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Molecular Research on Embryo Developmental Potential

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Pathology, Diagnostics, and Therapeutics".

Deadline for manuscript submissions: 20 June 2025 | Viewed by 9631

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Dr. Jan Tesarik

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MARGen Clinic, Molecular Assisted Reproducion and Genetics, 18006 Granada, Spain
Interests: human infertility; assisted reproduction; endocrinology; diagnosis; treatment; embryo developmental potential; sperm quality; oocyte quality
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Dear Colleagues,

Embryo developmental potential is an important factor for establishing normal pregnancy in both natural spontaneous reproduction and assisted reproduction treatment (ART) attempts. Since most existing methods of embryo quality evaluation are either too invasive (decreasing the developmental potential even in normal embryos) or not reliable enough, the need for non-invasive methods using molecular biomarkers is evident. This Special Issue is aimed at collecting relevant information on non-invasive molecular biomarkers relevant to embryo developmental potential, both in humans and other mammalian species.

Contributions relating the results of this non-invasive molecular analysis with pregnancy outcomes would be preferred, but any other data on the relationship of molecular biomarkers with embryo health and developmental potential are also welcome. In particular, data explaining the interplay between oocyte and sperm quality are of particular interest.

Finally, new ideas about possible diagnostic and treatment options adapted to particular cases of sperm and oocyte deficiencies in the context of existing ART methods are urgently needed to enable the selection of the best embryos from the available cohort to be transferred into the uterus.

Dr. Jan Tesarik
Guest Editor

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Keywords

embryo developmental potential
oocyte quality
sperm quality
non-invasive techniques
molecular biomarkers

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Research

13 pages, 2836 KiB

Open AccessArticle

Morphokinetic Behavior of the Second Polar Body in Human Zygotes as a Predictor for Embryonic Developmental Potential: An Exploratory Study Based on Time-Lapse Observation

by Toko Shimura, Panagiota Tsounapi, Keitaro Yumoto and Yasuyuki Mio

Int. J. Mol. Sci. 2025, 26(7), 3190; https://doi.org/10.3390/ijms26073190 - 29 Mar 2025

Viewed by 233

Abstract

Time-lapse imaging has made possible the detailed observation of all stages of embryonic development, including also from the extrusion of the second polar body up to the first cleavage. By extensive observation, we achieved detection of a variety of behaviors of PBIIs such as (a) morphologically static behavior, (b) amoeboid movement, (c) shrinking, (d) fragmenting, and (e) ruffling. Retrospective analysis was performed on 282 ICSI zygotes derived from 69 ART treatment cycles from January to August 2019. Zygotes with morphologically static PBIIs (a) and PBIIs showing various behaviors (b)~(e) were classified into Group 1 (n = 70) and Group 2 (n = 212), respectively. Based on the rates of irregular division, good quality embryos, and the time from the PBII extrusion, pronuclear breakdown to the first cleavage was compared between groups (Study 1). Furthermore, the relationship between the type of PBII behaviors and ploidy in 94 biopsied blastocysts from 15 cycles was examined, in which one or more euploid embryos were obtained between August 2021 and July 2024 (Study 2). The results showed that good quality embryos tended to have morphologically static PBIIs, and that euploid embryos were absent in embryos with fragmenting and ruffling PBIIs. The behavior of PBIIs may be a new predictor of embryonic developmental potential, and, in the future, morphokinetic behaviors of PBIIs may be a useful parameter for AI-assisted embryo evaluation systems. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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13 pages, 3872 KiB

Open AccessArticle

Evaluation of Lysophosphatidic Acid Effects and Its Receptors During Bovine Embryo Development

by Bo Yu, Shuying Dai, Lei Cheng, Qirong Lu, Qing Liu and Hongbo Chen

Int. J. Mol. Sci. 2025, 26(6), 2596; https://doi.org/10.3390/ijms26062596 - 13 Mar 2025

