Systematic review of mRNA expression in human oocytes: understanding the molecular mechanisms underlying oocyte competence.


Journal

Journal of assisted reproduction and genetics
ISSN: 1573-7330
Titre abrégé: J Assist Reprod Genet
Pays: Netherlands
ID NLM: 9206495

Informations de publication

Date de publication:
Oct 2023
Historique:
received: 26 02 2023
accepted: 02 08 2023
medline: 18 9 2023
pubmed: 10 8 2023
entrez: 9 8 2023
Statut: ppublish

Résumé

The biggest cell in the human body, the oocyte, encloses almost the complete machinery to start life. Despite all the research performed to date, defining oocyte quality is still a major goal of reproductive science. It is the consensus that mature oocytes are transcriptionally silent although, during their growth, the cell goes through stages of active transcription and translation, which will endow the oocyte with the competence to undergo nuclear maturation, and the oocyte and embryo to initiate timely translation before the embryonic genome is fully activated (cytoplasmic maturation). A systematic search was conducted across three electronic databases and the literature was critically appraised using the KMET score system. The aim was to identify quantitative differences in transcriptome of human oocytes that may link to patient demographics that could affect oocyte competence. Data was analysed following the principles of thematic analysis. Differences in the transcriptome were identified with respect to age or pathological conditions and affected chromosome mis segregation, perturbations of the nuclear envelope, premature maturation, and alterations in metabolic pathways-amongst others-in human oocytes.

Identifiants

pubmed: 37558907
doi: 10.1007/s10815-023-02906-9
pii: 10.1007/s10815-023-02906-9
pmc: PMC10504133
doi:

Substances chimiques

RNA, Messenger 0

Types de publication

Systematic Review Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

2283-2295

Informations de copyright

© 2023. The Author(s).

