Recent Advancements in Mammalian Embryo Culture: From Animal Models to Humans

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Reproductive Cells and Development".

Deadline for manuscript submissions: closed (30 April 2024) | Viewed by 7030

Special Issue Editors


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Guest Editor
Department of Biology, University of Naples “Federico II”, Complesso Universitario di Monte S. Angelo, Via Cinthia, 80126 Naples, Italy
Interests: andrology; sperm-oviduct interaction; cryopreservation of reproductive cells and tissues; in vitro folliculogenesis; fertilization; reproductive biotechnologies; dynamic organ culture of ovarian tissue; dynamic embryo culture

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Guest Editor
Department of Biology, University of Naples Federico II, Via Cinthia, 80126 Naples, Italy
Interests: reproductive biology; human clinical embryology; sperm biology; ovarian biology; oxidative stress; female fertility preservation

E-Mail Website
Guest Editor
Department of Biology, University of Naples Federico II, Via Cinthia, 80126 Naples, Italy
Interests: tissue engineering; microfluidics; 3D culture; reproductive biology; ovarian tissue culture

Special Issue Information

Dear Colleagues,

Animal models have provided clear evidence that embryos developed in vitro have reduced abilities to implant, develop to term, and give rise to healthy offspring compared to their in vivo counterparts. In vivo, embryos develop in submicroliter volumes of maternal fluids secreted by cells lining the virtual cavities of the oviduct and uterus, while the embryo is transported by ciliary metachronal waves and organ peristaltic contractions. During transport, the developing embryo communicates with oviduct epithelial cells and the endometrium through secreted factors, exosomes, and direct cell–cell interactions that influence embryo competence, oviduct function, and endometrial receptivity. This scenario has led some research groups to attempt to mimic such an environment in vitro using either static or dynamic culture systems. Recently, assisted reproductive techniques (ARTs) in humans and mammalian animal models, combined with non-invasive assessments such as morphokinetics, metabolomics, gene expression, and others, have greatly contributed to our understanding of mammalian preimplantation embryo development and provided promising avenues for overcoming limitations in current culture systems to produce successful embryos. Because ethical and legal concerns limit the testing of newly designed culture systems directly on human embryos, research on primate and non-primate mammalian models plays a key role in translating findings to improve embryo culture systems and developmental competence and define useful markers for embryo selection in humans.

This Special Issue of Cells, “Recent Advancements in Mammalian Embryo Culture: From Animal Models to Humans”, aims to gather high-quality original research and review articles with a focus on any facet of pre-implantation embryo development in vitro and in vivo, with a particular interest in the following:

  • Fertilization;
  • IVF and embryo transfer;
  • Single and group embryo culture;
  • Dynamic embryo culture;
  • Milli and/or microfluidics;
  • ART outcomes;
  • Blastocyst;
  • Maternal reproductive tract;
  • Oviduct;
  • Uterus;
  • Exosomes;
  • Metabolomics;
  • Embryo morphokinetics;
  • Embryo selection;
  • Aneuploidy;
  • Pregnancy;
  • Epigenetics;
  • Omics;
  • Oxidative stress;
  • DNA damage and repair;
  • Use of novel/new antioxidants in reproductive biology;
  • Health of the progeny.

Prof. Roberto Gualtieri
Prof. Talevi Riccardo
Dr. Vincenza De Gregorio
Guest Editors

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Keywords

  • preimplantation embryo development
  • oviduct
  • fallopian tube
  • uterus
  • endometrium
  • culture system
  • milli/microfluidics
  • morphokinetics
  • metabolomics
  • exosomes
  • embryo selection
  • aneuploidy

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Published Papers (3 papers)