Viewed by 445

Abstract

Lysophosphatidic acid (LPA) is a small bioactive phospholipid which plays an important role during embryonic development and promotes developmental potential of in-vitro-produced (IVP) embryos in several species, including sheep and pigs. In bovines, LPA accelerates IVP blastocyst formation through the Hippo/YAP pathway. However, other LPA effects and its potential receptors during bovine embryo development are less clear. In this study, we used enzyme-linked immunosorbent assay (ELISA) to assess the presence of LPA in bovine oviductal fluid and determine cell apoptosis in embryos after LPA stimulation by terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) assay and quantitative reverse transcription polymerase chain reaction (qRT-PCR). We further evaluated potential receptors of LPA through molecular docking, RNA-seq data analysis and quantitative RT-PCR. LPA was found to be present in oviductal fluid. An increase in total cell number and a decrease in apoptosis levels were detected in day 7 blastocysts after LPA treatment. Among eight LPA receptors (LPARs), GPR87 and LPAR2 showed the highest affinity with LPA and their transcripts were expressed in embryos after the 16-cell stage in RNA-seq and qRT-PCR analysis. However, only the expression of LPAR2 was significantly increased in day 6 blastocysts after LPA stimulation, indicating its potential role in LPA-mediated signaling pathways. Our data highlight the positive effects of LPA on embryos and enrich information of related signaling mediators of LPA during embryonic development. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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14 pages, 952 KiB

Open AccessArticle

Metabolomic Biomarkers in Bovine Embryo Culture Media and Their Relationship with the Developmental Potential of In Vitro-Produced Embryos

by Elina Tsopp, Kalle Kilk, Andres Gambini, Ants Kavak, Esta Nahkur, Anni Viljaste-Seera, Haldja Viinalass and Ülle Jaakma

Int. J. Mol. Sci. 2025, 26(5), 2362; https://doi.org/10.3390/ijms26052362 - 6 Mar 2025

Viewed by 646

Abstract

Recent studies have shown that the metabolome of single embryo culture media is linked to successful pregnancy. In this study, the analysis was expanded to compare the metabolomes of viable and non-viable early-stage embryos and to examine metabolomic markers associated with hatching in viable embryos. The authors hypothesized that the metabolomic profiles of high-quality early blastocysts differ from those of non-viable embryos that reach the blastocyst stage but undergo developmental arrest at later stages. The metabolic profile of 43 spent bovine embryo culture medium samples were analyzed using liquid chromatography–mass spectrometry, covering 189 metabolites, including 40 acylcarnitines, 42 amino acids/biogenic amines, 91 phospholipids, 15 sphingolipids, and the sum of hexoses. Embryos were produced from abattoir-derived oocytes, and the culture medium samples were derived from Grade 1 early blastocysts that progressed to hatching (VBL; n = 10), non-viable early blastocysts that developed to the blastocyst stage but failed to hatch (DBL; n = 12), Grade 1 hatched blastocysts (HBL; n = 16), and plain growth media for control (CM; n = 5). It was observed that methionine sulfoxide (Met-SO) and lysophosphatidylcholine (lysoPC) C24:0 concentrations were significantly lower in the culture media from viable blastocysts compared to those from non-viable blastocysts (p < 0.001). Additionally, blastocysts that resulted in successful hatching had significantly lower levels of phospholipid, arginine (Arg), and methionine-related metabolites that significantly differentiated the control and viable blastocyst culture media from the media containing non-viable embryos. Building on previous studies, there appears to be an overlap in metabolites released during hatching that are also associated with successful pregnancy. The identified biomarkers can aid in assessing an embryo’s developmental potential and enhance embryo selection for transfer or cryopreservation. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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18 pages, 7425 KiB