Références

Albertini DF, Telfer EE. Deconstructing the winding path to the recapitulation of mammalian oogenesis ex vivo. Proc Natl Acad Sci. 2016;113:9956–7.
doi: 10.1073/pnas.1610646113 pubmed: 27562166 pmcid: 5018762
Wu Y, Li M, Yang M. Post-Translational Modifications in Oocyte Maturation and Embryo Development. Front Cell Dev Biol. 2021;9:645318.
doi: 10.3389/fcell.2021.645318 pubmed: 34150752 pmcid: 8206635
Wu Y, Xu X, Qi M, Chen C, Li M, Yan R, et al. N6-methyladenosine regulates maternal RNA maintenance in oocytes and timely RNA decay during mouse maternal-to-zygotic transition. Nat Cell Biol. 2022;24:917–27.
doi: 10.1038/s41556-022-00915-x pubmed: 35606490
Wu D, Pedroza M, Chang J, Dean J. DIS3L2 ribonuclease degrades terminal-uridylated RNA to ensure oocyte maturation and female fertility. Nucleic Acids Res. 2023;51(7):3078–93. https://doi.org/10.1093/nar/gkad061 .
doi: 10.1093/nar/gkad061 pubmed: 36727488 pmcid: 10123098
Genome-wide analysis reveals a switch in the translational program upon oocyte meiotic resumption | Nucleic Acids Research | Oxford Academic [Internet]. [cited 2023 Apr 23].   https://academic.oup.com/nar/article/48/6/3257/5714267
Machlin JH, Shikanov A. Single-cell RNA-sequencing of retrieved human oocytes and eggs in clinical practice and for human ovarian cell atlasing. Mol Reprod Dev. 2022;89:597–607.
doi: 10.1002/mrd.23648 pubmed: 36264989 pmcid: 9805491
Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ. 2015;350:g7647.
doi: 10.1136/bmj.g7647 pubmed: 25555855
Kmet L, Lee R, Cook L. Standard quality assessment criteria for evaluating primary research papers from a variety of fields. 2004. https://doi.org/10.7939/R37M04F16
Ghaffari Novin M, Noruzinia M, Allahveisi A, Saremi A, Fadaei Fathabadi F, Mastery Farahani R, et al. Comparison of mitochondrial-related transcriptional levels of TFAM, NRF1 and MT-CO1 genes in single human oocytes at various stages of the oocyte maturation. Iran Biomed J. 2015;19:23–8.
pubmed: 25605486 pmcid: 4322229
Hoseini FS, Salsabili N, Akbari-Asbagh F, Aflatoonian R, Aghaee-Bakhtiari SH. Comparison of Gene Expression Profiles in Human Germinal Vesicle Before and After Cytoplasmic Transfer From Mature Oocytes in Iranian Infertile Couples. J Family Reprod Health. 2016;10:71–9.
pubmed: 27648096 pmcid: 5026671
Liu Q, Li Y, Feng Y, Liu C, Ma J, Li Y, et al. Single-cell analysis of differences in transcriptomic profiles of oocytes and cumulus cells at GV, MI, MII stages from PCOS patients. Sci Rep. 2016;6:39638.
doi: 10.1038/srep39638 pubmed: 28004769 pmcid: 5177934
Li M, Liu D, Wang L, Wang W, Wang A, Yao Y. Expression of placenta-specific 8 in human oocytes, embryos, and models of in vitro implantation. Fertil Steril. 2016;106:781–789.e2.
doi: 10.1016/j.fertnstert.2016.05.018 pubmed: 27322877
Barragán M, Pons J, Ferrer-Vaquer A, Cornet-Bartolomé D, Schweitzer A, Hubbard J, et al. The transcriptome of human oocytes is related to age and ovarian reserve. Mol Hum Reprod. 2017, cited 2022 Jun 6; 23.   https://pubmed.ncbi.nlm.nih.gov/28586423/
Canosa S, Adriaenssens T, Coucke W, Dalmasso P, Revelli A, Benedetto C, et al. Zona pellucida gene mRNA expression in human oocytes is related to oocyte maturity, zona inner layer retardance and fertilization competence. Mol Hum Reprod. 2017;23:292–303.
doi: 10.1093/molehr/gax008 pubmed: 28204536
Ruebel ML, Cotter M, Sims CR, Moutos DM, Badger TM, Cleves MA, et al. Obesity Modulates Inflammation and Lipid Metabolism Oocyte Gene Expression: A Single-Cell Transcriptome Perspective. J Clin Endocrinol Metab. 2017;102:2029–38.
doi: 10.1210/jc.2016-3524 pubmed: 28323970 pmcid: 5470765
Zhang Y, Yan Z, Qin Q, Nisenblat V, Chang H-M, Yu Y, et al. Transcriptome Landscape of Human Folliculogenesis Reveals Oocyte and Granulosa Cell Interactions. Mol Cell. 2018;72:1021–1034.e4.
doi: 10.1016/j.molcel.2018.10.029 pubmed: 30472193
Ferrero H, Corachán A, Aguilar A, Quiñonero A, Carbajo-García MC, Alamá P, et al. Single-cell RNA sequencing of oocytes from ovarian endometriosis patients reveals a differential transcriptomic profile associated with lower quality. Hum Reprod. 2019;34:1302–12.
doi: 10.1093/humrep/dez053 pubmed: 31211846
Zhao H, Li T, Zhao Y, Tan T, Liu C, Liu Y, et al. Single-Cell Transcriptomics of Human Oocytes: Environment-Driven Metabolic Competition and Compensatory Mechanisms During Oocyte Maturation. Antioxid Redox Signal. 2019;30:542–59.
doi: 10.1089/ars.2017.7151 pubmed: 29486586
Qi L, Liu B, Chen X, Liu Q, Li W, Lv B, et al. Single-Cell Transcriptomic Analysis Reveals Mitochondrial Dynamics in Oocytes of Patients With Polycystic Ovary Syndrome. Front Genet. 2020;11:396.
doi: 10.3389/fgene.2020.00396 pubmed: 32425983 pmcid: 7203476
Barone S, Sarogni P, Valli R, Pallotta MM, Silvia G, Frattini A, et al. Chromosome Missegregation in Single Human Oocytes Is Related to the Age and Gene Expression Profile. Int J Mol Sci. 2020;21:1934.
doi: 10.3390/ijms21061934 pubmed: 32178390 pmcid: 7139522
