivo or in vitro

Biol Reprod

Ultrastructure of bovine blastocysts following cryopreservation: effect of method of embryo production on blastocyst quality

Mol Reprod Dev

Developmental, qualitative and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro

Mol Reprod Dev

Development of fetuses from in vitro-produced and cloned bovine embryos

J Anim Sci

Errors in development of fetuses and placentas from in vitro produced bovine embryos

Theriogenology

Calculating the implantation potential of day 3 embryos in women younger than 38 years of age: a new model

Hum Reprod

The morphology of human pronuclear embryos is positively related to blastocyst development and implantation

Hum Reprod

Zygote evaluation: an efficient tool for embryo selection

Hum Reprod

Effect of time interval from insemination to first cleavage on the developmental characteristics, sex and pregnancy rates following transfer of bovine preimplantation embryos

J Reprod Fertil

Fertilization and cleavage of rhesus monkey oocytes in vitro

Biol Reprod

Timing of development is a critical parameter for predicting successful embryogenesis

Hum Reprod

Role of the Ped gene and apoptosis genes in control of preimplantation development

J Assist Reprod Gen

Factors influencing the success of in vitro fertilization for alleviating human infertility

J In Vitro Fert Embryo Transfer

Early cleavage of human embryos: an effective method for predicting successful IVF/ICSI outcome

Hum Reprod

Early cleavage of in-vitro fertilized human embryos to the 2-cell stage: a novel indicator of embryo quality and viability

Hum Reprod

Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro

Hum Reprod

Linkage of the preimplantation-embryo-developent (Ped) gene to the mouse major histocompatibility complex (MHC)

Biol Reprod

Search for the bovine homolog of the murine ped gene and characterization of its messenger RNA expression during bovine preimplantation development

Biol Reprod