Open AccessArticle

Exploration of Conditions for the Scaled Application of Laparoscopic Ovum Pick-Up in Sheep and Comparison of Follicular Development Differences Among Breeds

by Dongxu Li, Xiangli Wu, Ying Chen, Yangsheng Wu, Gulimire Abudureyimu, Hongyang Liang, Xiuling Ma, Wei Zhang, Liqin Wang and Jiapeng Lin

Int. J. Mol. Sci. 2025, 26(5), 1989; https://doi.org/10.3390/ijms26051989 - 25 Feb 2025

Viewed by 422

Abstract

In small ruminants, laparotomy for ovarian exploration followed by oocyte collection has been progressively replaced by laparoscopic puncture of follicles, which has become an important method for obtaining oocytes in vivo. However, the superovulation protocols and collection frequency used for laparoscopic ovum pick-up (LOPU) in sheep still require further investigation. This study explored the factors influencing LOPU efficiency in sheep, including Controlled Internal Drug Release (CIDR) for estrus synchronization, FSH source and dose, and recovery intervals. The optimal superovulation protocol (using the CIDR device, a total of 16 mg of long-acting recombinant ovine FSH (LR-FSH) administered in two doses, and a one-month interval between LOPU sessions) was subsequently identified. Ovarian follicles were collected via LOPU from Hu sheep and Altay sheep for transcriptomic and metabolomic sequencing to explore interbreed differences in follicular development. The results indicated that LOPU efficiency was significantly higher in the CIDR group (p < 0.05) and with a 30-day recovery interval (p < 0.05). No significant differences in LOPU efficiency were observed between FSH sources or hormone doses. Furthermore, Hu sheep exhibited significantly higher LOPU efficiency and more antral follicles than Altay sheep. Transcriptomic analysis of follicular contents and metabolomic profiling of follicular fluid revealed that differentially expressed genes and metabolites were primarily enriched in pathways related to steroidogenesis, amino acid metabolism, and fatty acid metabolism. This study provides an optimized treatment protocol to enhance LOPU efficiency and integrates multi-omics analyses to elucidate the molecular mechanisms underlying follicular development differences among various breeds. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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19 pages, 5944 KiB

Open AccessArticle

A Comparative Transcriptome and Proteome Analysis of the Molecular Mechanism Underlying Anterior to Dorsal Eye Rotation in the Celestial-Eye Goldfish (Carassius auratus)

by Rongni Li and Yansheng Sun

Int. J. Mol. Sci. 2025, 26(2), 466; https://doi.org/10.3390/ijms26020466 - 8 Jan 2025

Viewed by 728

Abstract

Goldfish (Carassius auratus), subjected to millennia of artificial selection and breeding, have diversified into numerous ornamental varieties, such as the celestial-eye (CE) goldfish, noted for its unique dorsal eye rotation. Previous studies have primarily focused on anatomical modifications in CE goldfish eyes, yet the molecular underpinnings of their distinctive eye orientation remain poorly understood. This study employed high-throughput transcriptome and proteome sequencing on 110-day-old full-sibling CE goldfish, which displayed either anterior or upward eye rotations. Verification of these findings was conducted using quantitative PCR (qPCR) for transcriptomic data and parallel reaction monitoring (PRM) for proteomic analysis. Our research identified 73,685 genes and 7717 proteins, pinpointing 8 common differentially expressed genes (DEGs) and proteins (DEPs) implicated in cytoskeleton remodeling, cell adhesion, apoptosis, and optic nerve regeneration. Enrichment analyses further delineated pathways associated with apoptosis, necroptosis, and cell adhesion molecules. The results indicated a significant role for genes involved in cytoskeletal dynamics, nervous system function, and apoptotic processes in the dorsal eye rotation of CE goldfish. Analyses of abnormalities in ocular membrane structures, along with disturbances in lipid and protein synthesis metabolism and energy metabolism during developmental stages, provided compelling evidence for the potential use of CE goldfish as a model organism in studying human eye-related disorders. This investigation provided the first comprehensive transcriptomic and proteomic overview of eye rotation in CE goldfish, offering insights crucial for the genetic breeding of new ornamental fish varieties. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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18 pages, 7286 KiB