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Research

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16 pages, 2034 KiB  
Article
Controlled Dynamic Microfluidic Culture of Murine, Bovine, and Human Embryos Improves Development: Proof-of-Concept Studies
by Jose Roberto Alegretti, Andre M. Da Rocha, Naiara C. Nogueira-de-Souza, Nobuhiro Kato, Bruna C. Barros, Eduardo L. A. Motta, Paulo C. Serafini, Shuichi Takayama and Gary D. Smith
Cells 2024, 13(24), 2080; https://doi.org/10.3390/cells13242080 - 17 Dec 2024
Viewed by 1142
Abstract
Classical preimplantation embryo culture is performed in static fluid environments. Whether a dynamic fluid environment, like the fallopian tube, is beneficial for embryo development remains to be determined across mammalian species. Objectives of these proof-of-concept studies were to determine if controllable dynamic microfluidic [...] Read more.
Classical preimplantation embryo culture is performed in static fluid environments. Whether a dynamic fluid environment, like the fallopian tube, is beneficial for embryo development remains to be determined across mammalian species. Objectives of these proof-of-concept studies were to determine if controllable dynamic microfluidic culture would enhance preimplantation murine, bovine, and human embryo development compared to static culture. This prospective randomized controlled trial tested static versus controlled dynamic culture of preimplantation mouse (n = 397), bovine (n = 242), and human (n = 512) zygotes to blastocyst stages with outcome measures of embryo cleavage, cellular fragmentation, apoptosis, and blastocyst conversion rates. Dynamic culture of mouse and bovine zygotes with microfluidics significantly improved embryo development. Mouse placental imprinted gene expression was significantly different between embryos derived in vivo, by static culture, and by dynamic culture. Using human sibling zygotes, this dynamic microfluidic culture system increased the number of blastomeres per cleavage-stage embryo, reduced cellular fragmentation or apoptosis, improved blastocyst conversion rates, and enhanced blastocyst developmental stages. In conclusion, species-specific longitudinal studies demonstrated that dynamic microfluidic culture significantly improved embryo development, independent of culture media composition, temperature, and gaseous environment. These cellular indicators represent improved embryo development that can translate into higher pregnancy rates in transgenics, domestic livestock and endangered species and treating human infertility. Full article
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12 pages, 1371 KiB  
Article
Embryos from Prepubertal Hyperglycemic Female Mice Respond Differentially to Oxygen Tension In Vitro
by Dhakshanya Predheepan, Sujith Raj Salian, Shubhashree Uppangala, Vani Lakshmi R, Guruprasad Kalthur, Borut Kovačič and Satish Kumar Adiga
Cells 2024, 13(11), 954; https://doi.org/10.3390/cells13110954 - 30 May 2024
Cited by 1 | Viewed by 1184
Abstract
Reduced oxygen during embryo culture in human ART prevents embryo oxidative stress. Oxidative stress is also the major mechanism by which maternal diabetes impairs embryonic development. This study employed induced hyperglycemia prepubertal mice to mimic childhood diabetes to understand the effects of varying [...] Read more.
Reduced oxygen during embryo culture in human ART prevents embryo oxidative stress. Oxidative stress is also the major mechanism by which maternal diabetes impairs embryonic development. This study employed induced hyperglycemia prepubertal mice to mimic childhood diabetes to understand the effects of varying oxygen tension during in vitro embryonic development. The oocytes were fertilized and cultured at low (≈5%) oxygen (LOT) or atmospheric (≈20%) oxygen tension (HOT) for up to 96 h. Embryo development, apoptosis in blastocysts, inner cell mass (ICM) outgrowth proliferation, and Hif1α expression were assessed. Though the oocyte quality and meiotic spindle were not affected, the fertilization rate (94.86 ± 1.18 vs. 85.17 ± 2.81), blastocyst rate (80.92 ± 2.92 vs. 69.32 ± 2.54), and ICM proliferation ability (51.04 ± 9.22 vs. 17.08 ± 3.05) of the hyperglycemic embryos were significantly higher in the LOT compared to the HOT group. On the other hand, blastocysts from the hyperglycemic group, cultured at HOT, had a 1.5-fold increase in apoptotic cells compared to the control and lower Hif1α transcripts in ICM outgrowths compared to the LOT. Increased susceptibility of embryos from hyperglycemic mice to higher oxygen tension warrants the need to individualize the conditions for embryo culture systems in ART clinics, particularly when an endogenous maternal pathology affects the ovarian environment. Full article
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Review

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25 pages, 1089 KiB  
Review
In Vitro Culture of Mammalian Embryos: Is There Room for Improvement?
by Roberto Gualtieri, Vincenza De Gregorio, Andrea Candela, Angela Travaglione, Vincenzo Genovese, Vincenza Barbato and Riccardo Talevi
Cells 2024, 13(12), 996; https://doi.org/10.3390/cells13120996 - 7 Jun 2024
Cited by 8 | Viewed by 4083
Abstract
Preimplantation embryo culture, pivotal in assisted reproductive technology (ART), has lagged in innovation compared to embryo selection advancements. This review examines the persisting gap between in vivo and in vitro embryo development, emphasizing the need for improved culture conditions. While in humans this [...] Read more.
Preimplantation embryo culture, pivotal in assisted reproductive technology (ART), has lagged in innovation compared to embryo selection advancements. This review examines the persisting gap between in vivo and in vitro embryo development, emphasizing the need for improved culture conditions. While in humans this gap is hardly estimated, animal models, particularly bovines, reveal clear disparities in developmental competence, cryotolerance, pregnancy and live birth rates between in vitro-produced (IVP) and in vivo-derived (IVD) embryos. Molecular analyses unveil distinct differences in morphology, metabolism, and genomic stability, underscoring the need for refining culture conditions for better ART outcomes. To this end, a deeper comprehension of oviduct physiology and embryo transport is crucial for grasping embryo–maternal interactions’ mechanisms. Research on autocrine and paracrine factors, and extracellular vesicles in embryo–maternal tract interactions, elucidates vital communication networks for successful implantation and pregnancy. In vitro, confinement, and embryo density are key factors to boost embryo development. Advanced dynamic culture systems mimicking fluid mechanical stimulation in the oviduct, through vibration, tilting, and microfluidic methods, and the use of innovative softer substrates, hold promise for optimizing in vitro embryo development. Full article
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