Rescue in vitro maturation using ovarian support cells of human oocytes from conventional stimulation cycles yields oocytes with improved nuclear maturation and transcriptomic resemblance to in vivo matured oocytes

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Abstract

Purpose

Determine if the gene expression profiles of ovarian support cells (OSCs) and cumulus-free oocytes are bidirectionally influenced by co-culture during in vitro maturation (IVM).

Methods

Fertility patients aged 25 to 45 years old undergoing conventional ovarian stimulation donated denuded immature oocytes for research. Oocytes were randomly allocated to either OSC-IVM culture (intervention) or Media-IVM culture (control) for 24–28 h. The OSC-IVM culture condition was composed of 100,000 OSCs in suspension culture with human chorionic gonadotropin (hCG), recombinant follicle stimulating hormone (rFSH), androstenedione, and doxycycline supplementation. The Media-IVM control lacked OSCs and contained the same supplementation. A limited set of in vivo matured MII oocytes were donated for comparative evaluation. Endpoints consisted of MII formation rate, morphological and spindle quality assessment, and gene expression analysis compared to in vitro and in vivo controls.

Results

OSC-IVM resulted in a statistically significant improvement in MII formation rate compared to the Media-IVM control, with no apparent effect on morphology or spindle assembly. OSC-IVM MII oocytes displayed a closer transcriptomic maturity signature to IVF-MII controls than Media-IVM control MII oocytes. The gene expression profile of OSCs was modulated in the presence of oocytes, displaying culture- and time-dependent differential gene expression during IVM.

Conclusion

The OSC-IVM platform is a novel tool for rescue maturation of human oocytes, yielding oocytes with improved nuclear maturation and a closer transcriptomic resemblance to in vivo matured oocytes, indicating a potential enhancement in oocyte cytoplasmic maturation. These improvements on oocyte quality after OSC-IVM are possibly occurring through bidirectional crosstalk of cumulus-free oocytes and ovarian support cells.

Supplementary Information

The online version contains supplementary material available at 10.1007/s10815-024-03143-4.

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Most cited references 62

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STAR: ultrafast universal RNA-seq aligner.

Alexander Dobin, Carrie A. Davis, Felix Schlesinger … (2013)

Accurate alignment of high-throughput RNA-seq data is a challenging and yet unsolved problem because of the non-contiguous transcript structure, relatively short read lengths and constantly increasing throughput of the sequencing technologies. Currently available RNA-seq aligners suffer from high mapping error rates, low mapping speed, read length limitation and mapping biases. To align our large (>80 billon reads) ENCODE Transcriptome RNA-seq dataset, we developed the Spliced Transcripts Alignment to a Reference (STAR) software based on a previously undescribed RNA-seq alignment algorithm that uses sequential maximum mappable seed search in uncompressed suffix arrays followed by seed clustering and stitching procedure. STAR outperforms other aligners by a factor of >50 in mapping speed, aligning to the human genome 550 million 2 × 76 bp paired-end reads per hour on a modest 12-core server, while at the same time improving alignment sensitivity and precision. In addition to unbiased de novo detection of canonical junctions, STAR can discover non-canonical splices and chimeric (fusion) transcripts, and is also capable of mapping full-length RNA sequences. Using Roche 454 sequencing of reverse transcription polymerase chain reaction amplicons, we experimentally validated 1960 novel intergenic splice junctions with an 80-90% success rate, corroborating the high precision of the STAR mapping strategy. STAR is implemented as a standalone C++ code. STAR is free open source software distributed under GPLv3 license and can be downloaded from http://code.google.com/p/rna-star/.

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SCANPY : large-scale single-cell gene expression data analysis

F. Alexander Wolf, Philipp Angerer, Fabian Theis (2018)

Scanpy is a scalable toolkit for analyzing single-cell gene expression data. It includes methods for preprocessing, visualization, clustering, pseudotime and trajectory inference, differential expression testing, and simulation of gene regulatory networks. Its Python-based implementation efficiently deals with data sets of more than one million cells (https://github.com/theislab/Scanpy). Along with Scanpy, we present AnnData, a generic class for handling annotated data matrices (https://github.com/theislab/anndata).