Open AccessArticle

CircTEC Inhibits the Follicular Atresia in Buffalo (Bubalus bubalis) via Targeting miR-144-5p/FZD3 Signaling Axis

by Juanru Cheng, Qinghua Xing, Yu Pan, Yanyan Yang, Ruimen Zhang, Deshun Shi and Yanfei Deng

Int. J. Mol. Sci. 2025, 26(1), 153; https://doi.org/10.3390/ijms26010153 - 27 Dec 2024

Viewed by 770

Abstract

The specific expression profile and function of circular RNA (circRNA) in follicular atresia remain largely unknown. Here, the circRNA expression profiles of granulosa cells derived from healthy follicles (HFs) and antral follicles (AFs) in buffalo were analyzed by RNA-seq, and the mechanism of a differentially expressed circRNA (DEcircRNA) circTEC regulating the granulosa cell function that affects follicular atresia was further explored. RNA-seq results showed that a total of 112 DEcircRNAs were identified. Among them, circTEC was highly expressed in HF, and its circular structure was confirmed by RNase R digestion assay, reversed PCR and Sanger sequencing. Functional experiments demonstrated that circTEC promotes the proliferation and steroid hormone synthesis of buffalo granulosa cells (bGCs), and it also inhibits their apoptosis. In-depth mechanism analysis showed that the expression level of circTEC in bGCs from AFs was adversely related to miR-144-5p and consistent with FZD3. CircTEC acts as an endogenous sponge of miR-144-5p to regulate the expression of the target gene FZD3 in AFs, which promotes the proliferation of bGCs and inhibits bGCs apoptosis, thereby inhibiting follicular atresia in buffalo. In summary, our study revealed the regulatory role of the circTEC/miR-144-5p/FZD3 axis during follicular atresia in buffalo. These results provided new insights into the biological mechanism underlying follicular atresia. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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15 pages, 8668 KiB

Open AccessArticle

Nanopore-Based Sequencing of the Full-Length Transcriptome of Male and Female Cleavage-Stage Embryos of the Chinese Mitten Crab (Eriocheir sinensis)

by Rui Han, Mengqi Ni, Wentao Lu, Dandan Zhu, Tianyi Feng, Yanan Yang and Zhaoxia Cui

Int. J. Mol. Sci. 2024, 25(22), 12097; https://doi.org/10.3390/ijms252212097 - 11 Nov 2024

Viewed by 1064

Abstract

The cleavage stage plays a crucial role in embryo development, characterized by a swift surge in cell proliferation alongside the accurate genetic material transmission to offspring. To delve into the characteristics of sex development during the cleavage stage of embryos, we generated the full-length transcriptome of Eriocheir sinensis male and female cleavage-stage embryos using Oxford Nanopore Technologies (ONT). Notably, this investigation represents the first sequencing effort distinguishing between genders in E. sinensis embryos. In the transcriptome structure analysis, male and female cleavage-stage embryos, while not clustered, exhibited a comparable frequency of alternative splicing (AS) occurrences. We also successfully identified 2875 transcription factors (TFs). The quantitative analysis showed the top 150 genes, in which the highly expressed genes in male embryos predominantly related to protein synthesis and metabolism. Further investigation unveiled 500 differentially expressed genes (DEGs), of which 7 male-biased ribosomal protein genes (RPGs) were particularly noteworthy and further confirmed. These analyses suggest that there may be a more active protein synthesis process in male E. sinensis cleavage-stage embryos. Furthermore, among the 2875 identified TFs, we predicted that 18 TFs could regulate the differentially expressed RPGs, with most TFs belonging to the zf-C2H2 and Homeobox families, which are crucial for embryonic development. During the cleavage stage of E. sinensis, the differential RPGs between genders were intricately linked to energy metabolism. We proposed that these RPGs exert regulatory effects on gene expression in E. sinensis, thereby regulating the difference of development between male and females. Our research sheds light on the developmental mechanisms of E. sinensis during the embryo stage and establishes a groundwork for a deeper understanding of sex development in E. sinensis. The results also provide comprehensive full-length transcriptome data for future gene expression and genetic studies in E. sinensis. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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15 pages, 3023 KiB