Yu B, Jayavelu ND, Battle SL, Mar JC, Schimmel T, Cohen J, et al. Single-cell analysis of transcriptome and DNA methylome in human oocyte maturation. PLoS One. 2020;15:e0241698.
doi: 10.1371/journal.pone.0241698 pubmed: 33152014 pmcid: 7643955
Yuan L, Yin P, Yan H, Zhong X, Ren C, Li K, et al. Single-cell transcriptome analysis of human oocyte ageing. J Cell Mol Med. 2021;25:6289–303.
doi: 10.1111/jcmm.16594 pubmed: 34037315 pmcid: 8256362
Llonch S, Barragán M, Nieto P, Mallol A, Elosua-Bayes M, Lorden P, et al. Single human oocyte transcriptome analysis reveals distinct maturation stage-dependent pathways impacted by age. Aging Cell. 2021;20:e13360.
doi: 10.1111/acel.13360 pubmed: 33908703 pmcid: 8135014
Braun V, Clarke V. Using thematic analysis in psychology. Qual Res Psychol. 2006;3:77–101.
doi: 10.1191/1478088706qp063oa
Translational regulation of the cell cycle: when, where, how and why? - PMC [Internet]. [cited 2023 Jul 14].   https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3203463/
Lemonnier T, Dupré A, Jessus C. The G2-to-M transition from a phosphatase perspective: a new vision of the meiotic division. Cell Div. 2020;15:9.
doi: 10.1186/s13008-020-00065-2 pubmed: 32508972 pmcid: 7249327
Del Llano E, Iyyappan R, Aleshkina D, Masek T, Dvoran M, Jiang Z, et al. SGK1 is essential for meiotic resumption in mammalian oocytes. Eur J Cell Biol. 2022;101:151210.
doi: 10.1016/j.ejcb.2022.151210 pubmed: 35240557
Machtinger R, Combelles CMH, Missmer SA, Correia KF, Fox JH, Racowsky C. The association between severe obesity and characteristics of failed fertilized oocytes. Hum Reprod. 2012;27:3198–207.
doi: 10.1093/humrep/des308 pubmed: 22968161
Li L, Baibakov B, Dean J. A subcortical maternal complex essential for preimplantation mouse embryogenesis. Dev Cell. 2008;15:416–25.
doi: 10.1016/j.devcel.2008.07.010 pubmed: 18804437 pmcid: 2597058
Imanaka S, Shigetomi H, Kobayashi H. Reprogramming of glucose metabolism of cumulus cells and oocytes and its therapeutic significance. Reprod Sci. 2022;29:653–67.
doi: 10.1007/s43032-021-00505-6 pubmed: 33675030
The G-protein-coupled receptors GPR3 and GPR12 are involved in cAMP signaling and maintenance of meiotic arrest in rodent oocytes - ScienceDirect [Internet]. [cited 2023 Apr 22].   https://www.sciencedirect.com/science/article/pii/S0012160605005476
Molecular and Cellular Mechanisms of Sperm-Oocyte Interactions Opinions Relative to in Vitro Fertilization (IVF) - PMC [Internet]. [cited 2023 Jul 14].   https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4139886/
Tesarik J. Control of Maternal-to-Zygotic Transition in Human Embryos and Other Animal Species (Especially Mouse): Similarities and Differences. Int J Mol Sci. 2022;23:8562.
doi: 10.3390/ijms23158562 pubmed: 35955697 pmcid: 9369289
te Velde ER, Pearson PL. The variability of female reproductive ageing. Hum Reprod Update. 2002;8:141–54.
doi: 10.1093/humupd/8.2.141
Kristensen SG, Pors SE, Andersen CY. Improving oocyte quality by transfer of autologous mitochondria from fully grown oocytes. Hum Reprod. 2017;32:725–32.
pubmed: 28333265
Chiaratti MR, Garcia BM, Carvalho KF, Macabelli CH, Ribeiro FK d S, Zangirolamo AF, et al. Oocyte mitochondria: role on fertility and disease transmission. Anim Reprod. 2018;15:231–8.
doi: 10.21451/1984-3143-AR2018-0069 pubmed: 34178146 pmcid: 8202466
Deng K, Du D, Fan D, Pei Z, Zhang S, Xu C. Growth Hormone Promotes Oocyte Maturation In Vitro by Protecting Mitochondrial Function and Reducing Apoptosis. Reprod Sci. 2023;30(7):2219–30. https://doi.org/10.1007/s43032-022-01147-y .
doi: 10.1007/s43032-022-01147-y pubmed: 36694082
Vuong LN, Le AH, Ho VNA, Pham TD, Sanchez F, Romero S, et al. Live births after oocyte in vitro maturation with a prematuration step in women with polycystic ovary syndrome. J Assist Reprod Genet. 2020;37:347–57.
doi: 10.1007/s10815-019-01677-6 pubmed: 31902102 pmcid: 7056678
Richani D, Gilchrist RB. Approaches to oocyte meiotic arrest in vitro and impact on oocyte developmental competence. Biol Reprod. 2022;106:243–52.
doi: 10.1093/biolre/ioab176 pubmed: 34534265
Gilchrist RB, Smitz J. Oocyte in vitro maturation: physiological basis and application to clinical practice. Fertil Steril. 2023;119:524–39.
doi: 10.1016/j.fertnstert.2023.02.010 pubmed: 36804961
Hu W, Zeng H, Shi Y, Zhou C, Huang J, Jia L, et al. Single-cell transcriptome and translatome dual-omics reveals potential mechanisms of human oocyte maturation. Nat Commun. 2022;13:5114.
doi: 10.1038/s41467-022-32791-2 pubmed: 36042231 pmcid: 9427852

Auteurs

Xavier Viñals Gonzalez (XV)

Institute for Women's Health, Preimplantation Genetics Group, University College London, 84-86 Chenies Mews, Bloomsbury, London, WC1E 6HU, UK. xavier.gonzalez.18@ucl.ac.uk.

Arwa Almutlaq (A)

Institute for Women's Health, Preimplantation Genetics Group, University College London, 84-86 Chenies Mews, Bloomsbury, London, WC1E 6HU, UK.

Sioban Sen Gupta (SS)

Institute for Women's Health, Preimplantation Genetics Group, University College London, 84-86 Chenies Mews, Bloomsbury, London, WC1E 6HU, UK.

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