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Mitochondrial electron transport chain, ROS generation and uncoupling (Review)

Ru-Zhou Zhao, Shuai Jiang, Lin Zhang … (2019)

The mammalian mitochondrial electron transport chain (ETC) includes complexes I-IV, as well as the electron transporters ubiquinone and cytochrome c. There are two electron transport pathways in the ETC: Complex I/III/IV, with NADH as the substrate and complex II/III/IV, with succinic acid as the substrate. The electron flow is coupled with the generation of a proton gradient across the inner membrane and the energy accumulated in the proton gradient is used by complex V (ATP synthase) to produce ATP. The first part of this review briefly introduces the structure and function of complexes I-IV and ATP synthase, including the specific electron transfer process in each complex. Some electrons are directly transferred to O2 to generate reactive oxygen species (ROS) in the ETC. The second part of this review discusses the sites of ROS generation in each ETC complex, including sites IF and IQ in complex I, site IIF in complex II and site IIIQo in complex III, and the physiological and pathological regulation of ROS. As signaling molecules, ROS play an important role in cell proliferation, hypoxia adaptation and cell fate determination, but excessive ROS can cause irreversible cell damage and even cell death. The occurrence and development of a number of diseases are closely related to ROS overproduction. Finally, proton leak and uncoupling proteins (UCPS) are discussed. Proton leak consists of basal proton leak and induced proton leak. Induced proton leak is precisely regulated and induced by UCPs. A total of five UCPs (UCP1-5) have been identified in mammalian cells. UCP1 mainly plays a role in the maintenance of body temperature in a cold environment through non-shivering thermogenesis. The core role of UCP2-5 is to reduce oxidative stress under certain conditions, therefore exerting cytoprotective effects. All diseases involving oxidative stress are associated with UCPs.

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Author and article information

Contributors

Christian C. Kramme:

ORCID: http://orcid.org/0000-0002-7518-8111

christian@gametogen.com

Journal

Journal ID (nlm-ta): J Assist Reprod Genet

Journal ID (iso-abbrev): J Assist Reprod Genet

Title: Journal of Assisted Reproduction and Genetics

Publisher: Springer US (New York )

ISSN (Print): 1058-0468

ISSN (Electronic): 1573-7330

Publication date (Electronic): 30 May 2024

Publication date PMC-release: 30 May 2024

Publication date (Print): August 2024

Volume: 41

Issue: 8

Pages: 2021-2036

Affiliations

[1 ]Gameto Inc., 430 E. 29th St Fl 14, New York, NY 10016 USA

[2 ]Obstetrics, Gynecology, and Reproductive Science, Icahn School of Medicine at Mount Sinai, ( https://ror.org/04a9tmd77) New York, NY USA

[3 ]Extend Fertility, New York, NY USA

[4 ]KEW Technology, Seattle, WA USA

[5 ]Ruber Juan Bravo University Hospital, Eugin Group, Madrid, Spain

[6 ]Reproductive Medicine Associates of New York, ( https://ror.org/03xswyc88) New York, NY USA

[7 ]GRID grid.38142.3c, ISNI 000000041936754X, Wyss Institute, Harvard Medical School, ; Boston, MA USA

[8 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Genetics, , Harvard Medical School, ; Boston, MA USA

[9 ]Department of Biomedical Engineering, Duke University, ( https://ror.org/00py81415) Durham, NC USA

[10 ]Department of Computer Science, Duke University, ( https://ror.org/00py81415) Durham, NC USA

Author information

Christian C. Kramme http://orcid.org/0000-0002-7518-8111

Article

Publisher ID: 3143

DOI: 10.1007/s10815-024-03143-4

PMC ID: 11339229

PubMed ID: 38814543

SO-VID: 5eda8d03-4af2-4118-9701-ff72f76590e4

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 10 August 2023

Date accepted : 9 May 2024

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ScienceOpen disciplines: Genetics

Keywords: ovarian support cells,in vitro maturation,stem cells,oocyte transcriptomics,granulosa cells

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ScienceOpen disciplines: Genetics

Keywords: ovarian support cells, in vitro maturation, stem cells, oocyte transcriptomics, granulosa cells

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Rescue in vitro maturation using ovarian support cells of human oocytes from conventional stimulation cycles yields oocytes with improved nuclear maturation and transcriptomic resemblance to in vivo matured oocytes

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Abstract

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Conclusion

Supplementary Information

Related collections

Universal stem cells

Most cited references 62

STAR: ultrafast universal RNA-seq aligner.

SCANPY : large-scale single-cell gene expression data analysis

Mitochondrial electron transport chain, ROS generation and uncoupling (Review)

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