Open AccessArticle

Developmental and Molecular Effects of C-Type Natriuretic Peptide Supplementation in In Vitro Culture of Bovine Embryos

by Camila Bortoliero Costa, Nathália Covre da Silva, Amanda Nespolo Silva, Elisa Mariano Pioltine, Thaisy Tino Dellaqua, Amanda Fonseca Zangirolamo, Flávio Vieira Meirelles, Marcelo Marcondes Seneda and Marcelo Fábio Gouveia Nogueira

Int. J. Mol. Sci. 2024, 25(20), 10938; https://doi.org/10.3390/ijms252010938 - 11 Oct 2024

Viewed by 1131

Abstract

The use of C-type natriuretic peptide (CNP) in the interaction with the oocyte and in the temporary postponement of spontaneous meiosis resumption has already been well described. However, its action in pre-implantation developmental-stage embryos is yet to be understood. Thus, our study aimed to detect the presence of the canonical CNP receptor (natriuretic peptide receptor, NPR2) in germinal vesicle (GV)-, metaphase II (MII)-, presumptive zygote (PZ)-, morula (MO)-, and blastocyst (BL)-stage embryos and, later, to observe possible modulations on the embryos when co-cultured with CNP. In Experiment I, we detected and quantified NPR2 on the abovementioned embryo stages. Further, in Experiment II, we intended to test different concentrations (100, 200, or 400 nM of CNP) at different times of inclusion in the in vitro culture (IVC; inclusion from the beginning, i.e., day 1, or from day 5). In Experiment III, 400 nM of CNP was used on day 1 (D1) in the IVC, which was not demonstrated to be embryotoxic, and it showed potentially promising results in the blastocyst production rate when compared to the control. Thus, we analyzed the embryonic development rates of bovine embryos (D7) and hatching kinetics (D7, D8, and D9). Subsequently, morula and blastocyst were collected and evaluated for transcript abundance of their competence and quality (apoptosis, oxidative stress, proliferation, and differentiation) and lipid metabolism. Differences with probabilities less than p < 0.05, and/or fold change (FC) > 1.5, were considered significant. We demonstrate the presence of NPR2 until the blastocyst development stage, when there was a significant decrease in membrane receptors. There was no statistical difference in the production rate after co-culture with 400 nM CNP. However, when we evaluated the abundance of morula transcripts, there was an upregulated transcription in ADCY6 (p = 0.057) and downregulated transcripts in BMP15 (p = 0.013), ACAT1 (p = 0.040), and CASP3 (p = 0.082). In addition, there was a total of 12 transcriptions in morula that presented variation FC > 1.5. In blastocysts, the treatment with CNP induced upregulation in BID, CASP3, SOX2, and HSPA5 transcripts and downregulation in BDNF, NLRP5, ELOVL1, ELOVL4, IGFBP4, and FDX1 transcripts (FC > 1.5). Thus, our study identified and quantified the presence of NPR2 in bovine pre-implantation embryos. Furthermore, 400 nM of CNP in IVC, a concentration not previously described in the literature, modulated some transcripts related to embryonic metabolism, and this was not embryotoxic morphologically. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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17 pages, 10727 KiB

Open AccessArticle

Supraphysiological Dose of Testosterone Impairs the Expression and Distribution of Sex Steroid Receptors during Endometrial Receptivity Development in Female Sprague–Dawley Rats

by Allia Najmie Muhammad Yusuf, Mohd Fariz Amri, Azizah Ugusman, Adila A Hamid and Mohd Helmy Mokhtar

Int. J. Mol. Sci. 2024, 25(18), 10202; https://doi.org/10.3390/ijms251810202 - 23 Sep 2024

Cited by 1 | Viewed by 1167

Abstract

This study aims to investigate the effect of a supraphysiological dose of testosterone on the levels of sex steroid hormones and the expression and distribution of sex steroid receptors in the uterus during the endometrial receptivity development period. In this study, adult female Sprague–Dawley rats (n = 24) were subcutaneously administered 1 mg/kg/day of testosterone alone or in combination with the inhibitors (finasteride or anastrozole or both) from day 1 to day 3 post-coitus, while a group of six untreated rats served as a control group. The rats were sacrificed on the evening of post-coital day 4 of to measure sex steroid hormone levels by ELISA. Meanwhile, gene expression and protein distribution of sex steroid receptors were analysed by quantitative polymerase chain reaction (qPCR) and immunohistochemistry (IHC), respectively. In this study, treatment with a supraphysiological dose of testosterone led to a significant reduction in oestrogen and progesterone levels compared to the control. The mRNA expression of the androgen receptor increased significantly in all treatment groups, while the mRNA expression of both the progesterone receptor and the oestrogen receptor-α decreased significantly in all treatment groups. The IHC findings of all sex steroid receptors were coherent with all mRNAs involved. This study shows that a supraphysiological dose of testosterone was able to interrupt the short period of the implantation window. This finding could serve as a basis for understanding the role of testosterone in endometrial receptivity in order to develop further therapeutic approaches targeting androgen-mediated disorders of endometrial receptivity. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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19 pages, 7320 KiB

Open AccessArticle

miR156-SPL and miR169-NF-YA Modules Regulate the Induction of Somatic Embryogenesis in Arabidopsis via LEC- and Auxin-Related Pathways

by Katarzyna Nowak, Anna M. Wójcik, Katarzyna Konopka, Alicja Jarosz, Katarzyna Dombert and Małgorzata D. Gaj

Int. J. Mol. Sci. 2024, 25(17), 9217; https://doi.org/10.3390/ijms25179217 - 25 Aug 2024

Cited by 2 | Viewed by 2102

Abstract

The embryogenic transition of plant somatic cells to produce somatic embryos requires extensive reprogramming of the cell transcriptome. The prominent role of transcription factors (TFs) and miRNAs in controlling somatic embryogenesis (SE) induction in plants was documented. The profiling of MIRNA expression in the embryogenic culture of Arabidopsis implied the contribution of the miR156 and miR169 to the embryogenic induction. In the present study, the function of miR156 and miR169 and the candidate targets, SPL and NF-YA genes, were investigated in Arabidopsis SE. The results showed that misexpression of MIRNA156 and candidate SPL target genes (SPL2, 3, 4, 5, 9, 10, 11, 13, 15) negatively affected the embryogenic potential of transgenic explants, suggesting that specific fine-tuning of the miR156 and target genes expression levels seems essential for efficient SE induction. The results revealed that SPL11 under the control of miR156 might contribute to SE induction by regulating the master regulators of SE, the LEC (LEAFY COTYLEDON) genes (LEC1, LEC2, FUS3). Moreover, the role of miR169 and its candidate NF-YA targets in SE induction was demonstrated. The results showed that several miR169 targets, including NF-YA1, 3, 5, 8, and 10, positively regulated SE. We found, that miR169 via NF-YA5 seems to modulate the expression of a master SE regulator LEC1/NF-YA and other auxin-related genes: YUCCA (YUC4, 10) and PIN1 in SE induction. The study provided new insights into miR156-SPL and miR169-NF-YA functions in the auxin-related and LEC-controlled regulatory network of SE. Full article

(This article belongs to the Special Issue Molecular Research on Embryo Developmental Potential)

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